Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Temozolomide: An Updated Overview of Resistance Mechanisms, Nanotechnology Advances and Clinical Applications

Author(s): Raúl Ortiz, Gloria Perazzoli, Laura Cabeza, Cristina Jiménez-Luna, Raquel Luque, Jose Prados* and Consolación Melguizo

Volume 19, Issue 4, 2021

Published on: 26 June, 2020

Page: [513 - 537] Pages: 25

DOI: 10.2174/1570159X18666200626204005

Price: $65

Abstract

Temozolomide (TMZ), an oral alkylating prodrug which delivers a methyl group to purine bases of DNA (O6-guanine; N7-guanine and N3-adenine), is frequently used together with radiotherapy as part of the first-line treatment of high-grade gliomas. The main advantages are its high oral bioavailability (almost 100% although the concentration found in the cerebrospinal fluid was approximately 20% of the plasma concentration of TMZ), its lipophilic properties, and small size that confer the ability to cross the blood-brain barrier. Furthermore, this agent has demonstrated activity not only in brain tumors but also in a variety of solid tumors. However, conventional therapy using surgery, radiation, and TMZ in glioblastoma results in a median patient survival of 14.6 months. Treatment failure has been associated with tumor drug resistance. This phenomenon has been linked to the expression of O6-methylguanine-DNA methyltransferase, but the mismatch repair system and the presence of cancer stem-like cells in tumors have also been related to TMZ resistance. The understanding of these mechanisms is essential for the development of new therapeutic strategies in the clinical use of TMZ, including the use of nanomaterial delivery systems and the association with other chemotherapy agents. The aim of this review is to summarize the resistance mechanisms of TMZ and the current advances to improve its clinical use.

Keywords: Alkylating agents, drug resistance, chemotherapy, nanoparticles, cancer, clinical trials.

Graphical Abstract
[1]
Mutter, N.; Stupp, R. Temozolomide: a milestone in neuro-oncology and beyond? Expert Rev. Anticancer Ther., 2006, 6(8), 1187-1204.
[http://dx.doi.org/10.1586/14737140.6.8.1187] [PMID: 16925485]
[2]
Thomas, A.; Tanaka, M.; Trepel, J.; Reinhold, W.C.; Rajapakse, V.N.; Pommier, Y. Temozolomide in the era of precision medicine. Cancer Res., 2017, 77(4), 823-826.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2983] [PMID: 28159862]
[3]
Zhang, J.; Stevens, M.F.G.; Bradshaw, T.D. Temozolomide: mechanisms of action, repair and resistance. Curr. Mol. Pharmacol., 2012, 5(1), 102-114.
[http://dx.doi.org/10.2174/1874467211205010102] [PMID: 22122467]
[4]
Denny, B.J.; Wheelhouse, R.T.; Stevens, M.F.G.; Tsang, L.L.H.; Slack, J.A. NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA. Biochemistry, 1994, 33(31), 9045-9051.
[http://dx.doi.org/10.1021/bi00197a003] [PMID: 8049205]
[5]
Ramalho, M.J.; Andrade, S.; Coelho, M.A.N.; Loureiro, J.A.; Pereira, M.C. Biophysical interaction of temozolomide and its active metabolite with biomembrane models: The relevance of drug-membrane interaction for glioblastoma multiforme therapy. Eur. J. Pharm. Biopharm., 2019, 136, 156-163.
[http://dx.doi.org/10.1016/j.ejpb.2019.01.015] [PMID: 30682492]
[6]
Stéphanou, A.; Ballesta, A. pH as a potential therapeutic target to improve temozolomide antitumor efficacy: A mechanistic modeling study. Pharmacol. Res. Perspect., 2019, 7(1), e00454.
[7]
Pawlowska, E.; Szczepanska, J.; Szatkowska, M.; Blasiak, J. An Interplay between senescence, apoptosis and autophagy in glioblastoma multiforme-role in pathogenesis and therapeutic perspective. Int. J. Mol. Sci., 2018, 19(3), 889.
[http://dx.doi.org/10.3390/ijms19030889] [PMID: 29562589]
[8]
Patel, M.; McCully, C.; Godwin, K.; Balis, F.M. Plasma and cerebrospinal fluid pharmacokinetics of intravenous temozolomide in non-human primates. J. Neurooncol., 2003, 61(3), 203-207.
[http://dx.doi.org/10.1023/A:1022592913323] [PMID: 12675312]
[9]
Ostermann, S.; Csajka, C.; Buclin, T.; Leyvraz, S.; Lejeune, F.; Decosterd, L.A.; Stupp, R. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin. Cancer Res., 2004, 10(11), 3728-3736.
[http://dx.doi.org/10.1158/1078-0432.CCR-03-0807] [PMID: 15173079]
[10]
Liu, H.L.; Huang, C.Y.; Chen, J.Y.; Wang, H.Y.; Chen, P.Y.; Wei, K.C. Pharmacodynamic and therapeutic investigation of focused ultrasound-induced blood-brain barrier opening for enhanced temozolomide delivery in glioma treatment. PLoS One, 2014, 9(12), e114311.
[http://dx.doi.org/10.1371/journal.pone.0114311] [PMID: 25490097]
[11]
Martínez-Garcia, M.; Álvarez-Linera, J.; Carrato, C.; Ley, L.; Luque, R.; Maldonado, X.; Martínez-Aguillo, M.; Navarro, L.M.; Vaz-Salgado, M.A.; Gil-Gil, M. SEOM clinical guidelines for diagnosis and treatment of glioblastoma (2017). Clin. Transl. Oncol., 2018, 20(1), 22-28.
[http://dx.doi.org/10.1007/s12094-017-1763-6] [PMID: 29086250]
[12]
Kong, D.S.; Lee, J.I.; Kim, J.H.; Kim, S.T.; Kim, W.S.; Suh, Y.L.; Dong, S.M.; Nam, D.H. Phase II trial of low-dose continuous (metronomic) treatment of temozolomide for recurrent glioblastoma. Neuro-oncol., 2010, 12(3), 289-296.
[http://dx.doi.org/10.1093/neuonc/nop030] [PMID: 20167817]
[13]
Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.B.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K.; Hau, P.; Brandes, A.A.; Gijtenbeek, J.; Marosi, C.; Vecht, C.J.; Mokhtari, K.; Wesseling, P.; Villa, S.; Eisenhauer, E.; Gorlia, T.; Weller, M.; Lacombe, D.; Cairncross, J.G.; Mirimanoff, R.O. European organisation for research and treatment of cancer brain tumour and radiation oncology groups; National Cancer Institute of Canada Clinical Trials Group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol., 2009, 10(5), 459-466.
[http://dx.doi.org/10.1016/S1470-2045(09)70025-7] [PMID: 19269895]
[14]
Lin, A.J.; Campian, J.L.; Hui, C.; Rudra, S.; Rao, Y.J.; Thotala, D.; Hallahan, D.; Huang, J. Impact of concurrent versus adjuvant chemotherapy on the severity and duration of lymphopenia in glioma patients treated with radiation therapy. J. Neurooncol., 2018, 136(2), 403-411.
[http://dx.doi.org/10.1007/s11060-017-2668-5] [PMID: 29143923]
[15]
Karachi, A.; Dastmalchi, F.; Mitchell, D.A.; Rahman, M. Temozolomide for immunomodulation in the treatment of glioblastoma. Neuro-oncol., 2018, 20(12), 1566-1572.
[http://dx.doi.org/10.1093/neuonc/noy072] [PMID: 29733389]
[16]
Campian, J.L.; Ye, X.; Gladstone, D.E.; Ambady, P.; Nirschl, T.R.; Borrello, I.; Golightly, M.; King, K.E.; Holdhoff, M.; Karp, J.; Drake, C.G.; Grossman, S.A. Pre-radiation lymphocyte harvesting and post-radiation reinfusion in patients with newly diagnosed high grade gliomas. J. Neurooncol., 2015, 124(2), 307-316.
[http://dx.doi.org/10.1007/s11060-015-1841-y] [PMID: 26070554]
[17]
Su, Y.B.; Sohn, S.; Krown, S.E.; Livingston, P.O.; Wolchok, J.D.; Quinn, C.; Williams, L.; Foster, T.; Sepkowitz, K.A.; Chapman, P.B. Selective CD4+ lymphopenia in melanoma patients treated with temozolomide: a toxicity with therapeutic implications. J. Clin. Oncol., 2004, 22(4), 610-616.
[http://dx.doi.org/10.1200/JCO.2004.07.060] [PMID: 14726505]
[18]
Wick, W.; Steinbach, J.P.; Küker, W.M.; Dichgans, J.; Bamberg, M.; Weller, M. One week on/one week off: a novel active regimen of temozolomide for recurrent glioblastoma. Neurology, 2004, 62(11), 2113-2115.
[http://dx.doi.org/10.1212/01.WNL.0000127617.89363.84] [PMID: 15184628]
[19]
Khan, B.A.; Khan, S.; White, B.; Eranki, A. Severe pneumocystis jiroveci pneumonia in a patient on temozolomide therapy: A case report and review of literature. Respir. Med. Case Rep., 2017, 22, 179-182.
[http://dx.doi.org/10.1016/j.rmcr.2017.08.012] [PMID: 28861334]
[20]
Akasaki, Y.; Kikuchi, T.; Homma, S.; Koido, S.; Ohkusa, T.; Tasaki, T.; Hayashi, K.; Komita, H.; Watanabe, N.; Suzuki, Y.; Yamamoto, Y.; Mori, R.; Arai, T.; Tanaka, T.; Joki, T.; Yanagisawa, T.; Murayama, Y. Phase I/II trial of combination of temozolomide chemotherapy and immunotherapy with fusions of dendritic and glioma cells in patients with glioblastoma. Cancer Immunol. Immunother., 2016, 65(12), 1499-1509.
[http://dx.doi.org/10.1007/s00262-016-1905-7] [PMID: 27688162]
[21]
Geffen, D.B.; Man, S. New drugs for the treatment of cancer, 1990-2001. Isr. Med. Assoc. J., 2002, 4(12), 1124-1131.
[PMID: 12516906]
[22]
Yan, Y.; Xu, Z.; Dai, S.; Qian, L.; Sun, L.; Gong, Z. Targeting autophagy to sensitive glioma to temozolomide treatment. J. Exp. Clin. Cancer Res., 2016, 35, 23.
[http://dx.doi.org/10.1186/s13046-016-0303-5] [PMID: 26830677]
[23]
Abbott, N.J. Blood-brain barrier structure and function and the challenges for CNS drug delivery. J. Inherit. Metab. Dis., 2013, 36(3), 437-449.
[http://dx.doi.org/10.1007/s10545-013-9608-0] [PMID: 23609350]
[24]
Hartz, A.M.S.; Bauer, B. ABC transporters in the CNS - an inventory. Curr. Pharm. Biotechnol., 2011, 12(4), 656-673.
[http://dx.doi.org/10.2174/138920111795164020] [PMID: 21118088]
[25]
Miller, D.S. Regulation of ABC transporters blood-brain barrier: the good, the bad, and the ugly. Adv. Cancer Res., 2015, 125, 43-70.
[http://dx.doi.org/10.1016/bs.acr.2014.10.002] [PMID: 25640266]
[26]
Su, B.; Wang, R.; Xie, Z.; Ruan, H.; Li, J.; Xie, C.; Lu, W.; Wang, J.; Wang, D.; Liu, M. Effect of retro-inverso isomer of bradykinin on size-dependent penetration of blood-brain tumor barrier. Small, 2018, 14(7)
[http://dx.doi.org/10.1002/smll.201702331] [PMID: 29292579]
[27]
van Tellingen, O.; Yetkin-Arik, B.; de Gooijer, M.C.; Wesseling, P.; Wurdinger, T.; de Vries, H.E. Overcoming the blood-brain tumor barrier for effective glioblastoma treatment. Drug Resist. Updat., 2015, 19, 1-12.
[http://dx.doi.org/10.1016/j.drup.2015.02.002] [PMID: 25791797]
[28]
Marchesi, F.; Turriziani, M.; Tortorelli, G.; Avvisati, G.; Torino, F.; De Vecchis, L. Triazene compounds: mechanism of action and related DNA repair systems. Pharmacol. Res., 2007, 56(4), 275-287.
[http://dx.doi.org/10.1016/j.phrs.2007.08.003] [PMID: 17897837]
[29]
Blough, M.D.; Zlatescu, M.C.; Cairncross, J.G. O6-methylguanine-DNA methyltransferase regulation by p53 in astrocytic cells. Cancer Res., 2007, 67(2), 580-584.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-2782] [PMID: 17234766]
[30]
Esteller, M.; Hamilton, S.R.; Burger, P.C.; Baylin, S.B.; Herman, J.G. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res., 1999, 59(4), 793-797.
[PMID: 10029064]
[31]
Kitange, G.J.; Carlson, B.L.; Schroeder, M.A.; Grogan, P.T.; Lamont, J.D.; Decker, P.A.; Wu, W.; James, C.D.; Sarkaria, J.N. Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro-oncol., 2009, 11(3), 281-291.
[http://dx.doi.org/10.1215/15228517-2008-090] [PMID: 18952979]
[32]
Weller, M.; Stupp, R.; Reifenberger, G.; Brandes, A.A.; van den Bent, M.J.; Wick, W.; Hegi, M.E. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat. Rev. Neurol., 2010, 6(1), 39-51.
[http://dx.doi.org/10.1038/nrneurol.2009.197] [PMID: 19997073]
[33]
Esteller, M.; Garcia-Foncillas, J.; Andion, E.; Goodman, S.N.; Hidalgo, O.F.; Vanaclocha, V.; Baylin, S.B.; Herman, J.G. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med., 2000, 343(19), 1350-1354.
[http://dx.doi.org/10.1056/NEJM200011093431901] [PMID: 11070098]
[34]
Thon, N.; Kreth, S.; Kreth, F.W. Personalized treatment strategies in glioblastoma: MGMT promoter methylation status. OncoTargets Ther., 2013, 6, 1363-1372.
[http://dx.doi.org/10.2147/OTT.S50208] [PMID: 24109190]
[35]
Parker, N.R.; Khong, P.; Parkinson, J.F.; Howell, V.M.; Wheeler, H.R. Molecular heterogeneity in glioblastoma: potential clinical implications. Front. Oncol., 2015, 5, 55.
[http://dx.doi.org/10.3389/fonc.2015.00055] [PMID: 25785247]
[36]
Perazzoli, G.; Prados, J.; Ortiz, R.; Caba, O.; Cabeza, L.; Berdasco, M.; Gónzalez, B.; Melguizo, C. Temozolomide resistance in glioblastoma cell lines: implication of MGMT, MMR, P-Glycoprotein and CD133 expression. PLoS One, 2015, 10(10), e0140131.
[http://dx.doi.org/10.1371/journal.pone.0140131] [PMID: 26447477]
[37]
Hegi, M.E.; Diserens, A.C.; Gorlia, T.; Hamou, M.F.; de Tribolet, N.; Weller, M.; Kros, J.M.; Hainfellner, J.A.; Mason, W.; Mariani, L.; Bromberg, J.E.; Hau, P.; Mirimanoff, R.O.; Cairncross, J.G.; Janzer, R.C.; Stupp, R. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med., 2005, 352(10), 997-1003.
[http://dx.doi.org/10.1056/NEJMoa043331] [PMID: 15758010]
[38]
Hegi, M.E.; Diserens, A.C.; Godard, S.; Dietrich, P.Y.; Regli, L.; Ostermann, S.; Otten, P.; Van Melle, G.; de Tribolet, N.; Stupp, R. Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin. Cancer Res., 2004, 10(6), 1871-1874.
[http://dx.doi.org/10.1158/1078-0432.CCR-03-0384] [PMID: 15041700]
[39]
Taylor, J.W.; Schiff, D. Treatment considerations for MGMT-unmethylated glioblastoma. Curr. Neurol. Neurosci. Rep., 2015, 15(1), 507.
[http://dx.doi.org/10.1007/s11910-014-0507-z] [PMID: 25394859]
[40]
Weller, M.; van den Bent, M.; Hopkins, K.; Tonn, J.C.; Stupp, R.; Falini, A.; Cohen-Jonathan-Moyal, E.; Frappaz, D.; Henriksson, R.; Balana, C.; Chinot, O.; Ram, Z.; Reifenberger, G.; Soffietti, R.; Wick, W. European Association for Neuro-Oncology (EANO) Task Force on Malignant Glioma. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol., 2014, 15(9), e395-e403.
[http://dx.doi.org/10.1016/S1470-2045(14)70011-7] [PMID: 25079102]
[41]
Spiegl-Kreinecker, S.; Pirker, C.; Filipits, M.; Lötsch, D.; Buchroithner, J.; Pichler, J.; Silye, R.; Weis, S.; Micksche, M.; Fischer, J.; Berger, W. O6-Methylguanine DNA methyltransferase protein expression in tumor cells predicts outcome of temozolomide therapy in glioblastoma patients. Neuro-oncol., 2010, 12(1), 28-36.
[http://dx.doi.org/10.1093/neuonc/nop003] [PMID: 20150365]
[42]
Brandes, A.A.; Tosoni, A.; Franceschi, E.; Reni, M.; Gatta, G.; Vecht, C. Glioblastoma in adults. Crit. Rev. Oncol. Hematol., 2008, 67(2), 139-152.
[http://dx.doi.org/10.1016/j.critrevonc.2008.02.005] [PMID: 18394916]
[43]
Weller, M.; Felsberg, J.; Hartmann, C.; Berger, H.; Steinbach, J.P.; Schramm, J.; Westphal, M.; Schackert, G.; Simon, M.; Tonn, J.C.; Heese, O.; Krex, D.; Nikkhah, G.; Pietsch, T.; Wiestler, O.; Reifenberger, G.; von Deimling, A.; Loeffler, M. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J. Clin. Oncol., 2009, 27(34), 5743-5750.
[http://dx.doi.org/10.1200/JCO.2009.23.0805] [PMID: 19805672]
[44]
Dahlrot, R.H.; Dowsett, J.; Fosmark, S.; Malmström, A.; Henriksson, R.; Boldt, H.; de Stricker, K.; Sørensen, M.D.; Poulsen, H.S.; Lysiak, M.; Söderkvist, P.; Rosell, J.; Hansen, S.; Kristensen, B.W. Prognostic value of O-6-methylguanine-DNA methyltransferase (MGMT) protein expression in glioblastoma excluding nontumour cells from the analysis. Neuropathol. Appl. Neurobiol., 2018, 44(2), 172-184.
[http://dx.doi.org/10.1111/nan.12415] [PMID: 28574607]
[45]
Radke, J.; Koch, A.; Pritsch, F.; Schumann, E.; Misch, M.; Hempt, C.; Lenz, K.; Löbel, F.; Paschereit, F.; Heppner, F.L.; Vajkoczy, P.; Koll, R.; Onken, J. Predictive MGMT status in a homogeneous cohort of IDH wildtype glioblastoma patients. Acta Neuropathol. Commun., 2019, 7(1), 89.
[http://dx.doi.org/10.1186/s40478-019-0745-z] [PMID: 31167648]
[46]
Schaff, L.R.; Yan, D.; Thyparambil, S.; Tian, Y.; Cecchi, F.; Rosenblum, M.; Reiner, A.S.; Panageas, K.S.; Hembrough, T.; Lin, A.L. Characterization of MGMT and EGFR protein expression in glioblastoma and association with survival. J. Neurooncol., 2020, 146(1), 163-170.
[http://dx.doi.org/10.1007/s11060-019-03358-x] [PMID: 31823165]
[47]
Marton, E.; Giordan, E.; Siddi, F.; Curzi, C.; Canova, G.; Scarpa, B.; Guerriero, A.; Rossi, S.; D’ Avella, D.; Longatti, P.; Feletti, A. Over ten years overall survival in glioblastoma: A different disease? J. Neurol. Sci., 2020, 408, 116518.
[http://dx.doi.org/10.1016/j.jns.2019.116518] [PMID: 31715330]
[48]
Hegi, M.E.; Liu, L.; Herman, J.G.; Stupp, R.; Wick, W.; Weller, M.; Mehta, M.P.; Gilbert, M.R. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J. Clin. Oncol., 2008, 26(25), 4189-4199.
[http://dx.doi.org/10.1200/JCO.2007.11.5964] [PMID: 18757334]
[49]
Wick, W.; Stupp, R.; Beule, A.C.; Bromberg, J.; Wick, A.; Ernemann, U.; Platten, M.; Marosi, C.; Mason, W.P.; van den Bent, M.; Weller, M.; Rorden, C.; Karnath, H.O. European Organisation for Research and Treatment of Cancer and the National Cancer Institute of Canada Clinical Trials Group. A novel tool to analyze MRI recurrence patterns in glioblastoma. Neuro-oncol., 2008, 10(6), 1019-1024.
[http://dx.doi.org/10.1215/15228517-2008-058] [PMID: 18676355]
[50]
Dahlrot, R.H.; Larsen, P.; Boldt, H.B.; Kreutzfeldt, M.S.; Hansen, S.; Hjelmborg, J.B.; Kristensen, B.W. Post treatment effect of MGMT methylation level on glioblastoma survival. J. Neuropathol. Exp. Neurol., 2019, 78(7), 633-640.
[http://dx.doi.org/10.1093/jnen/nlz032] [PMID: 31058280]
[51]
Felsberg, J.; Thon, N.; Eigenbrod, S.; Hentschel, B.; Sabel, M.C.; Westphal, M.; Schackert, G.; Kreth, F.W.; Pietsch, T.; Löffler, M.; Weller, M.; Reifenberger, G.; Tonn, J.C. German Glioma Network. Promoter methylation and expression of MGMT and the DNA mismatch repair genes MLH1, MSH2, MSH6 and PMS2 in paired primary and recurrent glioblastomas. Int. J. Cancer, 2011, 129(3), 659-670.
[http://dx.doi.org/10.1002/ijc.26083] [PMID: 21425258]
[52]
Karsy, M.; Neil, J.A.; Guan, J.; Mahan, M.A.; Colman, H.; Jensen, R.L.; Jensen, R.L. A practical review of prognostic correlations of molecular biomarkers in glioblastoma. Neurosurg. Focus, 2015, 38(3), E4.
[http://dx.doi.org/10.3171/2015.1.FOCUS14755] [PMID: 25727226]
[53]
Jacob, S.; Praz, F. DNA mismatch repair defects: role in colorectal carcinogenesis. Biochimie, 2002, 84(1), 27-47.
[http://dx.doi.org/10.1016/S0300-9084(01)01362-1] [PMID: 11900875]
[54]
Kinsella, T.J. Coordination of DNA mismatch repair and base excision repair processing of chemotherapy and radiation damage for targeting resistant cancers. Clin. Cancer Res., 2009, 15(6), 1853-1859.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1307] [PMID: 19240165]
[55]
Jeppesen, D.K.; Bohr, V.A.; Stevnsner, T. DNA repair deficiency in neurodegeneration. Prog. Neurobiol., 2011, 94(2), 166-200.
[http://dx.doi.org/10.1016/j.pneurobio.2011.04.013] [PMID: 21550379]
[56]
Liu, L.; Gerson, S.L. Targeted modulation of MGMT: clinical implications. Clin. Cancer Res., 2006, 12(2), 328-331.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-2543] [PMID: 16428468]
[57]
Messaoudi, K.; Clavreul, A.; Lagarce, F. Toward an effective strategy in glioblastoma treatment. Part I: resistance mechanisms and strategies to overcome resistance of glioblastoma to temozolomide. Drug Discov. Today, 2015, 20(7), 899-905.
[http://dx.doi.org/10.1016/j.drudis.2015.02.011] [PMID: 25744176]
[58]
Johannessen, T.C.A.; Bjerkvig, R.; Tysnes, B.B. DNA repair and cancer stem-like cells--potential partners in glioma drug resistance? Cancer Treat. Rev., 2008, 34(6), 558-567.
[http://dx.doi.org/10.1016/j.ctrv.2008.03.125] [PMID: 18501520]
[59]
Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature, 2008, 455(7216), 1061-1068.
[http://dx.doi.org/10.1038/nature07385] [PMID: 18772890]
[60]
Happold, C.; Roth, P.; Wick, W.; Schmidt, N.; Florea, A.M.; Silginer, M.; Reifenberger, G.; Weller, M. Distinct molecular mechanisms of acquired resistance to temozolomide in glioblastoma cells. J. Neurochem., 2012, 122(2), 444-455.
[http://dx.doi.org/10.1111/j.1471-4159.2012.07781.x] [PMID: 22564186]
[61]
Cahill, D.P.; Levine, K.K.; Betensky, R.A.; Codd, P.J.; Romany, C.A.; Reavie, L.B.; Batchelor, T.T.; Futreal, P.A.; Stratton, M.R.; Curry, W.T.; Iafrate, A.J.; Louis, D.N. Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin. Cancer Res., 2007, 13(7), 2038-2045.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-2149] [PMID: 17404084]
[62]
Yip, S.; Miao, J.; Cahill, D.P.; Iafrate, A.J.; Aldape, K.; Nutt, C.L.; Louis, D.N. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin. Cancer Res., 2009, 15(14), 4622-4629.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-3012] [PMID: 19584161]
[63]
Stark, A.M.; Doukas, A.; Hugo, H.H.; Mehdorn, H.M. The expression of mismatch repair proteins MLH1, MSH2 and MSH6 correlates with the Ki67 proliferation index and survival in patients with recurrent glioblastoma. Neurol. Res., 2010, 32(8), 816-820.
[http://dx.doi.org/10.1179/016164110X12645013515052] [PMID: 20223108]
[64]
Shinsato, Y.; Furukawa, T.; Yunoue, S.; Yonezawa, H.; Minami, K.; Nishizawa, Y.; Ikeda, R.; Kawahara, K.; Yamamoto, M.; Hirano, H.; Tokimura, H.; Arita, K. Reduction of MLH1 and PMS2 confers temozolomide resistance and is associated with recurrence of glioblastoma. Oncotarget, 2013, 4(12), 2261-2270.
[http://dx.doi.org/10.18632/oncotarget.1302] [PMID: 24259277]
[65]
Higuchi, F.; Fink, A.L.; Kiyokawa, J.; Miller, J.J.; Koerner, M.V.A.; Cahill, D.P.; Wakimoto, H. PLK1 inhibition targets myc-activated malignant glioma cells irrespective of mismatch repair deficiency-mediated acquired resistance to temozolomide. Mol. Cancer Ther., 2018, 17(12), 2551-2563.
[http://dx.doi.org/10.1158/1535-7163.MCT-18-0177] [PMID: 30217967]
[66]
Maxwell, J.A.; Johnson, S.P.; McLendon, R.E.; Lister, D.W.; Horne, K.S.; Rasheed, A.; Quinn, J.A.; Ali-Osman, F.; Friedman, A.H.; Modrich, P.L.; Bigner, D.D.; Friedman, H.S. Mismatch repair deficiency does not mediate clinical resistance to temozolomide in malignant glioma. Clin. Cancer Res., 2008, 14(15), 4859-4868.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-4807] [PMID: 18676759]
[67]
Fu, D.; Calvo, J.A.; Samson, L.D. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat. Rev. Cancer, 2012, 12(2), 104-120.
[http://dx.doi.org/10.1038/nrc3185] [PMID: 22237395]
[68]
Wood, R.D.; Mitchell, M.; Sgouros, J.; Lindahl, T. Human DNA repair genes. Science, 2001, 291(5507), 1284-1289.
[http://dx.doi.org/10.1126/science.1056154] [PMID: 11181991]
[69]
Iyama, T.; Wilson, D.M. III DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst.), 2013, 12(8), 620-636.
[http://dx.doi.org/10.1016/j.dnarep.2013.04.015] [PMID: 23684800]
[70]
Dantzer, F.; Amé, J.C.; Schreiber, V.; Nakamura, J.; Ménissier-de Murcia, J.; de Murcia, G. Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol., 2006, 409, 493-510.
[http://dx.doi.org/10.1016/S0076-6879(05)09029-4] [PMID: 16793420]
[71]
Aguilar-Quesada, R.; Muñoz-Gámez, J.A.; Martín-Oliva, D.; Peralta-Leal, A.; Quiles-Pérez, R.; Rodríguez-Vargas, J.M.; Ruiz de Almodóvar, M.; Conde, C.; Ruiz-Extremera, A.; Oliver, F.J. Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr. Med. Chem., 2007, 14(11), 1179-1187.
[http://dx.doi.org/10.2174/092986707780597998] [PMID: 17504138]
[72]
Curtin, N.J.; Wang, L.Z.; Yiakouvaki, A.; Kyle, S.; Arris, C.A.; Canan-Koch, S.; Webber, S.E.; Durkacz, B.W.; Calvert, H.A.; Hostomsky, Z.; Newell, D.R. Novel poly(ADP-ribose) polymerase-1 inhibitor, AG14361, restores sensitivity to temozolomide in mismatch repair-deficient cells. Clin. Cancer Res., 2004, 10(3), 881-889.
[http://dx.doi.org/10.1158/1078-0432.CCR-1144-3] [PMID: 14871963]
[73]
Tentori, L.; Graziani, G. Recent approaches to improve the antitumor efficacy of temozolomide. Curr. Med. Chem., 2009, 16(2), 245-257.
[http://dx.doi.org/10.2174/092986709787002718] [PMID: 19149575]
[74]
Ratnam, K.; Low, J.A. Current development of clinical inhibitors of poly(ADP-ribose) polymerase in oncology. Clin. Cancer Res., 2007, 13(5), 1383-1388.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-2260] [PMID: 17332279]
[75]
Calabrese, C.R.; Almassy, R.; Barton, S.; Batey, M.A.; Calvert, A.H.; Canan-Koch, S.; Durkacz, B.W.; Hostomsky, Z.; Kumpf, R.A.; Kyle, S.; Li, J.; Maegley, K.; Newell, D.R.; Notarianni, E.; Stratford, I.J.; Skalitzky, D.; Thomas, H.D.; Wang, L.Z.; Webber, S.E.; Williams, K.J.; Curtin, N.J. Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J. Natl. Cancer Inst., 2004, 96(1), 56-67.
[http://dx.doi.org/10.1093/jnci/djh005] [PMID: 14709739]
[76]
Miknyoczki, S.J.; Jones-Bolin, S.; Pritchard, S.; Hunter, K.; Zhao, H.; Wan, W.; Ator, M.; Bihovsky, R.; Hudkins, R.; Chatterjee, S.; Klein-Szanto, A.; Dionne, C.; Ruggeri, B. Chemopotentiation of temozolomide, irinotecan, and cisplatin activity by CEP-6800, a poly(ADP-ribose) polymerase inhibitor. Mol. Cancer Ther., 2003, 2(4), 371-382.
[PMID: 12700281]
[77]
Cheng, C.L.; Johnson, S.P.; Keir, S.T.; Quinn, J.A.; Ali-Osman, F.; Szabo, C.; Li, H.; Salzman, A.L.; Dolan, M.E.; Modrich, P.; Bigner, D.D.; Friedman, H.S. Poly(ADP-ribose) polymerase-1 inhibition reverses temozolomide resistance in a DNA mismatch repair-deficient malignant glioma xenograft. Mol. Cancer Ther., 2005, 4(9), 1364-1368.
[http://dx.doi.org/10.1158/1535-7163.MCT-05-0128] [PMID: 16170028]
[78]
Shackleton, M.; Quintana, E.; Fearon, E.R.; Morrison, S.J. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell, 2009, 138(5), 822-829.
[http://dx.doi.org/10.1016/j.cell.2009.08.017] [PMID: 19737509]
[79]
Tang, D.G. Understanding cancer stem cell heterogeneity and plasticity. Cell Res., 2012, 22(3), 457-472.
[http://dx.doi.org/10.1038/cr.2012.13] [PMID: 22357481]
[80]
Reya, T.; Morrison, S.J.; Clarke, M.F.; Weissman, I.L. Stem cells, cancer, and cancer stem cells. Nature, 2001, 414(6859), 105-111.
[http://dx.doi.org/10.1038/35102167] [PMID: 11689955]
[81]
Visvader, J.E.; Lindeman, G.J. Cancer stem cells: current status and evolving complexities. Cell Stem Cell, 2012, 10(6), 717-728.
[http://dx.doi.org/10.1016/j.stem.2012.05.007] [PMID: 22704512]
[82]
Kreso, A.; Dick, J.E. Evolution of the cancer stem cell model. Cell Stem Cell, 2014, 14(3), 275-291.
[http://dx.doi.org/10.1016/j.stem.2014.02.006] [PMID: 24607403]
[83]
Singh, S.K.; Hawkins, C.; Clarke, I.D.; Squire, J.A.; Bayani, J.; Hide, T.; Henkelman, R.M.; Cusimano, M.D.; Dirks, P.B. Identification of human brain tumour initiating cells. Nature, 2004, 432(7015), 396-401.
[http://dx.doi.org/10.1038/nature03128] [PMID: 15549107]
[84]
Kania, G.; Corbeil, D.; Fuchs, J.; Tarasov, K.V.; Blyszczuk, P.; Huttner, W.B.; Boheler, K.R.; Wobus, A.M. Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors. Stem Cells, 2005, 23(6), 791-804.
[http://dx.doi.org/10.1634/stemcells.2004-0232] [PMID: 15917475]
[85]
Beier, D.; Hau, P.; Proescholdt, M.; Lohmeier, A.; Wischhusen, J.; Oefner, P.J.; Aigner, L.; Brawanski, A.; Bogdahn, U.; Beier, C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res., 2007, 67(9), 4010-4015.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-4180] [PMID: 17483311]
[86]
Abou-Antoun, T.J.; Hale, J.S.; Lathia, J.D.; Dombrowski, S.M. Brain Cancer Stem Cells in Adults and Children: Cell Biology and Therapeutic Implications. Neurotherapeutics, 2017, 14(2), 372-384.
[http://dx.doi.org/10.1007/s13311-017-0524-0] [PMID: 28374184]
[87]
Plaks, V.; Kong, N.; Werb, Z. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell, 2015, 16(3), 225-238.
[http://dx.doi.org/10.1016/j.stem.2015.02.015] [PMID: 25748930]
[88]
Bryukhovetskiy, A.; Shevchenko, V.; Kovalev, S.; Chekhonin, V.; Baklaushev, V.; Bryukhovetskiy, I.; Zhukova, M. To the novel paradigm of proteome-based cell therapy of tumors: through comparative proteome mapping of tumor stem cells and tissue-specific stem cells of humans. Cell Transplant., 2014, 23(Suppl. 1), S151-S170.
[http://dx.doi.org/10.3727/096368914X684907] [PMID: 25303679]
[89]
Alcantara Llaguno, S.; Chen, J.; Kwon, C.H.; Jackson, E.L.; Li, Y.; Burns, D.K.; Alvarez-Buylla, A.; Parada, L.F. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell, 2009, 15(1), 45-56.
[http://dx.doi.org/10.1016/j.ccr.2008.12.006] [PMID: 19111880]
[90]
Chen, J.; Li, Y.; Yu, T.S.; McKay, R.M.; Burns, D.K.; Kernie, S.G.; Parada, L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature, 2012, 488(7412), 522-526.
[http://dx.doi.org/10.1038/nature11287] [PMID: 22854781]
[91]
Auffinger, B.; Spencer, D.; Pytel, P.; Ahmed, A.U.; Lesniak, M.S. The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence. Expert Rev. Neurother., 2015, 15(7), 741-752.
[http://dx.doi.org/10.1586/14737175.2015.1051968] [PMID: 26027432]
[92]
Jackson, M.; Hassiotou, F.; Nowak, A. Glioblastoma stem-like cells: at the root of tumor recurrence and a therapeutic target. Carcinogenesis, 2015, 36(2), 177-185.
[http://dx.doi.org/10.1093/carcin/bgu243] [PMID: 25504149]
[93]
Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 2006, 444(7120), 756-760.
[http://dx.doi.org/10.1038/nature05236] [PMID: 17051156]
[94]
Galli, R.; Binda, E.; Orfanelli, U.; Cipelletti, B.; Gritti, A.; De Vitis, S.; Fiocco, R.; Foroni, C.; Dimeco, F.; Vescovi, A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res., 2004, 64(19), 7011-7021.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-1364] [PMID: 15466194]
[95]
Kim, S.S.; Harford, J.B.; Pirollo, K.F.; Chang, E.H. Effective treatment of glioblastoma requires crossing the blood-brain barrier and targeting tumors including cancer stem cells: The promise of nanomedicine. Biochem. Biophys. Res. Commun., 2015, 468(3), 485-489.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.137] [PMID: 26116770]
[96]
Yoshida, G.J.; Saya, H. Therapeutic strategies targeting cancer stem cells. Cancer Sci., 2016, 107(1), 5-11.
[http://dx.doi.org/10.1111/cas.12817] [PMID: 26362755]
[97]
Alvino, E.; Castiglia, D.; Caporali, S.; Pepponi, R.; Caporaso, P.; Lacal, P.M.; Marra, G.; Fischer, F.; Zambruno, G.; Bonmassar, E.; Jiricny, J.; D’Atri, S. A single cycle of treatment with temozolomide, alone or combined with O(6)-benzylguanine, induces strong chemoresistance in melanoma cell clones in vitro: role of O(6)-methylguanine-DNA methyltransferase and the mismatch repair system. Int. J. Oncol., 2006, 29(4), 785-797.
[http://dx.doi.org/10.3892/ijo.29.4.785] [PMID: 16964376]
[98]
Bradshaw, T.D.; Stone, E.L.; Trapani, V.; Leong, C-O.; Matthews, C.S.; te Poele, R.; Stevens, M.F.G. Mechanisms of acquired resistance to 2-(4-Amino-3-methylphenyl)benzothiazole in breast cancer cell lines. Breast Cancer Res. Treat., 2008, 110(1), 57-68.
[http://dx.doi.org/10.1007/s10549-007-9690-9] [PMID: 17674193]
[99]
Huse, J.T.; Holland, E.C. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat. Rev. Cancer, 2010, 10(5), 319-331.
[http://dx.doi.org/10.1038/nrc2818] [PMID: 20414201]
[100]
Angers-Loustau, A.; Hering, R.; Werbowetski, T.E.; Kaplan, D.R.; Del Maestro, R.F. SRC regulates actin dynamics and invasion of malignant glial cells in three dimensions. Mol. Cancer Res., 2004, 2(11), 595-605.
[PMID: 15561776]
[101]
Du, J.; Bernasconi, P.; Clauser, K.R.; Mani, D.R.; Finn, S.P.; Beroukhim, R.; Burns, M.; Julian, B.; Peng, X.P.; Hieronymus, H.; Maglathlin, R.L.; Lewis, T.A.; Liau, L.M.; Nghiemphu, P.; Mellinghoff, I.K.; Louis, D.N.; Loda, M.; Carr, S.A.; Kung, A.L.; Golub, T.R. Bead-based profiling of tyrosine kinase phosphorylation identifies SRC as a potential target for glioblastoma therapy. Nat. Biotechnol., 2009, 27(1), 77-83.
[http://dx.doi.org/10.1038/nbt.1513] [PMID: 19098899]
[102]
Eom, K-Y.; Cho, B.J.; Choi, E.J.; Kim, J-H.; Chie, E.K.; Wu, H-G.; Kim, I.H.; Paek, S.H.; Kim, J-S.; Kim, I.A. The Effect of chemoradiotherapy with SRC tyrosine kinase inhibitor, pp2 and temozolomide on malignant glioma cells in vitro and in vivo. Cancer Res. Treat., 2016, 48(2), 687-697.
[http://dx.doi.org/10.4143/crt.2014.320] [PMID: 26044161]
[103]
Huveldt, D.; Lewis-Tuffin, L.J.; Carlson, B.L.; Schroeder, M.A.; Rodriguez, F.; Giannini, C.; Galanis, E.; Sarkaria, J.N.; Anastasiadis, P.Z. Targeting Src family kinases inhibits bevacizumab-induced glioma cell invasion. PLoS One, 2013, 8(2), e56505.
[http://dx.doi.org/10.1371/journal.pone.0056505] [PMID: 23457577]
[104]
Ujifuku, K.; Mitsutake, N.; Takakura, S.; Matsuse, M.; Saenko, V.; Suzuki, K.; Hayashi, K.; Matsuo, T.; Kamada, K.; Nagata, I.; Yamashita, S. miR-195, miR-455-3p and miR-10a(*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett., 2010, 296(2), 241-248.
[http://dx.doi.org/10.1016/j.canlet.2010.04.013] [PMID: 20444541]
[105]
Li, Y.; Liu, Y.; Ren, J.; Deng, S.; Yi, G.; Guo, M.; Shu, S.; Zhao, L.; Peng, Y.; Qi, S. miR-1268a regulates ABCC1 expression to mediate temozolomide resistance in glioblastoma. J. Neurooncol., 2018, 138(3), 499-508.
[http://dx.doi.org/10.1007/s11060-018-2835-3] [PMID: 29876787]
[106]
Xu, J.; Huang, H.; Peng, R.; Ding, X.; Jiang, B.; Yuan, X.; Xi, J. MicroRNA-30a increases the chemosensitivity of U251 glioblastoma cells to temozolomide by directly targeting beclin 1 and inhibiting autophagy. Exp. Ther. Med., 2018, 15(6), 4798-4804.
[PMID: 29805498]
[107]
Slaby, O.; Lakomy, R.; Fadrus, P.; Hrstka, R.; Kren, L.; Lzicarova, E.; Smrcka, M.; Svoboda, M.; Dolezalova, H.; Novakova, J.; Valik, D.; Vyzula, R.; Michalek, J. MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma, 2010, 57(3), 264-269.
[http://dx.doi.org/10.4149/neo_2010_03_264] [PMID: 20353279]
[108]
Yung, A.; Levin, V.A.; Albright, R.; Olson, J.; Fredericks, R.; Fink, K.; Prados, M.; Brada, M.; Spence, A.; Brunner, J.; Yue, N.; Dugan, M. Zakneon. S. Randomized trial of Temodal (TEM) vs. Procarbazine (PCB) in glioblastoma multiforme (GBM) at first relapse. Proc. Am. Soc. Clin. Oncol., 1999, 18, 139a.
[109]
Yung, W.K.; Prados, M.D.; Yaya-Tur, R.; Rosenfeld, S.S.; Brada, M.; Friedman, H.S.; Albright, R.; Olson, J.; Chang, S.M.; O’Neill, A.M.; Friedman, A.H.; Bruner, J.; Yue, N.; Dugan, M.; Zaknoen, S.; Levin, V.A. Temodal Brain Tumor Group. Multicenter phase II trial of temozolomide in patients with anaplastic astrocytoma or anaplastic oligoastrocytoma at first relapse. J. Clin. Oncol., 1999, 17(9), 2762-2771.
[http://dx.doi.org/10.1200/JCO.1999.17.9.2762] [PMID: 10561351]
[110]
Stupp, R.; Mason, W.P.; van den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.B.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U.; Curschmann, J.; Janzer, R.C.; Ludwin, S.K.; Gorlia, T.; Allgeier, A.; Lacombe, D.; Cairncross, J.G.; Eisenhauer, E.; Mirimanoff, R.O. European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med., 2005, 352(10), 987-996.
[http://dx.doi.org/10.1056/NEJMoa043330] [PMID: 15758009]
[111]
Louis, D.N.; Perry, A.; Reifenberger, G.; von Deimling, A.; Figarella-Branger, D.; Cavenee, W.K.; Ohgaki, H.; Wiestler, O.D.; Kleihues, P.; Ellison, D.W. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol., 2016, 131(6), 803-820.
[http://dx.doi.org/10.1007/s00401-016-1545-1] [PMID: 27157931]
[112]
Mieskolainen, M. Molecular characteristics of malignant gliomas and their future perspectives - a review; Eesti Arst, 2017.
[113]
Westphal, M.; Lamszus, K. Circulating biomarkers for gliomas. Nat. Rev. Neurol., 2015, 11(10), 556-566.
[http://dx.doi.org/10.1038/nrneurol.2015.171] [PMID: 26369507]
[114]
Wen, P.Y.; Reardon, D.A. Neuro-oncology in 2015: Progress in glioma diagnosis, classification and treatment. Nat. Rev. Neurol., 2016, 12(2), 69-70.
[http://dx.doi.org/10.1038/nrneurol.2015.242] [PMID: 26782337]
[115]
Gainer, J.L.; Sheehan, J.P.; Larner, J.M.; Jones, D.R. Trans sodium crocetinate with temozolomide and radiation therapy for glioblastoma multiforme. J. Neurosurg., 2017, 126(2), 460-466.
[http://dx.doi.org/10.3171/2016.3.JNS152693] [PMID: 27177177]
[116]
Stupp, R.; Taillibert, S.; Kanner, A.A.; Kesari, S.; Steinberg, D.M.; Toms, S.A.; Taylor, L.P.; Lieberman, F.; Silvani, A.; Fink, K.L.; Barnett, G.H.; Zhu, J.J.; Henson, J.W.; Engelhard, H.H.; Chen, T.C.; Tran, D.D.; Sroubek, J.; Tran, N.D.; Hottinger, A.F.; Landolfi, J.; Desai, R.; Caroli, M.; Kew, Y.; Honnorat, J.; Idbaih, A.; Kirson, E.D.; Weinberg, U.; Palti, Y.; Hegi, M.E.; Ram, Z. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: A Randomized Clinical Trial. JAMA, 2015, 314(23), 2535-2543.
[http://dx.doi.org/10.1001/jama.2015.16669] [PMID: 26670971]
[117]
Gilbert, M.R.; Dignam, J.J.; Armstrong, T.S.; Wefel, J.S.; Blumenthal, D.T.; Vogelbaum, M.A.; Colman, H.; Chakravarti, A.; Pugh, S.; Won, M.; Jeraj, R.; Brown, P.D.; Jaeckle, K.A.; Schiff, D.; Stieber, V.W.; Brachman, D.G.; Werner-Wasik, M.; Tremont-Lukats, I.W.; Sulman, E.P.; Aldape, K.D.; Curran, W.J., Jr; Mehta, M.P. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N. Engl. J. Med., 2014, 370(8), 699-708.
[http://dx.doi.org/10.1056/NEJMoa1308573] [PMID: 24552317]
[118]
Chinot, O.L.; Wick, W.; Mason, W.; Henriksson, R.; Saran, F.; Nishikawa, R.; Carpentier, A.F.; Hoang-Xuan, K.; Kavan, P.; Cernea, D.; Brandes, A.A.; Hilton, M.; Abrey, L.; Cloughesy, T. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med., 2014, 370(8), 709-722.
[http://dx.doi.org/10.1056/NEJMoa1308345] [PMID: 24552318]
[119]
Donawho, C.K.; Luo, Y.; Luo, Y.; Penning, T.D.; Bauch, J.L.; Bouska, J.J.; Bontcheva-Diaz, V.D.; Cox, B.F.; DeWeese, T.L.; Dillehay, L.E.; Ferguson, D.C.; Ghoreishi-Haack, N.S.; Grimm, D.R.; Guan, R.; Han, E.K.; Holley-Shanks, R.R.; Hristov, B.; Idler, K.B.; Jarvis, K.; Johnson, E.F.; Kleinberg, L.R.; Klinghofer, V.; Lasko, L.M.; Liu, X.; Marsh, K.C.; McGonigal, T.P.; Meulbroek, J.A.; Olson, A.M.; Palma, J.P.; Rodriguez, L.E.; Shi, Y.; Stavropoulos, J.A.; Tsurutani, A.C.; Zhu, G.D.; Rosenberg, S.H.; Giranda, V.L.; Frost, D.J. ABT-888, an orally active poly(ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin. Cancer Res., 2007, 13(9), 2728-2737.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-3039] [PMID: 17473206]
[120]
Baxter, P.A.; Su, J.M.; Onar-Thomas, A.; Billups, C.A.; Li, X.N.; Poussaint, T.Y.; Smith, E.R.; Thompson, P.; Adesina, A.; Ansell, P.; Giranda, V.; Paulino, A.; Kilburn, L.; Quaddoumi, I.; Broniscer, A.; Blaney, S.M.; Dunkel, I.J.; Fouladi, M. A phase I/II study of veliparib (ABT-888) with radiation and temozolomide in newly diagnosed diffuse pontine glioma: a Pediatric Brain Tumor Consortium study. Neuro-oncol., 2020, 22(6), 875-885.
[http://dx.doi.org/10.1093/neuonc/noaa016] [PMID: 32009149]
[121]
Twelves, C.; Short, S.; Wright, S. A two-part safety and exploratory efficacy randomized double-blind, placebo-controlled study of a 1:1 ratio of the cannabinoids cannabidiol and delta-9-tetrahydrocannabinol (CBD:THC) plus dose-intense temozolomide in patients with recurrent glioblastoma multiforme (GBM). J. Clin. Oncol., 2017, 35(15), 2046-2046.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.2046]
[122]
Gupta, S.K.; Kizilbash, S.H.; Carlson, B.L.; Mladek, A.C.; Boakye-Agyeman, F.; Bakken, K.K.; Pokorny, J.L.; Schroeder, M.A.; Decker, P.A.; Cen, L.; Eckel-Passow, J.E.; Sarkar, G.; Ballman, K.V.; Reid, J.M.; Jenkins, R.B.; Verhaak, R.G.; Sulman, E.P.; Kitange, G.J.; Sarkaria, J.N. Delineation of MGMT hypermethylation as a biomarker for veliparib-mediated temozolomide-sensitizing therapy of glioblastoma. J. Natl. Cancer Inst., 2015, 108(5), djv369.
[http://dx.doi.org/10.1093/jnci/djv369] [PMID: 26615020]
[123]
Claringbold, P.G.; Price, R.A.; Turner, J.H. Phase I-II study of radiopeptide 177Lu-octreotate in combination with capecitabine and temozolomide in advanced low-grade neuroendocrine tumors. Cancer Biother. Radiopharm., 2012, 27(9), 561-569.
[http://dx.doi.org/10.1089/cbr.2012.1276] [PMID: 23078020]
[124]
Claringbold, P.G.; Turner, J.H. Pancreatic neuroendocrine tumor Control: durable objective response to combination 177lu-octreotate-capecitabine-temozolomide radiopeptide chemotherapy. Neuroendocrinology, 2016, 103(5), 432-439.
[http://dx.doi.org/10.1159/000434723] [PMID: 26065489]
[125]
Tatar, Z.; Thivat, E.; Planchat, E.; Gimbergues, P.; Gadea, E.; Abrial, C.; Durando, X. Temozolomide and unusual indications: review of literature. Cancer Treat. Rev., 2013, 39(2), 125-135.
[http://dx.doi.org/10.1016/j.ctrv.2012.06.002] [PMID: 22818211]
[126]
Owen, S.; Souhami, L. The management of brain metastases in non-small cell lung cancer. Front. Oncol., 2014, 4, 248.
[http://dx.doi.org/10.3389/fonc.2014.00248] [PMID: 25309873]
[127]
Greenspoon, J.N.; Ellis, P.M.; Pond, G.; Caetano, S.; Broomfield, J.; Swaminath, A. Comparative survival in patients with brain metastases from non-small-cell lung cancer treated before and after implementation of radiosurgery. Curr. Oncol., 2017, 24(2), e146-e151.
[http://dx.doi.org/10.3747/co.24.3420] [PMID: 28490938]
[128]
Sperduto, P.W.; Wang, M.; Robins, H.I.; Schell, M.C.; Werner-Wasik, M.; Komaki, R.; Souhami, L.; Buyyounouski, M.K.; Khuntia, D.; Demas, W.; Shah, S.A.; Nedzi, L.A.; Perry, G.; Suh, J.H.; Mehta, M.P. A phase 3 trial of whole brain radiation therapy and stereotactic radiosurgery alone versus WBRT and SRS with temozolomide or erlotinib for non-small cell lung cancer and 1 to 3 brain metastases: Radiation Therapy Oncology Group 0320. Int. J. Radiat. Oncol. Biol. Phys., 2013, 85(5), 1312-1318.
[http://dx.doi.org/10.1016/j.ijrobp.2012.11.042] [PMID: 23391814]
[129]
Boggs, D.H.; Robins, H.I.; Langer, C.J.; Traynor, A.M.; Berkowitz, M.J.; Mehta, M.P. Strategies to prevent brain metastasis in high-risk non-small-cell lung cancer: lessons learned from a randomized study of maintenance temozolomide versus observation. Clin. Lung Cancer, 2014, 15(6), 433-440.
[http://dx.doi.org/10.1016/j.cllc.2014.06.008] [PMID: 25069747]
[130]
He, Q.; Bi, X.; Ren, C.; Wang, Y.; Zou, P.; Zhang, H.; Chi, N.; Xiu, C.; Wang, Y.; Tao, R. Phase II study of the efficacy and safety of high-dose pemetrexed in combination with cisplatin versus temozolomide for the treatment of non-small cell lung cancer with brain metastases. Anticancer Res., 2017, 37(8), 4711-4716.
[PMID: 28739776]
[131]
Guida, M.; Tommasi, S.; Strippoli, S.; Natalicchio, M.I.; De Summa, S.; Pinto, R.; Cramarossa, A.; Albano, A.; Pisconti, S.; Aieta, M.; Ridolfi, R.; Azzariti, A.; Guida, G.; Lorusso, V.; Colucci, G. The search for a melanoma-tailored chemotherapy in the new era of personalized therapy: a phase II study of chemo-modulating temozolomide followed by fotemustine and a cooperative study of GOIM (Gruppo Oncologico Italia Meridionale). BMC Cancer, 2018, 18(1), 552.
[http://dx.doi.org/10.1186/s12885-018-4479-2] [PMID: 29747595]
[132]
Middleton, M.R.; Friedlander, P.; Hamid, O.; Daud, A.; Plummer, R.; Falotico, N.; Chyla, B.; Jiang, F.; McKeegan, E.; Mostafa, N.M.; Zhu, M.; Qian, J.; McKee, M.; Luo, Y.; Giranda, V.L.; McArthur, G.A. Randomized phase II study evaluating veliparib (ABT-888) with temozolomide in patients with metastatic melanoma. Ann. Oncol., 2015, 26(10), 2173-2179.
[http://dx.doi.org/10.1093/annonc/mdv308] [PMID: 26202595]
[133]
Gabrielson, A.; Tesfaye, A.A.; Marshall, J.L.; Pishvaian, M.J.; Smaglo, B.; Jha, R.; Dorsch-Vogel, K.; Wang, H.; He, A.R. Phase II study of temozolomide and veliparib combination therapy for sorafenib-refractory advanced hepatocellular carcinoma. Cancer Chemother. Pharmacol., 2015, 76(5), 1073-1079.
[http://dx.doi.org/10.1007/s00280-015-2852-2] [PMID: 26449224]
[134]
Pishvaian, M.J.; Slack, R.S.; Jiang, W.; He, A.R.; Hwang, J.J.; Hankin, A.; Dorsch-Vogel, K.; Kukadiya, D.; Weiner, L.M.; Marshall, J.L.; Brody, J.R. A phase 2 study of the PARP inhibitor veliparib plus temozolomide in patients with heavily pretreated metastatic colorectal cancer. Cancer, 2018, 124(11), 2337-2346.
[http://dx.doi.org/10.1002/cncr.31309] [PMID: 29579325]
[135]
Han, H.S.; Diéras, V.; Robson, M.; Palácová, M.; Marcom, P.K.; Jager, A.; Bondarenko, I.; Citrin, D.; Campone, M.; Telli, M.L.; Domchek, S.M.; Friedlander, M.; Kaufman, B.; Garber, J.E.; Shparyk, Y.; Chmielowska, E.; Jakobsen, E.H.; Kaklamani, V.; Gradishar, W.; Ratajczak, C.K.; Nickner, C.; Qin, Q.; Qian, J.; Shepherd, S.P.; Isakoff, S.J.; Puhalla, S. Veliparib with temozolomide or carboplatin/paclitaxel versus placebo with carboplatin/paclitaxel in patients with BRCA1/2 locally recurrent/metastatic breast cancer: randomized phase II study. Ann. Oncol., 2018, 29(1), 154-161.
[http://dx.doi.org/10.1093/annonc/mdx505] [PMID: 29045554]
[136]
Hussain, M.; Carducci, M.A.; Slovin, S.; Cetnar, J.; Qian, J.; McKeegan, E.M.; Refici-Buhr, M.; Chyla, B.; Shepherd, S.P.; Giranda, V.L.; Alumkal, J.J. Targeting DNA repair with combination veliparib (ABT-888) and temozolomide in patients with metastatic castration-resistant prostate cancer. Invest. New Drugs, 2014, 32(5), 904-912.
[http://dx.doi.org/10.1007/s10637-014-0099-0] [PMID: 24764124]
[137]
Pietanza, M.C.; Waqar, S.N.; Krug, L.M.; Dowlati, A.; Hann, C.L.; Chiappori, A.; Owonikoko, T.K.; Woo, K.M.; Cardnell, R.J.; Fujimoto, J.; Long, L.; Diao, L.; Wang, J.; Bensman, Y.; Hurtado, B.; de Groot, P.; Sulman, E.P.; Wistuba, I.I.; Chen, A.; Fleisher, M.; Heymach, J.V.; Kris, M.G.; Rudin, C.M.; Byers, L.A. Randomized, double-blind, phase ii study of temozolomide in combination with either veliparib or placebo in patients with relapsed-sensitive or refractory small-cell lung cancer. J. Clin. Oncol., 2018, 36(23), 2386-2394.
[http://dx.doi.org/10.1200/JCO.2018.77.7672] [PMID: 29906251]
[138]
Pietanza, M.C.; Kadota, K.; Huberman, K.; Sima, C.S.; Fiore, J.J.; Sumner, D.K.; Travis, W.D.; Heguy, A.; Ginsberg, M.S.; Holodny, A.I.; Chan, T.A.; Rizvi, N.A.; Azzoli, C.G.; Riely, G.J.; Kris, M.G.; Krug, L.M. Phase II trial of temozolomide in patients with relapsed sensitive or refractory small cell lung cancer, with assessment of methylguanine-DNA methyltransferase as a potential biomarker. Clin. Cancer Res., 2012, 18(4), 1138-1145.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-2059] [PMID: 22228633]
[139]
Hochhauser, D.; Glynne-Jones, R.; Potter, V.; Grávalos, C.; Doyle, T.J.; Pathiraja, K.; Zhang, Q.; Zhang, L.; Sausville, E.A. A phase II study of temozolomide in patients with advanced aerodigestive tract and colorectal cancers and methylation of the O6-methylguanine-DNA methyltransferase promoter. Mol. Cancer Ther., 2013, 12(5), 809-818.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0710] [PMID: 23443801]
[140]
Struve, N.; Binder, Z.A.; Stead, L.F.; Brend, T.; Bagley, S.J.; Faulkner, C.; Ott, L.; Müller-Goebel, J.; Weik, A.S.; Hoffer, K.; Krug, L.; Rieckmann, T.; Bußmann, L.; Henze, M.; Morrissette, J.J.D.; Kurian, K.M.; Schüller, U.; Petersen, C.; Rothkamm, K.; O, Rourke D.M.; Short, S.C.; Kriegs, M. EGFRvIII upregulates DNA mismatch repair resulting in increased temozolomide sensitivity of MGMT promoter methylated glioblastoma. Oncogene, 2020, 39(15), 3041-3055.
[http://dx.doi.org/10.1038/s41388-020-1208-5] [PMID: 32066879]
[141]
McFaline-Figueroa, J.L.; Braun, C.J.; Stanciu, M.; Nagel, Z.D.; Mazzucato, P.; Sangaraju, D.; Cerniauskas, E.; Barford, K.; Vargas, A.; Chen, Y.; Tretyakova, N.; Lees, J.A.; Hemann, M.T.; White, F.M.; Samson, L.D. Minor changes in expression of the mismatch repair protein MSH2 exert a major impact on glioblastoma response to temozolomide. Cancer Res., 2015, 75(15), 3127-3138.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-3616] [PMID: 26025730]
[142]
Yoshimoto, K.; Mizoguchi, M.; Hata, N.; Murata, H.; Hatae, R.; Amano, T.; Nakamizo, A.; Sasaki, T. Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Front. Oncol., 2012, 2, 186.
[http://dx.doi.org/10.3389/fonc.2012.00186] [PMID: 23227453]
[143]
Jeong, J.H.; Hong, Y.S.; Park, Y.; Kim, J.; Kim, J.E.; Kim, K.P.; Kim, S.Y.; Park, J.H.; Kim, J.H.; Park, I.J.; Lim, S.B.; Yu, C.S.; Kim, J.C.; Kim, T.W. Phase 1 Study of preoperative chemoradiation therapy with temozolomide and capecitabine in patients with locally advanced rectal cancer. Int. J. Radiat. Oncol. Biol. Phys., 2016, 96(2), 289-295.
[http://dx.doi.org/10.1016/j.ijrobp.2016.05.009] [PMID: 27473815]
[144]
Calegari, M.A.; Inno, A.; Monterisi, S.; Orlandi, A.; Santini, D.; Basso, M.; Cassano, A.; Martini, M.; Cenci, T.; de Pascalis, I.; Camarda, F.; Barbaro, B.; Larocca, L.M.; Gori, S.; Tonini, G.; Barone, C. A phase 2 study of temozolomide in pretreated metastatic colorectal cancer with MGMT promoter methylation. Br. J. Cancer, 2017, 116(10), 1279-1286.
[http://dx.doi.org/10.1038/bjc.2017.109] [PMID: 28427088]
[145]
Amatu, A.; Barault, L.; Moutinho, C.; Cassingena, A.; Bencardino, K.; Ghezzi, S.; Palmeri, L.; Bonazzina, E.; Tosi, F.; Ricotta, R.; Cipani, T.; Crivori, P.; Gatto, R.; Chirico, G.; Marrapese, G.; Truini, M.; Bardelli, A.; Esteller, M.; Di Nicolantonio, F.; Sartore-Bianchi, A.; Siena, S. Tumor MGMT promoter hypermethylation changes over time limit temozolomide efficacy in a phase II trial for metastatic colorectal cancer. Ann. Oncol., 2016, 27(6), 1062-1067.
[http://dx.doi.org/10.1093/annonc/mdw071] [PMID: 26916096]
[146]
Pietrantonio, F.; Perrone, F.; de Braud, F.; Castano, A.; Maggi, C.; Bossi, I.; Gevorgyan, A.; Biondani, P.; Pacifici, M.; Busico, A.; Gariboldi, M.; Festinese, F.; Tamborini, E.; Di Bartolomeo, M. Activity of temozolomide in patients with advanced chemorefractory colorectal cancer and MGMT promoter methylation. Ann. Oncol., 2014, 25(2), 404-408.
[http://dx.doi.org/10.1093/annonc/mdt547] [PMID: 24379162]
[147]
Pietrantonio, F.; de Braud, F.; Milione, M.; Maggi, C.; Iacovelli, R.; Dotti, K.F.; Perrone, F.; Tamborini, E.; Caporale, M.; Berenato, R.; Leone, G.; Pellegrinelli, A.; Bossi, I.; Festinese, F.; Federici, S.; Di Bartolomeo, M. Dose-dense temozolomide in patients with mgmt-silenced chemorefractory colorectal cancer. Target. Oncol., 2016, 11(3), 337-343.
[http://dx.doi.org/10.1007/s11523-015-0397-2] [PMID: 26538496]
[148]
Tentori, L.; Graziani, G.; Gilberti, S.; Lacal, P.M.; Bonmassar, E.; D’Atri, S. Triazene compounds induce apoptosis in O6-alkylguanine-DNA alkyltransferase deficient leukemia cell lines. Leukemia, 1995, 9(11), 1888-1895.
[PMID: 7475280]
[149]
Brandwein, J.M.; Yang, L.; Schimmer, A.D.; Schuh, A.C.; Gupta, V.; Wells, R.A.; Alibhai, S.M.; Xu, W.; Minden, M.D. A phase II study of temozolomide therapy for poor-risk patients aged >or=60 years with acute myeloid leukemia: low levels of MGMT predict for response. Leukemia, 2007, 21(4), 821-824.
[http://dx.doi.org/10.1038/sj.leu.2404545] [PMID: 17252015]
[150]
Lenz, G.; Hutter, G.; Hiddemann, W.; Dreyling, M. Promoter methylation and expression of DNA repair genes hMLH1 and MGMT in acute myeloid leukemia. Ann. Hematol., 2004, 83(10), 628-633.
[http://dx.doi.org/10.1007/s00277-004-0925-0] [PMID: 15309527]
[151]
Brandwein, J.M.; Kassis, J.; Leber, B.; Hogge, D.; Howson-Jan, K.; Minden, M.D.; Galarneau, A.; Pouliot, J.F. Phase II study of targeted therapy with temozolomide in acute myeloid leukaemia and high-risk myelodysplastic syndrome patients pre-screened for low O(6) -methylguanine DNA methyltransferase expression. Br. J. Haematol., 2014, 167(5), 664-670.
[http://dx.doi.org/10.1111/bjh.13094] [PMID: 25160658]
[152]
Gojo, I.; Beumer, J.H.; Pratz, K.W.; McDevitt, M.A.; Baer, M.R.; Blackford, A.L.; Smith, B.D.; Gore, S.D.; Carraway, H.E.; Showel, M.M.; Levis, M.J.; Dezern, A.E.; Gladstone, D.E.; Ji, J.J.; Wang, L.; Kinders, R.J.; Pouquet, M.; Ali-Walbi, I.; Rudek, M.A.; Poh, W.; Herman, J.G.; Karnitz, L.M.; Kaufmann, S.H.; Chen, A.; Karp, J.E. A Phase 1 Study of the PARP inhibitor veliparib in combination with temozolomide in acute myeloid leukemia. Clin. Cancer Res., 2017, 23(3), 697-706.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-0984] [PMID: 27503200]
[153]
Medeiros, B.C.; Kohrt, H.E.; Gotlib, J.; Coutre, S.E.; Zhang, B.; Arber, D.A.; Zehnder, J.L. Tailored temozolomide therapy according to MGMT methylation status for elderly patients with acute myeloid leukemia. Am. J. Hematol., 2012, 87(1), 45-50.
[http://dx.doi.org/10.1002/ajh.22191] [PMID: 22052619]
[154]
Hassel, J.C.; Sucker, A.; Edler, L.; Kurzen, H.; Moll, I.; Stresemann, C.; Spieth, K.; Mauch, C.; Rass, K.; Dummer, R.; Schadendorf, D. MGMT gene promoter methylation correlates with tolerance of temozolomide treatment in melanoma but not with clinical outcome. Br. J. Cancer, 2010, 103(6), 820-826.
[http://dx.doi.org/10.1038/sj.bjc.6605796] [PMID: 20736948]
[155]
Kreth, S.; Thon, N.; Eigenbrod, S.; Lutz, J.; Ledderose, C.; Egensperger, R.; Tonn, J.C.; Kretzschmar, H.A.; Hinske, L.C.; Kreth, F.W. O-methylguanine-DNA methyltransferase (MGMT) mRNA expression predicts outcome in malignant glioma independent of MGMT promoter methylation. PLoS One, 2011, 6(2), e17156.
[http://dx.doi.org/10.1371/journal.pone.0017156] [PMID: 21365007]
[156]
Ranson, M.; Hersey, P.; Thompson, D.; Beith, J.; McArthur, G.A.; Haydon, A.; Davis, I.D.; Kefford, R.F.; Mortimer, P.; Harris, P.A.; Baka, S.; Seebaran, A.; Sabharwal, A.; Watson, A.J.; Margison, G.P.; Middleton, M.R. Randomized trial of the combination of lomeguatrib and temozolomide compared with temozolomide alone in chemotherapy naive patients with metastatic cutaneous melanoma. J. Clin. Oncol., 2007, 25(18), 2540-2545.
[http://dx.doi.org/10.1200/JCO.2007.10.8217] [PMID: 17577032]
[157]
Kushwaha, D.; Ramakrishnan, V.; Ng, K.; Steed, T.; Nguyen, T.; Futalan, D.; Akers, J.C.; Sarkaria, J.; Jiang, T.; Chowdhury, D.; Carter, B.S.; Chen, C.C. A genome-wide miRNA screen revealed miR-603 as a MGMT-regulating miRNA in glioblastomas. Oncotarget, 2014, 5(12), 4026-4039.
[http://dx.doi.org/10.18632/oncotarget.1974] [PMID: 24994119]
[158]
Chen, X.; Zhang, M.; Gan, H.; Wang, H.; Lee, J.H.; Fang, D.; Kitange, G.J.; He, L.; Hu, Z.; Parney, I.F.; Meyer, F.B.; Giannini, C.; Sarkaria, J.N.; Zhang, Z. A novel enhancer regulates MGMT expression and promotes temozolomide resistance in glioblastoma. Nat. Commun., 2018, 9(1), 2949.
[http://dx.doi.org/10.1038/s41467-018-05373-4] [PMID: 30054476]
[159]
Roos, W.P.; Nikolova, T.; Quiros, S.; Naumann, S.C.; Kiedron, O.; Zdzienicka, M.Z.; Kaina, B. Brca2/Xrcc2 dependent HR, but not NHEJ, is required for protection against O(6)-methylguanine triggered apoptosis, DSBs and chromosomal aberrations by a process leading to SCEs. DNA Repair (Amst.), 2009, 8(1), 72-86.
[http://dx.doi.org/10.1016/j.dnarep.2008.09.003] [PMID: 18840549]
[160]
Reuland, S.N.; Goldstein, N.B.; Partyka, K.A.; Cooper, D.A.; Fujita, M.; Norris, D.A.; Shellman, Y.G. The combination of BH3-mimetic ABT-737 with the alkylating agent temozolomide induces strong synergistic killing of melanoma cells independent of p53. PLoS One, 2011, 6(8), e24294.
[http://dx.doi.org/10.1371/journal.pone.0024294] [PMID: 21897876]
[161]
Li, R.H.; Hou, X.Y.; Yang, C.S.; Liu, W.L.; Tang, J.Q.; Liu, Y.Q.; Jiang, G. Temozolomide for treating malignant melanoma. J. Coll. Physicians Surg. Pak., 2015, 25(9), 680-688.
[PMID: 26374366]
[162]
Tong, R.; Kohane, D.S. New strategies in cancer nanomedicine. Annu. Rev. Pharmacol. Toxicol., 2016, 56, 41-57.
[http://dx.doi.org/10.1146/annurev-pharmtox-010715-103456] [PMID: 26514197]
[163]
Shi, J.; Kantoff, P.W.; Wooster, R.; Farokhzad, O.C. Cancer nanomedicine: progress, challenges and opportunities. Nat. Rev. Cancer, 2017, 17(1), 20-37.
[http://dx.doi.org/10.1038/nrc.2016.108] [PMID: 27834398]
[164]
Fang, C.; Wang, K.; Stephen, Z.R.; Mu, Q.; Kievit, F.M.; Chiu, D.T.; Press, O.W.; Zhang, M. Temozolomide nanoparticles for targeted glioblastoma therapy. ACS Appl. Mater. Interfaces, 2015, 7(12), 6674-6682.
[http://dx.doi.org/10.1021/am5092165] [PMID: 25751368]
[165]
Ortiz, R.; Cabeza, L.; Perazzoli, G.; Jimenez-Lopez, J.; García-Pinel, B.; Melguizo, C.; Prados, J. Nanoformulations for glioblastoma multiforme: a new hope for treatment. Future Med. Chem., 2019, 11(18), 2459-2480.
[http://dx.doi.org/10.4155/fmc-2018-0521] [PMID: 31544490]
[166]
Wagner, S.; Zensi, A.; Wien, S.L.; Tschickardt, S.E.; Maier, W.; Vogel, T.; Worek, F.; Pietrzik, C.U.; Kreuter, J.; von Briesen, H. Uptake mechanism of ApoE-modified nanoparticles on brain capillary endothelial cells as a blood-brain barrier model. PLoS One, 2012, 7(3), e32568.
[http://dx.doi.org/10.1371/journal.pone.0032568] [PMID: 22396775]
[167]
Durán, N.; Silveira, C.P.; Durán, M.; Martinez, D.S.T. Silver nanoparticle protein corona and toxicity: a mini-review. J. Nanobiotechnology, 2015, 13, 55.
[http://dx.doi.org/10.1186/s12951-015-0114-4] [PMID: 26337542]
[168]
Tian, X-H.; Lin, X-N.; Wei, F.; Feng, W.; Huang, Z.C.; Wang, P.; Ren, L.; Diao, Y. Enhanced brain targeting of temozolomide in polysorbate-80 coated polybutylcyanoacrylate nanoparticles. Int. J. Nanomedicine, 2011, 6, 445-452.
[PMID: 21445277]
[169]
Arcella, A.; Palchetti, S.; Digiacomo, L.; Pozzi, D.; Capriotti, A.L.; Frati, L.; Oliva, M.A.; Tsaouli, G.; Rota, R.; Screpanti, I.; Mahmoudi, M.; Caracciolo, G. Brain targeting by liposome-biomolecular corona boosts anticancer efficacy of temozolomide in glioblastoma cells. ACS Chem. Neurosci., 2018, 9(12), 3166-3174.
[http://dx.doi.org/10.1021/acschemneuro.8b00339] [PMID: 30015470]
[170]
Qin, Y.; Fan, W.; Chen, H.; Yao, N.; Tang, W.; Tang, J.; Yuan, W.; Kuai, R.; Zhang, Z.; Wu, Y.; He, Q. In vitro and in vivo investigation of glucose-mediated brain-targeting liposomes. J. Drug Target., 2010, 18(7), 536-549.
[http://dx.doi.org/10.3109/10611861003587235] [PMID: 20132091]
[171]
Patil, R.; Portilla-Arias, J.; Ding, H.; Inoue, S.; Konda, B.; Hu, J.; Wawrowsky, K.A.; Shin, P.K.; Black, K.L.; Holler, E.; Ljubimova, J.Y. Temozolomide delivery to tumor cells by a multifunctional nano vehicle based on poly(β-L-malic acid). Pharm. Res., 2010, 27(11), 2317-2329.
[http://dx.doi.org/10.1007/s11095-010-0091-0] [PMID: 20387095]
[172]
Zhang, J.; Xiao, X.; Zhu, J.; Gao, Z.; Lai, X.; Zhu, X.; Mao, G. Lactoferrin- and RGD-comodified, temozolomide and vincristine-coloaded nanostructured lipid carriers for gliomatosis cerebri combination therapy. Int. J. Nanomedicine, 2018, 13, 3039-3051.
[http://dx.doi.org/10.2147/IJN.S161163] [PMID: 29861635]
[173]
Lam, F.C.; Morton, S.W.; Wyckoff, J.; Vu Han, T-L.; Hwang, M.K.; Maffa, A.; Balkanska-Sinclair, E.; Yaffe, M.B.; Floyd, S.R.; Hammond, P.T. Enhanced efficacy of combined temozolomide and bromodomain inhibitor therapy for gliomas using targeted nanoparticles. Nat. Commun., 2018, 9(1), 1991.
[http://dx.doi.org/10.1038/s41467-018-04315-4] [PMID: 29777137]
[174]
Kim, S.S.; Rait, A.; Kim, E.; DeMarco, J.; Pirollo, K.F.; Chang, E.H. Encapsulation of temozolomide in a tumor-targeting nanocomplex enhances anti-cancer efficacy and reduces toxicity in a mouse model of glioblastoma. Cancer Lett., 2015, 369(1), 250-258.
[http://dx.doi.org/10.1016/j.canlet.2015.08.022] [PMID: 26325605]
[175]
Jain, A.; Singhai, P.; Gurnany, E.; Updhayay, S.; Mody, N. Transferrin-tailored solid lipid nanoparticles as vectors for site-specific delivery of temozolomide to brain. J. Nanopart. Res., 2013, 15(1518), 1-9.
[176]
Lyons, S.A.; O’Neal, J.; Sontheimer, H. Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia, 2002, 39(2), 162-173.
[http://dx.doi.org/10.1002/glia.10083] [PMID: 12112367]
[177]
Zhang, P.; Tang, M.; Huang, Q.; Zhao, G.; Huang, N.; Zhang, X.; Tan, Y.; Cheng, Y. Combination of 3-methyladenine therapy and Asn-Gly-Arg (NGR)-modified mesoporous silica nanoparticles loaded with temozolomide for glioma therapy in vitro. Biochem. Biophys. Res. Commun., 2019, 509(2), 549-556.
[http://dx.doi.org/10.1016/j.bbrc.2018.12.158] [PMID: 30600180]
[178]
Song, S.; Mao, G.; Du, J.; Zhu, X. Novel RGD containing, temozolomide-loading nanostructured lipid carriers for glioblastoma multiforme chemotherapy. Drug Deliv., 2016, 23(4), 1404-1408.
[http://dx.doi.org/10.3109/10717544.2015.1064186] [PMID: 26203687]
[179]
Minaei, S.E.; Khoei, S.; Khoee, S.; Vafashoar, F.; Mahabadi, V.P. In vitro anti-cancer efficacy of multi-functionalized magnetite nanoparticles combining alternating magnetic hyperthermia in glioblastoma cancer cells. Mater. Sci. Eng. C, 2019, 101, 575-587.
[http://dx.doi.org/10.1016/j.msec.2019.04.007] [PMID: 31029351]
[180]
Emamgholizadeh Minaei, S.; Khoei, S.; Khoee, S.; Karimi, M.R. Tri-block copolymer nanoparticles modified with folic acid for temozolomide delivery in glioblastoma. Int. J. Biochem. Cell Biol., 2019, 108, 72-83.
[http://dx.doi.org/10.1016/j.biocel.2019.01.010] [PMID: 30660689]
[181]
Ananta, J.S.; Paulmurugan, R.; Massoud, T.F. Temozolomide-loaded PLGA nanoparticles to treat glioblastoma cells: a biophysical and cell culture evaluation. Neurol. Res., 2016, 38(1), 51-59.
[http://dx.doi.org/10.1080/01616412.2015.1133025] [PMID: 26905383]
[182]
Ananta, J.S.; Paulmurugan, R.; Massoud, T.F. Nanoparticle-delivered antisense microrna-21 enhances the effects of temozolomide on glioblastoma cells. Mol. Pharm., 2015, 12(12), 4509-4517.
[http://dx.doi.org/10.1021/acs.molpharmaceut.5b00694] [PMID: 26559642]
[183]
Malhotra, M.; Sekar, T.V.; Ananta, J.S.; Devulapally, R.; Afjei, R.; Babikir, H.A.; Paulmurugan, R.; Massoud, T.F. Targeted nanoparticle delivery of therapeutic antisense microRNAs presensitizes glioblastoma cells to lower effective doses of temozolomide in vitro and in a mouse model. Oncotarget, 2018, 9(30), 21478-21494.
[http://dx.doi.org/10.18632/oncotarget.25135] [PMID: 29765554]
[184]
Ramalho, M.J.; Sevin, E.; Gosselet, F.; Lima, J.; Coelho, M.A.N.; Loureiro, J.A.; Pereira, M.C. Receptor-mediated PLGA nanoparticles for glioblastoma multiforme treatment. Int. J. Pharm., 2018, 545(1-2), 84-92.
[http://dx.doi.org/10.1016/j.ijpharm.2018.04.062] [PMID: 29715532]
[185]
Jain, A.; Chasoo, G.; Singh, S.K.; Saxena, A.K.; Jain, S.K. Transferrin-appended PEGylated nanoparticles for temozolomide delivery to brain: in vitro characterisation. J. Microencapsul., 2011, 28(1), 21-28.
[http://dx.doi.org/10.3109/02652048.2010.522257] [PMID: 21171813]
[186]
Chu, L.; Wang, A.; Ni, L.; Yan, X.; Song, Y.; Zhao, M.; Sun, K.; Mu, H.; Liu, S.; Wu, Z.; Zhang, C. Nose-to-brain delivery of temozolomide-loaded PLGA nanoparticles functionalized with anti-EPHA3 for glioblastoma targeting. Drug Deliv., 2018, 25(1), 1634-1641.
[http://dx.doi.org/10.1080/10717544.2018.1494226] [PMID: 30176744]
[187]
Illum, L. Is nose-to-brain transport of drugs in man a reality? J. Pharm. Pharmacol., 2004, 56(1), 3-17.
[http://dx.doi.org/10.1211/0022357022539] [PMID: 14979996]
[188]
Khan, A.; Aqil, M.; Imam, S.S.; Ahad, A.; Sultana, Y.; Ali, A.; Khan, K. Temozolomide loaded nano lipid based chitosan hydrogel for nose to brain delivery: Characterization, nasal absorption, histopathology and cell line study. Int. J. Biol. Macromol., 2018, 116, 1260-1267.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.05.079] [PMID: 29775717]
[189]
Tomaszowski, K.H.; Hellmann, N.; Ponath, V.; Takatsu, H.; Shin, H.W.; Kaina, B. Uptake of glucose-conjugated MGMT inhibitors in cancer cells: role of flippases and type IV P-type ATPases. Sci. Rep., 2017, 7(1), 13925.
[http://dx.doi.org/10.1038/s41598-017-14129-x] [PMID: 29066805]
[190]
Roy, S.K.; Gupta, E.; Dolan, M.E. Pharmacokinetics of O6-benzylguanine in rats and its metabolism by rat liver microsomes. Drug Metab. Dispos., 1995, 23(12), 1394-1399.
[PMID: 8689950]
[191]
Stephen, Z.R.; Kievit, F.M.; Veiseh, O.; Chiarelli, P.A.; Fang, C.; Wang, K.; Hatzinger, S.J.; Ellenbogen, R.G.; Silber, J.R.; Zhang, M. Redox-responsive magnetic nanoparticle for targeted convection-enhanced delivery of O6-benzylguanine to brain tumors. ACS Nano, 2014, 8(10), 10383-10395.
[http://dx.doi.org/10.1021/nn503735w] [PMID: 25247850]
[192]
Vlachostergios, P.J.; Hatzidaki, E.; Papandreou, C.N. MGMT repletion after treatment of glioblastoma cells with temozolomide and O6-benzylguanine implicates NFκB and mutant p53. Neurol. Res., 2013, 35(8), 879-882.
[http://dx.doi.org/10.1179/1743132813Y.0000000191] [PMID: 23561593]
[193]
Yoo, B.; Ifediba, M.A.; Ghosh, S.; Medarova, Z.; Moore, A. Combination treatment with theranostic nanoparticles for glioblastoma sensitization to TMZ. Mol. Imaging Biol., 2014, 16(5), 680-689.
[http://dx.doi.org/10.1007/s11307-014-0734-3] [PMID: 24696184]
[194]
Shchors, K.; Persson, A.I.; Rostker, F.; Tihan, T.; Lyubynska, N.; Li, N.; Swigart, L.B.; Berger, M.S.; Hanahan, D.; Weiss, W.A.; Evan, G.I. Using a preclinical mouse model of high-grade astrocytoma to optimize p53 restoration therapy. Proc. Natl. Acad. Sci. USA, 2013, 110(16), E1480-E1489.
[http://dx.doi.org/10.1073/pnas.1219142110] [PMID: 23542378]
[195]
Srivenugopal, K.S.; Shou, J.; Mullapudi, S.R.; Lang, F.F., Jr; Rao, J.S.; Ali-Osman, F. Enforced expression of wild-type p53 curtails the transcription of the O(6)-methylguanine-DNA methyltransferase gene in human tumor cells and enhances their sensitivity to alkylating agents. Clin. Cancer Res., 2001, 7(5), 1398-1409.
[PMID: 11350911]
[196]
Kim, S.S.; Rait, A.; Kim, E.; Pirollo, K.F.; Nishida, M.; Farkas, N.; Dagata, J.A.; Chang, E.H. A nanoparticle carrying the p53 gene targets tumors including cancer stem cells, sensitizes glioblastoma to chemotherapy and improves survival. ACS Nano, 2014, 8(6), 5494-5514.
[http://dx.doi.org/10.1021/nn5014484] [PMID: 24811110]
[197]
Kim, S.S.; Rait, A.; Kim, E.; Pirollo, K.F.; Chang, E.H.A. A tumor-targeting p53 nanodelivery system limits chemoresistance to temozolomide prolonging survival in a mouse model of glioblastoma multiforme. Nanomedicine (Lond.), 2015, 11(2), 301-311.
[http://dx.doi.org/10.1016/j.nano.2014.09.005] [PMID: 25240597]
[198]
Dagıstan, Y.; Karaca, I.; Bozkurt, E.R.; Ozar, E.; Yagmurlu, K.; Toklu, A.; Bilir, A. Combination hyperbaric oxygen and temozolomide therapy in C6 rat glioma model. Acta Cir. Bras., 2012, 27(6), 383-387.
[http://dx.doi.org/10.1590/S0102-86502012000600005] [PMID: 22666755]
[199]
Xie, Y.; Zeng, X.; Wu, X.; Hu, J.; Zhu, Y.; Yang, X. Hyperbaric oxygen as an adjuvant to temozolomide nanoparticle inhibits glioma growth by inducing G2/M phase arrest. Nanomed. (Lond.), 2018, 13(8), 887-898.
[http://dx.doi.org/10.2217/nnm-2017-0395] [PMID: 29473458]
[200]
Graham, K.; Unger, E. Overcoming tumor hypoxia as a barrier to radiotherapy, chemotherapy and immunotherapy in cancer treatment. Int. J. Nanomedicine, 2018, 13, 6049-6058.
[http://dx.doi.org/10.2147/IJN.S140462] [PMID: 30323592]
[201]
Zong, Z.; Hua, L.; Wang, Z.; Xu, H.; Ye, C.; Pan, B.; Zhao, Z.; Zhang, L.; Lu, J.; Mei, L.H.; Rutong, Y. Self-assembled angiopep-2 modified lipid-poly (hypoxic radiosensitized polyprodrug) nanoparticles delivery TMZ for glioma synergistic TMZ and RT therapy. Drug Deliv., 2019, 26(1), 34-44.
[http://dx.doi.org/10.1080/10717544.2018.1534897] [PMID: 30744436]
[202]
Vescovi, A.L.; Galli, R.; Reynolds, B.A. Brain tumour stem cells. Nat. Rev. Cancer, 2006, 6(6), 425-436.
[http://dx.doi.org/10.1038/nrc1889] [PMID: 16723989]
[203]
Sun, T.; Wu, H.; Li, Y.; Huang, Y.; Yao, L.; Chen, X.; Han, X.; Zhou, Y.; Du, Z. Targeting transferrin receptor delivery of temozolomide for a potential glioma stem cell-mediated therapy. Oncotarget, 2017, 8(43), 74451-74465.
[http://dx.doi.org/10.18632/oncotarget.20165] [PMID: 29088799]
[204]
Rai, R.; Banerjee, M.; Wong, D.H.; McCullagh, E.; Gupta, A.; Tripathi, S.; Riquelme, E.; Jangir, R.; Yadav, S.; Raja, M.; Melkani, P.; Dixit, V.; Patil, U.; Shrivastava, R.; Middya, S.; Olivares, F.; Guerrero, J.; Surya, A.; Pham, S.M.; Bernales, S.; Protter, A.A.; Hung, D.T.; Chakravarty, S. Temozolomide analogs with improved brain/plasma ratios - Exploring the possibility of enhancing the therapeutic index of temozolomide. Bioorg. Med. Chem. Lett., 2016, 26(20), 5103-5109.
[http://dx.doi.org/10.1016/j.bmcl.2016.08.064] [PMID: 27614414]
[205]
Zhang, J.; Hummersone, M.; Matthews, C.S.; Stevens, M.F.; Bradshaw, T.D. N3-substituted temozolomide analogs overcome methylguanine-DNA methyltransferase and mismatch repair precipitating apoptotic and autophagic cancer cell death. Oncology, 2015, 88(1), 28-48.
[http://dx.doi.org/10.1159/000366131] [PMID: 25277441]
[206]
Cousin, D.; Zhang, J.; Hummersone, M.G.; Matthews, C.S.; Frigerio, M.; Bradshaw, T.D. Stevens. M.F.G. Antitumor imidazo[5,1-d]-1,2,3,5-tetrazines: compounds modified at the 3-position overcome resistance in human glioblastoma cell lines. MedChemComm, 2016, 7, 2332-2343.
[http://dx.doi.org/10.1039/C6MD00384B]
[207]
Yang, Z.; Wei, D.; Dai, X.; Stevens, M.F.G.; Bradshaw, T.D.; Luo, Y.; Zhang, J. C8-Substituted imidazotetrazine analogs overcome temozolomide resistance by inducing DNA adducts and DNA damage. Front. Oncol., 2019, 9, 485.
[http://dx.doi.org/10.3389/fonc.2019.00485] [PMID: 31263673]
[208]
Bouzinab, K.; Summers, H.S.; Stevens, M.F.G.; Moody, C.J.; Thomas, N.R.; Gershkovich, P.; Weston, N.; Ashford, M.B.; Bradshaw, T.D.; Turyanska, L. Delivery of temozolomide and N3-propargyl analog to brain tumors using an apoferritin nanocage. ACS Appl. Mater. Interfaces, 2020, 12(11), 12609-12617.
[http://dx.doi.org/10.1021/acsami.0c01514] [PMID: 32073826]
[209]
Chen, T.C.; Cho, H.Y.; Wang, W.; Wetzel, S.J.; Singh, A.; Nguyen, J.; Hofman, F.M.; Schönthal, A.H. Chemotherapeutic effect of a novel temozolomide analog on nasopharyngeal carcinoma in vitro and in vivo. J. Biomed. Sci., 2015, 22, 71.
[http://dx.doi.org/10.1186/s12929-015-0175-6] [PMID: 26282951]
[210]
Beier, C.P.; Schmid, C.; Gorlia, T.; Kleinletzenberger, C.; Beier, D.; Grauer, O.; Steinbrecher, A.; Hirschmann, B.; Brawanski, A.; Dietmaier, C.; Jauch-Worley, T.; Kölbl, O.; Pietsch, T.; Proescholdt, M.; Rümmele, P.; Muigg, A.; Stockhammer, G.; Hegi, M.; Bogdahn, U.; Hau, P. RNOP-09: pegylated liposomal doxorubicine and prolonged temozolomide in addition to radiotherapy in newly diagnosed glioblastoma--a phase II study. BMC Cancer, 2009, 9(308), 308.
[http://dx.doi.org/10.1186/1471-2407-9-308] [PMID: 19725960]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy