The Delicate Equilibrium between Oxidants and Antioxidants in Brain Glioma

Author(s): María Jesús Ramírez-Expósito, José Manuel Martínez-Martos*.

Journal Name: Current Neuropharmacology

Volume 17 , Issue 4 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Gliomas are the most frequent brain tumors in the adult population and unfortunately the adjuvant therapies are not effective. Brain tumorigenesis has been related both to the increased levels of free radicals as inductors of severe damages in healthy cells, but also with the reduced response of endogenous enzyme and non-enzymatic antioxidant defenses. In turn, both processes induce the change to malignant cells. In this review, we analyzed the role of the imbalance between free radicals production and antioxidant mechanism in the development and progression of gliomas but also the influence of redox status on the two major distinctive forms of programmed cell death related to cancer: apoptosis and autophagy. These data may be the reference to the development of new pharmacological options based on redox microenvironment for glioma treatment.

Keywords: Glioma, reactive oxygen species, antioxidant systems, autophagy, apoptosis.

[1]
Caruso, G.; Caffo, M. Antisense oligonucleotides in the treatment of cerebral gliomas. Review of concerning patents. Recent Patents CNS Drug Discov., 2014, 9(1), 2-12.
[http://dx.doi.org/10.2174/1574889809666140307113439] [PMID: 24605941]
[2]
Rinaldi, M.; Caffo, M.; Minutoli, L.; Marini, H.; Abbritti, R.V.; Squadrito, F.; Trichilo, V.; Valenti, A.; Barresi, V.; Altavilla, D.; Passalacqua, M.; Caruso, G. ROS and brain gliomas: An overview of potential and innovative therapeutic strategies. Int. J. Mol. Sci., 2016, 17(6), E984.
[http://dx.doi.org/10.3390/ijms17060984] [PMID: 27338365]
[3]
Bondy, M.L.; Scheurer, M.E.; Malmer, B.; Barnholtz-Sloan, J.S.; Davis, F.G.; Il’yasova, D.; Kruchko, C.; McCarthy, B.J.; Rajaraman, P.; Schwartzbaum, J.A.; Sadetzki, S.; Schlehofer, B.; Tihan, T.; Wiemels, J.L.; Wrensch, M.; Buffler, P.A. Brain tumor epidemiology, C. brain tumor epidemiology: Consensus from the brain tumor epidemiology consortium. Cancer, 2008, 113(7)(Suppl.), 1953-1968.
[http://dx.doi.org/10.1002/cncr.23741] [PMID: 18798534]
[4]
Davis, F.G.; Malmer, B.S.; Aldape, K.; Barnholtz-Sloan, J.S.; Bondy, M.L.; Brännström, T.; Bruner, J.M.; Burger, P.C.; Collins, V.P.; Inskip, P.D.; Kruchko, C.; McCarthy, B.J.; McLendon, R.E.; Sadetzki, S.; Tihan, T.; Wrensch, M.R.; Buffler, P.A. Issues of diagnostic review in brain tumor studies: From the Brain Tumor Epidemiology Consortium. Cancer Epidemiol. Biomarkers Prev., 2008, 17(3), 484-489.
[http://dx.doi.org/10.1158/1055-9965.EPI-07-0725] [PMID: 18349266]
[5]
Louis, D.N.; Ohgaki, H.; Wiestler, O.D.; Cavenee, W.K.; Burger, P.C.; Jouvet, A.; Scheithauer, B.W.; Kleihues, P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol., 2007, 114(2), 97-109.
[http://dx.doi.org/10.1007/s00401-007-0243-4] [PMID: 17618441]
[6]
Illán-Cabeza, N.A.; García-García, A.R.; Martínez-Martos, J.M.; Ramírez-Expósito, M.J.; Peña-Ruiz, T.; Moreno-Carretero, M.N. A potential antitumor agent, (6-amino-1-methyl-5-nitrosouracilato-N3)-triphenylphosphine-gold(I): Structural studies and in vivo biological effects against experimental glioma. Eur. J. Med. Chem., 2013, 64, 260-272.
[http://dx.doi.org/10.1016/j.ejmech.2013.03.067] [PMID: 23644209]
[7]
Deng, Z.; Hu, J.; Liu, S. Reactive oxygen, nitrogen, and sulfur species (RONSS)-responsive polymersomes for triggered drug release. Macromol. Rapid Commun., 2017, 38(11)
[http://dx.doi.org/10.1002/marc.201600685] [PMID: 28240442]
[8]
Wu, C.C.; Bratton, S.B. Regulation of the intrinsic apoptosis pathway by reactive oxygen species. Antioxid. Redox Signal., 2013, 19(6), 546-558.
[http://dx.doi.org/10.1089/ars.2012.4905] [PMID: 22978471]
[9]
Sosa, V.; Moliné, T.; Somoza, R.; Paciucci, R.; Kondoh, H. LLeonart, M.E. Oxidative stress and cancer: An overview. Ageing Res. Rev., 2013, 12(1), 376-390.
[http://dx.doi.org/10.1016/j.arr.2012.10.004] [PMID: 23123177]
[10]
Hung, Y.C.; Pan, T.L.; Hu, W.L. Roles of reactive oxygen species in anticancer therapy with Salvia miltiorrhiza Bunge. Oxid. Med. Cell. Longev., 2016, 2016, 5293284.
[http://dx.doi.org/10.1155/2016/5293284] [PMID: 27579153]
[11]
Yang, Y.; Karakhanova, S.; Hartwig, W.; D’Haese, J.G.; Philippov, P.P.; Werner, J.; Bazhin, A.V. Mitochondria and mitochondrial ROS in cancer: Novel targets for anticancer therapy. J. Cell. Physiol., 2016, 231(12), 2570-2581.
[http://dx.doi.org/10.1002/jcp.25349] [PMID: 26895995]
[12]
Sabharwal, S.S.; Schumacker, P.T. Mitochondrial ROS in cancer: Initiators, amplifiers or an Achilles’ heel? Nat. Rev. Cancer, 2014, 14(11), 709-721.
[http://dx.doi.org/10.1038/nrc3803] [PMID: 25342630]
[13]
Bauer, G. Targeting extracellular ROS signaling of tumor cells. Anticancer Res., 2014, 34(4), 1467-1482.
[PMID: 24692674]
[14]
Martín, V.; Herrera, F.; García-Santos, G.; Antolín, I.; Rodriguez-Blanco, J.; Rodriguez, C. Signaling pathways involved in antioxidant control of glioma cell proliferation. Free Radic. Biol. Med., 2007, 42(11), 1715-1722.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.02.028] [PMID: 17462539]
[15]
Anderson, K.N.; Bejcek, B.E. Parthenolide induces apoptosis in glioblastomas without affecting NF-kappaB. J. Pharmacol. Sci., 2008, 106(2), 318-320.
[http://dx.doi.org/10.1254/jphs.SC0060164] [PMID: 18277052]
[16]
Jackson, C.; Ruzevick, J.; Amin, A.G.; Lim, M. Potential role for STAT3 inhibitors in glioblastoma. Neurosurg. Clin. N. Am., 2012, 23(3), 379-389.
[http://dx.doi.org/10.1016/j.nec.2012.04.002] [PMID: 22748651]
[17]
Yu, M.O.; Park, K.J.; Park, D.H.; Chung, Y.G.; Chi, S.G.; Kang, S.H. Reactive oxygen species production has a critical role in hypoxia-induced Stat3 activation and angiogenesis in human glioblastoma. J. Neurooncol., 2015, 125(1), 55-63.
[http://dx.doi.org/10.1007/s11060-015-1889-8] [PMID: 26297045]
[18]
Hsieh, C.H.; Lee, C.H.; Liang, J.A.; Yu, C.Y.; Shyu, W.C. Cycling hypoxia increases U87 glioma cell radioresistance via ROS induced higher and long-term HIF-1 signal transduction activity. Oncol. Rep., 2010, 24(6), 1629-1636.
[http://dx.doi.org/10.3892/or_00001027] [PMID: 21042761]
[19]
Wang, P.; Wan, W.; Xiong, S.; Wang, J.; Zou, D.; Lan, C.; Yu, S.; Liao, B.; Feng, H.; Wu, N. HIF1α regulates glioma chemosensitivity through the transformation between differentiation and dedifferentiation in various oxygen levels. Sci. Rep., 2017, 7(1), 7965.
[http://dx.doi.org/10.1038/s41598-017-06086-2] [PMID: 28801626]
[20]
Ahmad, F.; Ghosh, S.; Sinha, S.; Joshi, S.D.; Mehta, V.S.; Sen, E. TGF-β-induced hCG-β regulates redox homeostasis in glioma cells. Mol. Cell. Biochem., 2015, 399(1-2), 105-112.
[http://dx.doi.org/10.1007/s11010-014-2237-6] [PMID: 25300619]
[21]
Park, E.J.; Park, K. Induction of oxidative stress and inflammatory cytokines by manganese chloride in cultured T98G cells, human brain glioblastoma cell line. Toxicol. In Vitro, 2010, 24(2), 472-479.
[http://dx.doi.org/10.1016/j.tiv.2009.09.022] [PMID: 19815061]
[22]
Wu, Q.; Ni, X. ROS-mediated DNA methylation pattern alterations in carcinogenesis. Curr. Drug Targets, 2015, 16(1), 13-19.
[http://dx.doi.org/10.2174/1389450116666150113121054] [PMID: 25585126]
[23]
Marengo, B.; Nitti, M.; Furfaro, A.L.; Colla, R.; Ciucis, C.D.; Marinari, U.M.; Pronzato, M.A.; Traverso, N.; Domenicotti, C. Redox homeostasis and cellular antioxidant systems: Crucial players in cancer growth and therapy. Oxid. Med. Cell. Longev., 2016, 2016, 6235641.
[http://dx.doi.org/10.1155/2016/6235641] [PMID: 27418953]
[24]
Dewaele, M.; Maes, H.; Agostinis, P. ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Cancer Metastasis Rev., 2006, 25, 669-705.
[PMID: 17160556]
[25]
Yang, Y.; Karakhanova, S.; Werner, J.; Bazhin, A.V. Reactive oxygen species in cancer biology and anticancer therapy. Curr. Med. Chem., 2013, 20(30), 3677-3692.
[http://dx.doi.org/10.2174/0929867311320999165] [PMID: 23862622]
[26]
Carrera, M.P.; Ramírez-Expósito, M.J.; Martínez-Martos, J.M. Actual and potential agents and biomarkers in the treatment of cancer. Anticancer. Agents Med. Chem., 2009, 9(5), 500-516.
[http://dx.doi.org/10.2174/187152009788451824] [PMID: 19519292]
[27]
Federico, A.; Morgillo, F.; Tuccillo, C.; Ciardiello, F.; Loguercio, C. Chronic inflammation and oxidative stress in human carcinogenesis. Int. J. Cancer, 2007, 121(11), 2381-2386.
[http://dx.doi.org/10.1002/ijc.23192] [PMID: 17893868]
[28]
Nair, U.; Bartsch, H.; Nair, J. Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic. Biol. Med., 2007, 43(8), 1109-1120.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.07.012] [PMID: 17854706]
[29]
Zhang, Y.; Chen, S.Y.; Hsu, T.; Santella, R.M. Immunohistochemical detection of malondialdehyde-DNA adducts in human oral mucosa cells. Carcinogenesis, 2002, 23(1), 207-211.
[http://dx.doi.org/10.1093/carcin/23.1.207] [PMID: 11756243]
[30]
M.J.. Mayas, M.D.; Carrera, M.P.; Cobo, M.P.; García, M.J.; martínez-Martos, J.M. Oxidative stress parameters in rat with gliomas induced by transplacental N-ethyl-N-nitrosourea exposure. Eur. J. Neurol., 2012, 19, 772-772.
[31]
Zengin, E.; Atukeren, P.; Kokoglu, E.; Gumustas, M.K.; Zengin, U. Alterations in lipid peroxidation and antioxidant status in different types of intracranial tumors within their relative peritumoral tissues. Clin. Neurol. Neurosurg., 2009, 111(4), 345-351.
[http://dx.doi.org/10.1016/j.clineuro.2008.11.008] [PMID: 19117666]
[32]
Cirak, B.; Inci, S.; Palaoglu, S.; Bertan, V. Lipid peroxidation in cerebral tumors. Clin. Chim. Acta, 2003, 327(1-2), 103-107.
[http://dx.doi.org/10.1016/S0009-8981(02)00334-0] [PMID: 12482624]
[33]
Ramirez-Exposito, M.J.; Carrera, M.P.; Mayas, M.D.; Martínez-Martos, J.M. Redox status in transplacental ethyl-nitrosourea-induced experimental glioma. In: 9th FENS Forum of Neuroscience, Milan (Italy)2014, p. 423.
[34]
Roszkowski, K.; Olinski, R. Urinary 8-oxoguanine as a predictor of survival in patients undergoing radiotherapy. Cancer Epidemiol. Biomarkers Prev., 2012, 21(4), 629-634.
[http://dx.doi.org/10.1158/1055-9965.EPI-11-0981] [PMID: 22301827]
[35]
Lian, M.; Zhang, X.; Wang, H.; Liu, H.; Chen, W.; Guo, S. Increased 8-hydroxydeoxyguanosine in high-grade gliomas is associated with activation of autophagy. Int. J. Neurosci., 2014, 124(12), 926-934.
[http://dx.doi.org/10.3109/00207454.2014.891998] [PMID: 24617962]
[36]
Chang, S.M.; Parney, I.F.; Huang, W.; Anderson, F.A., Jr; Asher, A.L.; Bernstein, M.; Lillehei, K.O.; Brem, H.; Berger, M.S.; Laws, E.R. Patterns of care for adults with newly diagnosed malignant glioma. JAMA, 2005, 293(5), 557-564.
[http://dx.doi.org/10.1001/jama.293.5.557] [PMID: 15687310]
[37]
Tuzgen, S.; Hanimoglu, H.; Tanriverdi, T.; Kacira, T.; Sanus, G.Z.; Atukeren, P.; Dashti, R.; Gumustas, K.; Canbaz, B.; Kaynar, M.Y. Relationship between DNA damage and total antioxidant capacity in patients with glioblastoma multiforme. Clin. Oncol. (R. Coll. Radiol.), 2007, 19(3), 177-181.
[http://dx.doi.org/10.1016/j.clon.2006.11.012] [PMID: 17359903]
[38]
lida, T.; A., F.; Kawashima, M. Accumulation of 8-oxo-2´-deoxyguanosine and increased expression of hMTH1 protein in brain tumors. Neuro-oncol., 2011, 3, 73-81.
[39]
Chuang, J.I.; Chang, T.Y.; Liu, H.S. Glutathione depletion-induced apoptosis of Ha-ras-transformed NIH3T3 cells can be prevented by melatonin. Oncogene, 2003, 22(9), 1349-1357.
[http://dx.doi.org/10.1038/sj.onc.1206289] [PMID: 12618760]
[40]
Guha, P.; Dey, A.; Sen, R.; Chatterjee, M.; Chattopadhyay, S.; Bandyopadhyay, S.K. Intracellular GSH depletion triggered mitochondrial Bax translocation to accomplish resveratrol-induced apoptosis in the U937 cell line. J. Pharmacol. Exp. Ther., 2011, 336(1), 206-214.
[http://dx.doi.org/10.1124/jpet.110.171983] [PMID: 20876229]
[41]
Salazar-Ramiro, A.; Ramírez-Ortega, D.; Pérez de la Cruz, V.; Hérnandez-Pedro, N.Y.; González-Esquivel, D.F.; Sotelo, J.; Pineda, B. Role of redox status in development of glioblastoma. Front. Immunol., 2016, 7, 156.
[http://dx.doi.org/10.3389/fimmu.2016.00156] [PMID: 27199982]
[42]
Traverso, N.; Ricciarelli, R.; Nitti, M.; Marengo, B.; Furfaro, A.L.; Pronzato, M.A.; Marinari, U.M.; Domenicotti, C. Role of glutathione in cancer progression and chemoresistance. Oxid. Med. Cell. Longev., 2013, 2013, 972913.
[http://dx.doi.org/10.1155/2013/972913] [PMID: 23766865]
[43]
Gottesman, M.M.; Fojo, T.; Bates, S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer, 2002, 2(1), 48-58.
[http://dx.doi.org/10.1038/nrc706] [PMID: 11902585]
[44]
Kretz-Remy, C.; Arrigo, A.P. Gene expression and thiol redox state. Methods Enzymol., 2002, 348, 200-215.
[http://dx.doi.org/10.1016/S0076-6879(02)48639-9] [PMID: 11885273]
[45]
Harris, I.S.; Treloar, A.E.; Inoue, S.; Sasaki, M.; Gorrini, C.; Lee, K.C.; Yung, K.Y.; Brenner, D.; Knobbe-Thomsen, C.B.; Cox, M.A.; Elia, A.; Berger, T.; Cescon, D.W.; Adeoye, A.; Brüstle, A.; Molyneux, S.D.; Mason, J.M.; Li, W.Y.; Yamamoto, K.; Wakeham, A.; Berman, H.K.; Khokha, R.; Done, S.J.; Kavanagh, T.J.; Lam, C.W.; Mak, T.W. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell, 2015, 27(2), 211-222.
[http://dx.doi.org/10.1016/j.ccell.2014.11.019] [PMID: 25620030]
[46]
Navarro, J.; Obrador, E.; Carretero, J.; Petschen, I.; Aviñó, J.; Perez, P.; Estrela, J.M. Changes in glutathione status and the antioxidant system in blood and in cancer cells associate with tumour growth in vivo. Free Radic. Biol. Med., 1999, 26(3-4), 410-418.
[http://dx.doi.org/10.1016/S0891-5849(98)00213-5] [PMID: 9895233]
[47]
Woźniak, B.; Woźniak, A.; Kasprzak, H.A.; Drewa, G.; Mila-Kierzenkowska, C.; Drewa, T.; Planutis, G. Lipid peroxidation and activity of some antioxidant enzymes in patients with glioblastoma and astrocytoma. J. Neurooncol., 2007, 81(1), 21-26.
[http://dx.doi.org/10.1007/s11060-006-9202-5] [PMID: 16773213]
[48]
Oberley, L.W.; Buettner, G.R. Role of superoxide dismutase in cancer: a review. Cancer Res., 1979, 39(4), 1141-1149.
[PMID: 217531]
[49]
Hempel, N.; Carrico, P.M.; Melendez, J.A. Manganese superoxide dismutase (Sod2) and redox-control of signaling events that drive metastasis. Anticancer. Agents Med. Chem., 2011, 11(2), 191-201.
[http://dx.doi.org/10.2174/187152011795255911] [PMID: 21434856]
[50]
Dhar, S.K.; St Clair, D.K. Manganese superoxide dismutase regulation and cancer. Free Radic. Biol. Med., 2012, 52(11-12), 2209-2222.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.03.009] [PMID: 22561706]
[51]
Che, M.; Wang, R.; Li, X.; Wang, H.Y.; Zheng, X.F.S. Expanding roles of superoxide dismutases in cell regulation and cancer. Drug Discov. Today, 2016, 21(1), 143-149.
[http://dx.doi.org/10.1016/j.drudis.2015.10.001] [PMID: 26475962]
[52]
Popov, B.; Gadjeva, V.; Valkanov, P.; Popova, S.; Tolekova, A. Lipid peroxidation, superoxide dismutase and catalase activities in brain tumor tissues. Arch. Physiol. Biochem., 2003, 111(5), 455-459.
[http://dx.doi.org/10.3109/13813450312331342328] [PMID: 16026034]
[53]
Aggarwal, S.; Subberwal, M.; Kumar, S.; Sharma, M. Brain tumor and role of beta-carotene, a-tocopherol, superoxide dismutase and glutathione peroxidase. J. Cancer Res. Ther., 2006, 2(1), 24-27.
[http://dx.doi.org/10.4103/0973-1482.19771] [PMID: 17998669]
[54]
Gönenç, A.; Ozkan, Y.; Torun, M.; Simşek, B. Plasma malondialdehyde (MDA) levels in breast and lung cancer patients. J. Clin. Pharm. Ther., 2001, 26(2), 141-144.
[http://dx.doi.org/10.1046/j.1365-2710.2001.00334.x] [PMID: 11350537]
[55]
Del Maestro, R.F.; McDonald, W.R. A. Oxy radicals and their scavenger systems., 1983, 2, 28-35.
[56]
Jeong, C.H.; Joo, S.H. Downregulation of reactive oxygen species in apoptosis. J. Cancer Prev., 2016, 21(1), 13-20.
[http://dx.doi.org/10.15430/JCP.2016.21.1.13] [PMID: 27051644]
[57]
Yilmaz, N.; Dulger, H.; Kiymaz, N.; Yilmaz, C.; Bayram, I.; Ragip, B.; Oğer, M. Lipid peroxidation in patients with brain tumor. Int. J. Neurosci., 2006, 116(8), 937-943.
[http://dx.doi.org/10.1080/00207450600553141] [PMID: 16861159]
[58]
Preuss, M.; Girnun, G.D.; Darby, C.J.; Khoo, N.; Spector, A.A.; Robbins, M.E. Role of antioxidant enzyme expression in the selective cytotoxic response of glioma cells to gamma-linolenic acid supplementation. Free Radic. Biol. Med., 2000, 28(7), 1143-1156.
[http://dx.doi.org/10.1016/S0891-5849(00)00210-0] [PMID: 10832077]
[59]
Smith, P.S.; Zhao, W.; Spitz, D.R.; Robbins, M.E. Inhibiting catalase activity sensitizes 36B10 rat glioma cells to oxidative stress. Free Radic. Biol. Med., 2007, 42(6), 787-797.
[http://dx.doi.org/10.1016/j.freeradbiomed.2006.11.032] [PMID: 17320761]
[60]
Hirrlinger, J.; Dringen, R. The cytosolic redox state of astrocytes: Maintenance, regulation and functional implications for metabolite trafficking. Brain Res. Brain Res. Rev., 2010, 63(1-2), 177-188.
[http://dx.doi.org/10.1016/j.brainresrev.2009.10.003] [PMID: 19883686]
[61]
Dokic, I.; Hartmann, C.; Herold-Mende, C.; Régnier-Vigouroux, A. Glutathione peroxidase 1 activity dictates the sensitivity of glioblastoma cells to oxidative stress. Glia, 2012, 60(11), 1785-1800.
[http://dx.doi.org/10.1002/glia.22397] [PMID: 22951908]
[62]
Tanriverdi, T.; Hanimoglu, H.; Kacira, T.; Sanus, G.Z.; Kemerdere, R.; Atukeren, P.; Gumustas, K.; Canbaz, B.; Kaynar, M.Y. Glutathione peroxidase, glutathione reductase and protein oxidation in patients with glioblastoma multiforme and transitional meningioma. J. Cancer Res. Clin. Oncol., 2007, 133(9), 627-633.
[http://dx.doi.org/10.1007/s00432-007-0212-2] [PMID: 17457608]
[63]
Rao, G.M.; Rao, A.V.; Raja, A.; Rao, S.; Rao, A. Role of antioxidant enzymes in brain tumours. Clin. Chim. Acta, 2000, 296(1-2), 203-212.
[http://dx.doi.org/10.1016/S0009-8981(00)00219-9] [PMID: 10807983]
[64]
Kasibhatla, S.; Tseng, B. Why target apoptosis in cancer treatment? Mol. Cancer Ther., 2003, 2(6), 573-580.
[PMID: 12813137]
[65]
Levine, B.; Klionsky, D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell, 2004, 6(4), 463-477.
[http://dx.doi.org/10.1016/S1534-5807(04)00099-1] [PMID: 15068787]
[66]
Pallichankandy, S.; Rahman, A.; Thayyullathil, F.; Galadari, S. ROS-dependent activation of autophagy is a critical mechanism for the induction of anti-glioma effect of sanguinarine. Free Radic. Biol. Med., 2015, 89, 708-720.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.10.404] [PMID: 26472194]
[67]
Eisenberg, T.; Knauer, H.; Schauer, A.; Büttner, S.; Ruckenstuhl, C.; Carmona-Gutierrez, D.; Ring, J.; Schroeder, S.; Magnes, C.; Antonacci, L.; Fussi, H.; Deszcz, L.; Hartl, R.; Schraml, E.; Criollo, A.; Megalou, E.; Weiskopf, D.; Laun, P.; Heeren, G.; Breitenbach, M.; Grubeck-Loebenstein, B.; Herker, E.; Fahrenkrog, B.; Fröhlich, K.U.; Sinner, F.; Tavernarakis, N.; Minois, N.; Kroemer, G.; Madeo, F. Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol., 2009, 11(11), 1305-1314.
[http://dx.doi.org/10.1038/ncb1975] [PMID: 19801973]
[68]
Kaminskyy, V.O.; Zhivotovsky, B. Free radicals in cross talk between autophagy and apoptosis. Antioxid. Redox Signal., 2014, 21(1), 86-102.
[http://dx.doi.org/10.1089/ars.2013.5746] [PMID: 24359220]
[69]
Turrens, J.F. Mitochondrial formation of reactive oxygen species. J. Physiol., 2003, 552(Pt 2), 335-344.
[http://dx.doi.org/10.1113/jphysiol.2003.049478] [PMID: 14561818]
[70]
de Miguel, M.; Cordero, M.D. Oxidative therapy against cancer, oxidative stress and diseases In Teach, 2012.
[71]
Pilkington, G.J.; Parker, K.; Murray, S.A. Approaches to mitochondrially mediated cancer therapy. Semin. Cancer Biol., 2008, 18(3), 226-235.
[http://dx.doi.org/10.1016/j.semcancer.2007.12.006] [PMID: 18203619]
[72]
Chandra, J.; Samali, A.; Orrenius, S. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med., 2000, 29(3-4), 323-333.
[http://dx.doi.org/10.1016/S0891-5849(00)00302-6] [PMID: 11035261]
[73]
Ishikawa, K.; Takenaga, K.; Akimoto, M.; Koshikawa, N.; Yamaguchi, A.; Imanishi, H.; Nakada, K.; Honma, Y.; Hayashi, J. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science, 2008, 320(5876), 661-664.
[http://dx.doi.org/10.1126/science.1156906] [PMID: 18388260]
[74]
Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov., 2009, 8(7), 579-591.
[http://dx.doi.org/10.1038/nrd2803] [PMID: 19478820]
[75]
Yu, L.; Wan, F.; Dutta, S.; Welsh, S.; Liu, Z.; Freundt, E.; Baehrecke, E.H.; Lenardo, M. Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA, 2006, 103(13), 4952-4957.
[http://dx.doi.org/10.1073/pnas.0511288103] [PMID: 16547133]
[76]
Trachootham, D.; Lu, W.; Ogasawara, M.A.; Nilsa, R.D.; Huang, P. Redox regulation of cell survival. Antioxid. Redox Signal., 2008, 10(8), 1343-1374.
[http://dx.doi.org/10.1089/ars.2007.1957] [PMID: 18522489]
[77]
Scherz-Shouval, R.; Elazar, Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci., 2011, 36(1), 30-38.
[http://dx.doi.org/10.1016/j.tibs.2010.07.007] [PMID: 20728362]
[78]
Choi, A.M.; Ryter, S.W.; Levine, B. Autophagy in human health and disease. N. Engl. J. Med., 2013, 368(19), 1845-1846.
[http://dx.doi.org/10.1056/NEJMc1303158] [PMID: 23656658]
[79]
White, E. Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer, 2012, 12(6), 401-410.
[http://dx.doi.org/10.1038/nrc3262] [PMID: 22534666]
[80]
Kenific, C.M.; Debnath, J. Cellular and metabolic functions for autophagy in cancer cells. Trends Cell Biol., 2015, 25(1), 37-45.
[http://dx.doi.org/10.1016/j.tcb.2014.09.001] [PMID: 25278333]
[81]
Poillet-Perez, L.; Despouy, G.; Delage-Mourroux, R.; Boyer-Guittaut, M. Interplay between ROS and autophagy in cancer cells, from tumor initiation to cancer therapy. Redox Biol., 2015, 4, 184-192.
[http://dx.doi.org/10.1016/j.redox.2014.12.003] [PMID: 25590798]
[82]
Morselli, E.; Galluzzi, L.; Kepp, O.; Vicencio, J.M.; Criollo, A.; Maiuri, M.C.; Kroemer, G. Anti- and pro-tumor functions of autophagy. Biochim. Biophys. Acta, 2009, 1793(9), 1524-1532.
[http://dx.doi.org/10.1016/j.bbamcr.2009.01.006] [PMID: 19371598]
[83]
Debnath, J. The multifaceted roles of autophagy in tumors-implications for breast cancer. J. Mammary Gland Biol. Neoplasia, 2011, 16(3), 173-187.
[http://dx.doi.org/10.1007/s10911-011-9223-3] [PMID: 21779879]
[84]
Morselli, E.; Galluzzi, L.; Kepp, O.; Mariño, G.; Michaud, M.; Vitale, I.; Maiuri, M.C.; Kroemer, G. Oncosuppressive functions of autophagy. Antioxid. Redox Signal., 2011, 14(11), 2251-2269.
[http://dx.doi.org/10.1089/ars.2010.3478] [PMID: 20712403]
[85]
Brahimi-Horn, M.C.; Bellot, G.; Pouysségur, J. Hypoxia and energetic tumour metabolism. Curr. Opin. Genet. Dev., 2011, 21(1), 67-72.
[http://dx.doi.org/10.1016/j.gde.2010.10.006] [PMID: 21074987]
[86]
Lazova, R.; Camp, R.L.; Klump, V.; Siddiqui, S.F.; Amaravadi, R.K.; Pawelek, J.M. Punctate LC3B expression is a common feature of solid tumors and associated with proliferation, metastasis, and poor outcome. Clin. Cancer Res., 2012, 18(2), 370-379.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-1282] [PMID: 22080440]
[87]
Lu, Z.; Luo, R.Z.; Lu, Y.; Zhang, X.; Yu, Q.; Khare, S.; Kondo, S.; Kondo, Y.; Yu, Y.; Mills, G.B.; Liao, W.S.; Bast, R.C., Jr The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J. Clin. Invest., 2008, 118(12), 3917-3929.
[PMID: 19033662]
[88]
Yang, Z.J.; Chee, C.E.; Huang, S.; Sinicrope, F.A. The role of autophagy in cancer: therapeutic implications. Mol. Cancer Ther., 2011, 10(9), 1533-1541.
[http://dx.doi.org/10.1158/1535-7163.MCT-11-0047] [PMID: 21878654]
[89]
Degenhardt, K.; Mathew, R.; Beaudoin, B.; Bray, K.; Anderson, D.; Chen, G.; Mukherjee, C.; Shi, Y.; Gélinas, C.; Fan, Y.; Nelson, D.A.; Jin, S.; White, E. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell, 2006, 10(1), 51-64.
[http://dx.doi.org/10.1016/j.ccr.2006.06.001] [PMID: 16843265]
[90]
White, E.; DiPaola, R.S. The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res., 2009, 15(17), 5308-5316.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-5023] [PMID: 19706824]
[91]
Maiuri, M.C.; Zalckvar, E.; Kimchi, A.; Kroemer, G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol., 2007, 8(9), 741-752.
[http://dx.doi.org/10.1038/nrm2239] [PMID: 17717517]
[92]
Miracco, C.; Cosci, E.; Oliveri, G.; Luzi, P.; Pacenti, L.; Monciatti, I.; Mannucci, S.; De Nisi, M.C.; Toscano, M.; Malagnino, V.; Falzarano, S.M.; Pirtoli, L.; Tosi, P. Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int. J. Oncol., 2007, 30(2), 429-436.
[PMID: 17203225]
[93]
Pirtoli, L.; Cevenini, G.; Tini, P.; Vannini, M.; Oliveri, G.; Marsili, S.; Mourmouras, V.; Rubino, G.; Miracco, C. The prognostic role of Beclin 1 protein expression in high-grade gliomas. Autophagy, 2009, 5(7), 930-936.
[http://dx.doi.org/10.4161/auto.5.7.9227] [PMID: 19556884]
[94]
Palumbo, S.; Comincini, S. Autophagy and ionizing radiation in tumors: the “survive or not survive” dilemma. J. Cell. Physiol., 2013, 228(1), 1-8.
[http://dx.doi.org/10.1002/jcp.24118] [PMID: 22585676]
[95]
Palumbo, S.; Pirtoli, L.; Tini, P.; Cevenini, G.; Calderaro, F.; Toscano, M.; Miracco, C.; Comincini, S. Different involvement of autophagy in human malignant glioma cell lines undergoing irradiation and temozolomide combined treatments. J. Cell. Biochem., 2012, 113(7), 2308-2318.
[http://dx.doi.org/10.1002/jcb.24102] [PMID: 22345070]
[96]
Zhuang, W.; Qin, Z.; Liang, Z. The role of autophagy in sensitizing malignant glioma cells to radiation therapy. Acta Biochim. Biophys. Sin. (Shanghai), 2009, 41(5), 341-351.
[http://dx.doi.org/10.1093/abbs/gmp028] [PMID: 19430698]
[97]
Zhuang, W.; Li, B.; Long, L.; Chen, L.; Huang, Q.; Liang, Z. Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity. Int. J. Cancer, 2011, 129(11), 2720-2731.
[http://dx.doi.org/10.1002/ijc.25975] [PMID: 21384342]
[98]
Kaza, N.; Kohli, L.; Roth, K.A. Autophagy in brain tumors: a new target for therapeutic intervention. Brain Pathol., 2012, 22(1), 89-98.
[http://dx.doi.org/10.1111/j.1750-3639.2011.00544.x] [PMID: 22150924]
[99]
Isakovic, A.M.; Dulovic, M.; Markovic, I.; Kravic-Stevovic, T.; Bumbasirevic, V.; Trajkovic, V.; Isakovic, A. Autophagy suppression sensitizes glioma cells to IMP dehydrogenase inhibition-induced apoptotic death. Exp. Cell Res., 2017, 350(1), 32-40.
[http://dx.doi.org/10.1016/j.yexcr.2016.11.001] [PMID: 27818246]
[100]
Gammoh, N.; Fraser, J.; Puente, C.; Syred, H.M.; Kang, H.; Ozawa, T.; Lam, D.; Acosta, J.C.; Finch, A.J.; Holland, E.; Jiang, X. Suppression of autophagy impedes glioblastoma development and induces senescence. Autophagy, 2016, 12(9), 1431-1439.
[http://dx.doi.org/10.1080/15548627.2016.1190053] [PMID: 27304681]
[101]
Bi, Y.; Shen, C.; Li, C.; Liu, Y.; Gao, D.; Shi, C.; Peng, F.; Liu, Z.; Zhao, B.; Zheng, Z.; Wang, X.; Hou, X.; Liu, H.; Wu, J.; Zou, H.; Wang, K.; Zhong, C.; Zhang, J.; Shi, C.; Zhao, S. Inhibition of autophagy induced by quercetin at a late stage enhances cytotoxic effects on glioma cells. Tumour Biol., 2016, 37(3), 3549-3560.
[http://dx.doi.org/10.1007/s13277-015-4125-4] [PMID: 26454746]
[102]
Li, C.; Liu, Y.; Liu, H.; Zhang, W.; Shen, C.; Cho, K.; Chen, X.; Peng, F.; Bi, Y.; Hou, X.; Yang, Z.; Zheng, Z.; Wang, K.; Wang, X.; Zhang, J.; Zhong, C.; Zou, H.; Zhang, X.; Zhao, S. Impact of autophagy inhibition at different stages on cytotoxic effect of autophagy inducer in glioblastoma cells. Cell. Physiol. Biochem., 2015, 35(4), 1303-1316.
[http://dx.doi.org/10.1159/000373952] [PMID: 25721868]
[103]
Wang, M.C.; Liang, X.; Liu, Z.Y.; Cui, J.; Liu, Y.; Jing, L.; Jiang, L.L.; Ma, J.Q.; Han, L.L.; Guo, Q.Q.; Yang, C.C.; Wang, J.; Wu, T.; Nan, K.J.; Yao, Y. In vitro synergistic antitumor efficacy of sequentially combined chemotherapy/icotinib in non-small cell lung cancer cell lines. Oncol. Rep., 2015, 33(1), 239-249.
[http://dx.doi.org/10.3892/or.2014.3583] [PMID: 25370413]
[104]
Hu, D.; Cao, S.; Zhang, G.; Xiao, Y.; Liu, S.; Shang, Y. Florfenicol-induced mitochondrial dysfunction suppresses cell proliferation and autophagy in fibroblasts. Sci. Rep., 2017, 7(1), 13554.
[http://dx.doi.org/10.1038/s41598-017-13860-9] [PMID: 29051574]
[105]
Agostinelli, E.; Seiler, N. Non-irradiation-derived reactive oxygen species (ROS) and cancer: therapeutic implications. Amino Acids, 2006, 31(3), 341-355.
[http://dx.doi.org/10.1007/s00726-005-0271-8] [PMID: 16680401]
[106]
Kanzawa, T.; Kondo, Y.; Ito, H.; Kondo, S.; Germano, I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res., 2003, 63(9), 2103-2108.
[PMID: 12727826]
[107]
Kondo, Y.; Kondo, S. Autophagy and cancer therapy. Autophagy, 2006, 2(2), 85-90.
[http://dx.doi.org/10.4161/auto.2.2.2463] [PMID: 16874083]
[108]
Chen, Y.; McMillan-Ward, E.; Kong, J.; Israels, S.J.; Gibson, S.B. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ., 2008, 15(1), 171-182.
[http://dx.doi.org/10.1038/sj.cdd.4402233] [PMID: 17917680]
[109]
Gibson, S.B. A matter of balance between life and death: targeting reactive oxygen species (ROS)-induced autophagy for cancer therapy. Autophagy, 2010, 6(7), 835-837.
[http://dx.doi.org/10.4161/auto.6.7.13335] [PMID: 20818163]
[110]
Kalyanaraman, B.; Cheng, G.; Hardy, M.; Ouari, O.; Bennett, B.; Zielonka, J. Teaching the basics of reactive oxygen species and their relevance to cancer biology: Mitochondrial reactive oxygen species detection, redox signaling, and targeted therapies. Redox Biol., 2018, 15, 347-362.
[http://dx.doi.org/10.1016/j.redox.2017.12.012] [PMID: 29306792]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 17
ISSUE: 4
Year: 2019
Page: [342 - 351]
Pages: 10
DOI: 10.2174/1570159X16666180302120925
Price: $58

Article Metrics

PDF: 19
HTML: 3