Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Review Article

Protective Effect of Resveratrol against Glioblastoma: A Review

Author(s): Milad Ashrafizadeh, Reza Mohammadinejad, Tahereh Farkhondeh and Saeed Samarghandian*

Volume 21, Issue 10, 2021

Published on: 29 September, 2020

Page: [1216 - 1227] Pages: 12

DOI: 10.2174/1871520620666200929151139

Price: $65

Abstract

Background: One of the most common tumors of the central nervous system is Glioblastoma (GBM).

Objective: There is not still an appropriate cure for this malignant tumor. Plant-derived natural products have demonstrated great potential in cancer therapy, and Resveratrol (Res) is among them. Therefore, the current study focused on the protective effect of resveratrol against glioblastoma and its underlying mechanism.

Methods: PubMed, Medline, Scopus, Web of Science, and Google Scholar were searched by using the following keywords: Resveratrol, Glioblastoma, Brain tumor, Cancer therapy, Medicinal herbs to July 2020.

Results: Res is a non-flavonoid polyphenol responsible for the protection of plants against pathogen attacks. Res has multiple pharmacological effects, including antioxidant, anti-inflammatory, anti-diabetic, and anti-tumor. Res is capable of penetration into the blood-brain barrier, making it suitable for brain tumor therapy. Besides, Res targets various molecular signaling pathways in cancer therapy.

Conclusion: In the present review, it was found that Res administration is beneficial in GBM therapy by inhibition of proliferation, viability, and migration via modulation of molecular pathways.

Keywords: Resveratrol, glioblastoma, brain tumor, cancer therapy, medicinal herbs, central nervous system.

Graphical Abstract
[1]
Contreras-Ochoa, C.O.; López-Arellano, M.E.; Roblero-Bartolon, G.; Díaz-Chávez, J.; Moreno-Banda, G.L.; Reyna-Figueroa, J.; Munguía-Moreno, J.A.; Madrid-Marina, V.; Lagunas-Martínez, A. Molecular mechanisms of cell death induced in glioblastoma by experimental and antineoplastic drugs: New and old drugs induce apoptosis in glioblastoma. Hum. Exp. Toxicol., 2020, 39(4), 464-476.
[http://dx.doi.org/10.1177/0960327119892041] [PMID: 31823663]
[2]
Kiskova, T.; Kubatka, P.; Büsselberg, D.; Kassayova, M. The plant-derived compound resveratrol in brain cancer: A review. Biomolecules, 2020, 10(1), 161.
[http://dx.doi.org/10.3390/biom10010161] [PMID: 31963897]
[3]
Li, H.; Yuan, H. MiR-1297 negatively regulates metabolic reprogramming in glioblastoma via repressing KPNA2. Hum. Cell, 2020, 33(3), 619-629. doi: 10.1007/s13577-019-00316-7.
[http://dx.doi.org/10.3390/cancers11091231] [PMID: 31450721]
[4]
Silantyev, A.S.; Falzone, L.; Libra, M.; Gurina, O.I.; Kardashova, K.S.; Nikolouzakis, T.K.; Nosyrev, A.E.; Sutton, C.W.; Mitsias, P.D.; Tsatsakis, A. Current and future trends on diagnosis and prognosis of glioblastoma: From molecular biology to proteomics. Cells, 2019, 8(8), 863.
[http://dx.doi.org/10.3390/cells8080863] [PMID: 31405017]
[5]
Bark, J.M.; Kulasinghe, A.; Chua, B.; Day, B.W.; Punyadeera, C. Circulating biomarkers in patients with glioblastoma. Br. J. Cancer, 2020, 122(3), 295-305.
[http://dx.doi.org/10.1038/s41416-019-0603-6.]
[6]
Barresi, V.; Eccher, A.; Simbolo, M.; Cappellini, R.; Ricciardi, G.K.; Calabria, F.; Cancedda, M.; Mazzarotto, R.; Bonetti, B.; Pinna, G.; Sala, F. Diffuse gliomas in patients aged 55 years or over: A suggestion for IDH mutation testing. Neuropathology, 2020, 40(1), 68-74.
[http://dx.doi.org/10.1111/neup.12608.]
[7]
Brown, T.J.; Brennan, M.C.; Li, M.; Church, E.W.; Brandmeir, N.J.; Rakszawski, K.L.; Patel, A.S.; Rizk, E.B.; Suki, D.; Sawaya, R.; Glantz, M. Association of the extent of resection with survival in glioblastoma: A systematic review and meta-analysis. JAMA Oncol., 2016, 2(11), 1460-1469.
[http://dx.doi.org/10.1001/jamaoncol.2016.1373] [PMID: 27310651]
[8]
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]
[9]
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]
[10]
Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.; 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]
[11]
Soffietti, R.; Baumert, B.G.; Bello, L.; von Deimling, A.; Duffau, H.; Frénay, M.; Grisold, W.; Grant, R.; Graus, F.; Hoang-Xuan, K.; Klein, M.; Melin, B.; Rees, J.; Siegal, T.; Smits, A.; Stupp, R.; Wick, W. European Federation of Neurological Societies. Guidelines on management of low-grade gliomas: Report of an EFNS-EANO Task Force. Eur. J. Neurol., 2010, 17(9), 1124-1133.
[http://dx.doi.org/10.1111/j.1468-1331.2010.03151.x] [PMID: 20718851]
[12]
Sullivan, J.P.; Nahed, B.V.; Madden, M.W.; Oliveira, S.M.; Springer, S.; Bhere, D.; Chi, A.S.; Wakimoto, H.; Rothenberg, S.M.; Sequist, L.V.; Kapur, R.; Shah, K.; Iafrate, A.J.; Curry, W.T.; Loeffler, J.S.; Batchelor, T.T.; Louis, D.N.; Toner, M.; Maheswaran, S.; Haber, D.A. Brain tumor cells in circulation are enriched for mesenchymal gene expression. Cancer Discov., 2014, 4(11), 1299-1309.
[http://dx.doi.org/10.1158/2159-8290.CD-14-0471] [PMID: 25139148]
[13]
Sharifi, Z.; Abdulkarim, B.; Meehan, B.; Rak, J.; Daniel, P.; Schmitt, J.; Lauzon, N.; Eppert, K.; Duncan, H.M.; Petrecca, K.; Guiot, M.C.; Jean-Claude, B.; Sabri, S. Mechanisms and antitumor activity of a binary EGFR/DNA-targeting strategy overcomes resistance of glioblastoma stem cells to temozolomide. Clin. Cancer Res., 2019, 25(24), 7594-7608.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0955] [PMID: 31540977]
[14]
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]
[15]
Samarghandian, S.; Azimi-Nezhad, M.; Farkhondeh, T. Immunomodulatory and antioxidant effects of saffron aqueous extract (Crocus sativus L.) on streptozotocin-induced diabetes in rats. Indian Heart J., 2017, 69(2), 151-159.
[16]
Ahmadi, Z.; Roomiani, S.; Bemani, N.; Ashrafizadeh, M. The targeting of autophagy and endoplasmic reticulum stress mechanisms by honokiol therapy. Rev. Clin. Med., 2019, 6(2), 66-73.
[17]
Ahmadi, Z.; Ashrafizadeh, M. Melatonin as a potential modulator of Nrf2. Fundam. Clin. Pharmacol., 2020, 34(1), 11-19.
[http://dx.doi.org/10.1111/fcp.12498] [PMID: 31283051]
[18]
Samarghandian, S.; Farkhondeh, T.; Azimi-Nezhad, M. Protective effects of chrysin against drugs and toxic agents. Dose Response, 2017, 15(2), 1559325817711782.
[http://dx.doi.org/10.1177/1559325817711782] [PMID: 28694744]
[19]
Farkhondeh, T.; Samarghandian, S.; Pourbagher-Shahri, A.M.; Sedaghat, M. The impact of curcumin and its modified formulations on Alzheimer’s disease. J. Cell. Physiol., 2019, 234(10), 16953-16965.
[20]
Ashrafizadeh, M.; Mohammadinejad, R.; Tavakol, S.; Ahmadi, Z.; Roomiani, S.; Katebi, M. Autophagy, anoikis, ferroptosis, necroptosis, and endoplasmic reticulum stress: Potential applications in melanoma therapy. J. Cell. Physiol., 2019, 234(11), 19471-19479.
[http://dx.doi.org/10.1002/jcp.28740] [PMID: 31032940]
[21]
Delen, E.; Doganlar, O.; Doganlar, Z.B.; Delen, O. Inhibition of the invasion of human glioblastoma U87 cell line by ruxolitinib: A molecular player of miR-17 and miR-20a regulating JAK/STAT pathway. Turk Neurosurg., 2020, 30(2), 182-189.
[http://dx.doi.org/10.5137/1019-5149.JTN.26122-19.1] [PMID: 31452174]
[22]
Kelleher, F.C.; O’Sullivan, H. FOXM1 in sarcoma: Role in cell cycle, pluripotency genes and stem cell pathways. Oncotarget, 2016, 7(27), 42792-42804.
[http://dx.doi.org/10.18632/oncotarget.8669] [PMID: 27074562]
[23]
Qian, C.; Wang, B.; Zou, Y.; Zhang, Y.; Hu, X.; Sun, W.; Xiao, H.; Liu, H.; Shi, L. MicroRNA 145 enhances chemosensitivity of glioblastoma stem cells to demethoxycurcumin. Cancer Manag. Res., 2019, 11, 6829-6840.
[http://dx.doi.org/10.2147/CMAR.S210076] [PMID: 31440081]
[24]
Luo, W.; Yan, D.; Song, Z.; Zhu, X.; Liu, X.; Li, X.; Zhao, S. miR-126-3p sensitizes glioblastoma cells to temozolomide by inactivating Wnt/β-catenin signaling via targeting SOX2. Life Sci., 2019, 226, 98-106.
[http://dx.doi.org/10.1016/j.lfs.2019.04.023] [PMID: 30980849]
[25]
Xu, J.; Su, Z.; Ding, Q.; Shen, L.; Nie, X.; Pan, X.; Yan, A.; Yan, R.; Zhou, Y.; Li, L. Inhibition of proliferation by knockdown of Transmembrane (TMEM) 168 in glioblastoma cells via suppression of Wnt/beta-catenin pathway. Oncol. Res., 2019, 27(7), 819-826.
[26]
Taglieri, L.; Rubinacci, G.; Giuffrida, A.; Carradori, S.; Scarpa, S. The kinesin Eg5 inhibitor K858 induces apoptosis and reverses the malignant invasive phenotype in human glioblastoma cells. Invest. New Drugs, 2018, 36(1), 28-35.
[27]
Welford, S.M.; Giaccia, A.J. Hypoxia and senescence: The impact of oxygenation on tumor suppression. Mol. Cancer Res., 2011, 9(5), 538-544.
[http://dx.doi.org/10.1158/1541-7786.MCR-11-0065] [PMID: 21385881]
[28]
Cimmino, F.; Pezone, L.; Avitabile, M.; Acierno, G.; Andolfo, I.; Capasso, M.; Iolascon, A. Inhibition of hypoxia inducible factors combined with all-trans retinoic acid treatment enhances glial transdifferentiation of neuroblastoma cells. Sci. Rep., 2015, 5, 11158.
[http://dx.doi.org/10.1038/srep11158] [PMID: 26057707]
[29]
Kim, Y.; Nam, H.J.; Lee, J.; Park, D.Y.; Kim, C.; Yu, Y.S.; Kim, D.; Park, S.W.; Bhin, J.; Hwang, D.; Lee, H.; Koh, G.Y.; Baek, S.H. Methylation-dependent regulation of HIF-1α stability restricts retinal and tumour angiogenesis. Nat. Commun., 2016, 7, 10347.
[http://dx.doi.org/10.1038/ncomms10347] [PMID: 26757928]
[30]
Saccà, C.D.; Gorini, F.; Ambrosio, S.; Amente, S.; Faicchia, D.; Matarese, G.; Lania, L.; Majello, B. Inhibition of lysine-specific demethylase LSD1 induces senescence in Glioblastoma cells through a HIF-1α-dependent pathway. Biochim. Biophys. Acta. Gene Regul. Mech., 2019, 1862(5), 535-546.
[http://dx.doi.org/10.1016/j.bbagrm.2019.03.004] [PMID: 30951900]
[31]
Ahmadi, Z.; Ashrafizadeh, M. Melatonin as a potential modulator of Nrf2. Fundam. Clin. Pharmacol., 2020, 34(1), 11-19.
[http://dx.doi.org/10.1111/fcp.12498.]
[32]
Leinonen, H.M.; Kansanen, E.; Pölönen, P.; Heinäniemi, M.; Levonen, A-L. Role of the Keap1-Nrf2 pathway in cancer. Adv. Cancer Res., 2014, 122, 281-320.
[http://dx.doi.org/10.1016/B978-0-12-420117-0.00008-6.]
[33]
Lister, A.; Nedjadi, T.; Kitteringham, N.R.; Campbell, F.; Costello, E.; Lloyd, B.; Copple, I.M.; Williams, S.; Owen, A.; Neoptolemos, J.P.; Goldring, C.E.; Park, B.K. Nrf2 is overexpressed in pancreatic cancer: implications for cell proliferation and therapy. Mol. Cancer, 2011, 10(1), 37.
[http://dx.doi.org/10.1186/1476-4598-10-37] [PMID: 21489257]
[34]
Padmanabhan, B.; Tong, K.I.; Ohta, T.; Nakamura, Y.; Scharlock, M.; Ohtsuji, M.; Kang, M-I.; Kobayashi, A.; Yokoyama, S.; Yamamoto, M. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell, 2006, 21(5), 689-700.
[http://dx.doi.org/10.1016/j.molcel.2006.01.013] [PMID: 16507366]
[35]
Shibata, T.; Ohta, T.; Tong, K.I.; Kokubu, A.; Odogawa, R.; Tsuta, K.; Asamura, H.; Yamamoto, M.; Hirohashi, S. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc. Natl. Acad. Sci. USA, 2008, 105(36), 13568-13573.
[http://dx.doi.org/10.1073/pnas.0806268105] [PMID: 18757741]
[36]
Singh, A.; Misra, V.; Thimmulappa, R.K.; Lee, H.; Ames, S.; Hoque, M.O.; Herman, J.G.; Baylin, S.B.; Sidransky, D.; Gabrielson, E.; Brock, M.V.; Biswal, S. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med., 2006, 3(10), e420.
[http://dx.doi.org/10.1371/journal.pmed.0030420] [PMID: 17020408]
[37]
Solis, L.M.; Behrens, C.; Dong, W.; Suraokar, M.; Ozburn, N.C.; Moran, C.A.; Corvalan, A.H.; Biswal, S.; Swisher, S.G.; Bekele, B.N.; Minna, J.D.; Stewart, D.J.; Wistuba, I.I. Nrf2 and Keap1 abnormalities in non-small cell lung carcinoma and association with clinicopathologic features. Clin. Cancer Res., 2010, 16(14), 3743-3753.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-3352] [PMID: 20534738]
[38]
Yoo, N.J.; Kim, H.R.; Kim, Y.R.; An, C.H.; Lee, S.H. Somatic mutations of the KEAP1 gene in common solid cancers. Histopathology, 2012, 60(6), 943-952.
[http://dx.doi.org/10.1111/j.1365-2559.2012.04178.x] [PMID: 22348534]
[39]
Pölönen, P.; Jawahar Deen, A.; Leinonen, H.M.; Jyrkkänen, H-K.; Kuosmanen, S.; Mononen, M.; Jain, A.; Tuomainen, T.; Pasonen-Seppänen, S.; Hartikainen, J.M.; Mannermaa, A.; Nykter, M.; Tavi, P.; Johansen, T.; Heinäniemi, M.; Levonen, A.L. Nrf2 and SQSTM1/p62 jointly contribute to mesenchymal transition and invasion in glioblastoma. Oncogene, 2019, 38(50), 7473-7490.
[http://dx.doi.org/10.1038/s41388-019-0956-6] [PMID: 31444413]
[40]
Song, Y.; Chen, Y.; Li, Y.; Lyu, X.; Cui, J.; Cheng, Y.; Zheng, T.; Zhao, L.; Zhao, G. Resveratrol suppresses epithelial-mesenchymal transition in GBM by regulating SMAD-dependent signaling. BioMed Res. Int., 2019, 2019, 1321973-1321973.
[http://dx.doi.org/10.1155/2019/1321973] [PMID: 31119150]
[41]
Cho, C-F.; Wolfe, J.M.; Fadzen, C.M.; Calligaris, D.; Hornburg, K.; Chiocca, E.A.; Agar, N.Y.R.; Pentelute, B.L.; Lawler, S.E. Blood-brain-barrier spheroids as an in vitro screening platform for brain-penetrating agents. Nat. Commun., 2017, 8, 15623.
[http://dx.doi.org/10.1038/ncomms15623] [PMID: 28585535]
[42]
Banks, W.A. From blood-brain barrier to blood-brain interface: New opportunities for CNS drug delivery. Nat. Rev. Drug Discov., 2016, 15(4), 275-292.
[http://dx.doi.org/10.1038/nrd.2015.21] [PMID: 26794270]
[43]
Chauhan, V.P.; Stylianopoulos, T.; Martin, J.D.; Popović, Z.; Chen, O.; Kamoun, W.S.; Bawendi, M.G.; Fukumura, D.; Jain, R.K. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol., 2012, 7(6), 383-388.
[http://dx.doi.org/10.1038/nnano.2012.45] [PMID: 22484912]
[44]
Senapati, S.; Mahanta, A.K.; Kumar, S.; Maiti, P. Controlled drug delivery vehicles for cancer treatment and their performance. Signal Transduct. Target. Ther., 2018, 3(1), 7.
[http://dx.doi.org/10.1038/s41392-017-0004-3] [PMID: 29560283]
[45]
Moscariello, P.; Ng, D.Y.W.; Jansen, M.; Weil, T.; Luhmann, H.J.; Hedrich, J. Brain delivery of multifunctional dendrimer protein bioconjugates. Adv. Sci. (Weinh.), 2018, 5(5), 1700897.
[http://dx.doi.org/10.1002/advs.201700897] [PMID: 29876217]
[46]
Fan, R.; Chuan, D.; Hou, H.; Chen, H.; Han, B.; Zhang, X.; Zhou, L.; Tong, A.; Xu, J.; Guo, G. Development of a hybrid nanocarrier-recognizing tumor vasculature and penetrating the BBB for glioblastoma multi-targeting therapy. Nanoscale, 2019, 11(23), 11285-11304.
[http://dx.doi.org/10.1039/C9NR01320B] [PMID: 31165845]
[47]
Barati, N.; Momtazi-Borojeni, A.A.; Majeed, M.; Sahebkar, A. Potential therapeutic effects of curcumin in gastric cancer. J. Cell. Physiol., 2019, 234(3), 2317-2328.
[http://dx.doi.org/10.1002/jcp.27229] [PMID: 30191991]
[48]
Lee, J.E.; Yoon, S.S.; Moon, E.Y. Curcumin-induced autophagy augments its antitumor effect against A172 human glioblastoma cells. Biomol. Ther. (Seoul), 2019, 27(5), 484-491.
[http://dx.doi.org/10.4062/biomolther.2019.107] [PMID: 31405268]
[49]
Park, K.S.; Yoon, S.Y.; Park, S.H.; Hwang, J.H. Anti-migration and anti-invasion effects of curcumin via suppression of fascin expression in glioblastoma cells. Brain Tumor Res. Treat., 2019, 7(1), 16-24.
[http://dx.doi.org/10.14791/btrt.2019.7.e28] [PMID: 31062527]
[50]
Huang, B.R.; Tsai, C.H.; Chen, C.C.; Way, T.D.; Kao, J.Y.; Liu, Y.S.; Lin, H.Y.; Lai, S.W.; Lu, D.Y. Curcumin promotes connexin 43 degradation and temozolomide-induced apoptosis in glioblastoma cells. Am. J. Chin. Med., 2019, 47(3), 657-674.
[http://dx.doi.org/10.1142/S0192415X19500344] [PMID: 30974966]
[51]
Ashrafizadeh, M.; Ahmadi, Z.; Farkhondeh, T.; Samarghandian, S. Autophagy as a molecular target of quercetin underlying its protective effects in human diseases. Arch. Physiol. Biochem., 2019, 1-9.
[http://dx.doi.org/10.1080/13813455.2019.1671458] [PMID: 31564166]
[52]
Liu, Y.; Tang, Z.G.; Yang, J.Q.; Zhou, Y.; Meng, L.H.; Wang, H.; Li, C.L. Low concentration of quercetin antagonizes the invasion and angiogenesis of human glioblastoma U251 cells. OncoTargets Ther., 2017, 10, 4023-4028.
[http://dx.doi.org/10.2147/OTT.S136821] [PMID: 28860810]
[53]
Dyck, G.J.B.; Raj, P.; Zieroth, S.; Dyck, J.R.B.; Ezekowitz, J.A. The effects of resveratrol in patients with cardiovascular disease and heart failure: A narrative review. Int. J. Mol. Sci., 2019, 20(4), 904.
[http://dx.doi.org/10.3390/ijms20040904] [PMID: 30791450]
[54]
Huang, X.; Li, X.; Xie, M.; Huang, Z.; Huang, Y.; Wu, G.; Peng, Z.; Sun, Y.; Ming, Q.; Liu, Y. Resveratrol: Review on its discovery, pharmacokinetics and anti-leukemia effects. Chem. Biol. Interact., 2019, 306, 29-38.
[http://dx.doi.org/10.1016/j.cbi.2019.04.001] [PMID: 30954463]
[55]
Hou, C-Y.; Tain, Y-L.; Yu, H-R.; Huang, L-T. The effects of resveratrol in the treatment of metabolic syndrome. Int. J. Mol. Sci., 2019, 20(3), 535.
[http://dx.doi.org/10.3390/ijms20030535] [PMID: 30695995]
[56]
Baur, J.A.; Sinclair, D.A. Therapeutic potential of resveratrol: The in vivo evidence. Nat. Rev. Drug Discov., 2006, 5(6), 493-506.
[http://dx.doi.org/10.1038/nrd2060] [PMID: 16732220]
[57]
Singh, A.P.; Singh, R.; Verma, S.S.; Rai, V.; Kaschula, C.H.; Maiti, P.; Gupta, S.C. Health benefits of resveratrol: Evidence from clinical studies. Med. Res. Rev., 2019, 39(5), 1851-1891.
[http://dx.doi.org/10.1002/med.21565] [PMID: 30741437]
[58]
Dolinsky, V.W.; Dyck, J.R. Calorie restriction and resveratrol in cardiovascular health and disease. Biochim. Biophys. Acta, 2011, 1812(11), 1477-1489.
[http://dx.doi.org/10.1016/j.bbadis.2011.06.010] [PMID: 21749920]
[59]
Block, G.; Jensen, C.D.; Norkus, E.P.; Dalvi, T.B.; Wong, L.G.; McManus, J.F.; Hudes, M.L. Usage patterns, health, and nutritional status of long-term multiple dietary supplement users: A cross-sectional study. Nutr. J., 2007, 6(1), 30.
[http://dx.doi.org/10.1186/1475-2891-6-30] [PMID: 17958896]
[60]
Kroon, P.A.; Iyer, A.; Chunduri, P.; Chan, V.; Brown, L.P.; Iyer, A.; Chunduri, P.; Chan, V.; Brown, L. The cardiovascular nutrapharmacology of resveratrol: Pharmacokinetics, molecular mechanisms and therapeutic potential. Curr. Med. Chem., 2010, 17(23), 2442-2455.
[http://dx.doi.org/10.2174/092986710791556032] [PMID: 20491649]
[61]
Boocock, D.J.; Faust, G.E.; Patel, K.R.; Schinas, A.M.; Brown, V.A.; Ducharme, M.P.; Booth, T.D.; Crowell, J.A.; Perloff, M.; Gescher, A.J.; Steward, W.P.; Brenner, D.E. Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiol. Biomarkers Prev., 2007, 16(6), 1246-1252.
[http://dx.doi.org/10.1158/1055-9965.EPI-07-0022] [PMID: 17548692]
[62]
Zordoky, B.N.; Robertson, I.M.; Dyck, J.R. Preclinical and clinical evidence for the role of resveratrol in the treatment of cardiovascular diseases. Biochim. Biophys. Acta, 2015, 1852(6), 1155-1177.
[http://dx.doi.org/10.1016/j.bbadis.2014.10.016] [PMID: 25451966]
[63]
Song, Y.; Chen, Y.; Li, Y.; Lyu, X.; Cui, J.; Cheng, Y.; Zheng, T.; Zhao, L.; Zhao, G. Resveratrol suppresses epithelial-mesenchymal transition in GBM by regulating SMAD-dependent signaling. Biomed Res. Int., 2019, 2019 Article ID, 1321973.
[http://dx.doi.org/10.1155/2019/1321973]
[64]
Reitz, C.; Brayne, C.; Mayeux, R. Epidemiology of Alzheimer disease. Nat. Rev. Neurol., 2011, 7(3), 137-152.
[http://dx.doi.org/10.1038/nrneurol.2011.2] [PMID: 21304480]
[65]
Hardy, J.; Selkoe, D.J. The amyloid hypothesis of Alzheimer’s disease: Progress and problems on the road to therapeutics. Science, 2002, 297(5580), 353-356.
[66]
Holtzman, D.M.; Mandelkow, E.; Selkoe, D.J. Alzheimer disease in 2020. Cold Spring Harb. Perspect. Med., 2012, 2(11), a011585.
[http://dx.doi.org/10.1101/cshperspect.a011585] [PMID: 23125202]
[67]
Corpas, R.; Griñán-Ferré, C.; Rodríguez-Farré, E.; Pallàs, M.; Sanfeliu, C. Resveratrol induces brain resilience against Alzheimer neurodegeneration through proteostasis enhancement. Mol. Neurobiol., 2019, 56(2), 1502-1516.
[http://dx.doi.org/10.1007/s12035-018-1157-y] [PMID: 29948950]
[68]
Badger, J.L.; Cordero-Llana, O.; Hartfield, E.M.; Wade-Martins, R. Parkinson’s disease in a dish - Using stem cells as a molecular tool. Neuropharmacology, 2014, 76(Pt A), 88-96..
[http://dx.doi.org/10.1016/j.neuropharm.2013.08.035] [PMID: 24035919]
[69]
Tysnes, O-B.; Storstein, A. Epidemiology of Parkinson’s disease. J. Neural Transm. (Vienna), 2017, 124(8), 901-905.
[http://dx.doi.org/10.1007/s00702-017-1686-y] [PMID: 28150045]
[70]
Lee, V.M-Y.; Trojanowski, J.Q. Mechanisms of Parkinson’s disease linked to pathological α-synuclein: New targets for drug discovery. Neuron, 2006, 52(1), 33-38.
[http://dx.doi.org/10.1016/j.neuron.2006.09.026] [PMID: 17015225]
[71]
Grünblatt, E.; Mandel, S.; Youdim, M.B. MPTP and 6-hydroxydopamine-induced neurodegeneration as models for Parkinson’s disease: Neuroprotective strategies. J. Neurol., 2000, 247(2)(Suppl. 2), II95-II102.
[PMID: 10991672]
[72]
Liu, Q.; Zhu, D.; Jiang, P.; Tang, X.; Lang, Q.; Yu, Q.; Zhang, S.; Che, Y.; Feng, X. Resveratrol synergizes with low doses of L-DOPA to improve MPTP-induced Parkinson disease in mice. Behav. Brain Res., 2019, 367, 10-18.
[http://dx.doi.org/10.1016/j.bbr.2019.03.043] [PMID: 30922940]
[73]
Mukherjee, S.; Baidoo, J.N.E.; Sampat, S.; Mancuso, A.; David, L.; Cohen, L.S.; Zhou, S.; Banerjee, P. Liposomal TriCurin, a synergistic combination of curcumin, epicatechin gallate and resveratrol, repolarizes tumor-associated microglia/macrophages, and eliminates Glioblastoma (GBM) and GBM stem cells. Molecules, 2018, 23(1), E201.
[http://dx.doi.org/10.3390/molecules23010201] [PMID: 29346317]
[74]
Sayd, S.; Thirant, C.; El-Habr, E.A.; Lipecka, J.; Dubois, L.G.; Bogeas, A.; Tahiri-Jouti, N.; Chneiweiss, H.; Junier, M-P. Sirtuin-2 activity is required for glioma stem cell proliferation arrest but not necrosis induced by resveratrol. Stem Cell Rev. Rep., 2014, 10(1), 103-113.
[http://dx.doi.org/10.1007/s12015-013-9465-0] [PMID: 23955573]
[75]
Empl, M.T.; Macke, S.; Winterhalter, P.; Puff, C.; Lapp, S.; Stoica, G.; Baumgärtner, W.; Steinberg, P. The growth of the canine glioblastoma cell line D-GBM and the canine histiocytic sarcoma cell line DH82 is inhibited by the resveratrol oligomers hopeaphenol and r2-viniferin. Vet. Comp. Oncol., 2014, 12(2), 149-159.
[http://dx.doi.org/10.1111/j.1476-5829.2012.00349.x] [PMID: 22882564]
[76]
Gagliano, N.; Moscheni, C.; Torri, C.; Magnani, I.; Bertelli, A.A.; Gioia, M. Effect of resveratrol on Matrix Metalloproteinase-2 (MMP-2) and Secreted Protein Acidic and Rich in Cysteine (SPARC) on human cultured glioblastoma cells. Biomed. Pharmacother., 2005, 59(7), 359-364.
[http://dx.doi.org/10.1016/j.biopha.2005.06.001] [PMID: 16084059]
[77]
Zhang, W.; Murao, K.; Zhang, X.; Matsumoto, K.; Diah, S.; Okada, M.; Miyake, K.; Kawai, N.; Fei, Z.; Tamiya, T. Resveratrol represses YKL-40 expression in human glioma U87 cells. BMC Cancer, 2010, 10(1), 593.
[http://dx.doi.org/10.1186/1471-2407-10-593] [PMID: 21029458]
[78]
Gavrilas, L.I.; Cruceriu, D.; Ionescu, C.; Miere, D.; Balacescu, O. Pro-apoptotic genes as new targets for single and combinatorial treatments with resveratrol and curcumin in colorectal cancer. Food Funct., 2019, 10(6), 3717-3726.
[http://dx.doi.org/10.1039/C9FO01014A] [PMID: 31169275]
[79]
Almeida, T.C.; Guerra, C.C.C.; De Assis, B.L.G.; de Oliveira Aguiar Soares, R.D.; Garcia, C.C.M.; Lima, A.A.; da Silva, G.N. Antiproliferative and toxicogenomic effects of resveratrol in bladder cancer cells with different TP53 status. Environ. Mol. Mutagen., 2019, 60(8), 740-751.
[http://dx.doi.org/10.1002/em.22297] [PMID: 31095781]
[80]
Mineda, A.; Nishimura, M.; Kagawa, T.; Takiguchi, E.; Kawakita, T.; Abe, A.; Irahara, M. Resveratrol suppresses proliferation and induces apoptosis of uterine sarcoma cells by inhibiting the Wnt signaling pathway. Exp. Ther. Med., 2019, 17(3), 2242-2246.
[http://dx.doi.org/10.3892/etm.2019.7209] [PMID: 30867708]
[81]
Önay Uçar, E.; Şengelen, A. Resveratrol and siRNA in combination reduces Hsp27 expression and induces caspase-3 activity in human glioblastoma cells. Cell Stress Chaperones, 2019, 24(4), 763-775.
[http://dx.doi.org/10.1007/s12192-019-01004-z] [PMID: 31073903]
[82]
Farooqi, A.A.; Khalid, S.; Ahmad, A. Regulation of cell signaling pathways and miRNAs by resveratrol in different cancers. Int. J. Mol. Sci., 2018, 19(3), E652.
[http://dx.doi.org/10.3390/ijms19030652] [PMID: 29495357]
[83]
Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest., 2010, 120(5), 1786-1786.
[http://dx.doi.org/10.1172/JCI39104C1] [PMID: 19487818]
[84]
Iwadate, Y. Epithelial-mesenchymal transition in glioblastoma progression. Oncol. Lett., 2016, 11(3), 1615-1620.
[http://dx.doi.org/10.3892/ol.2016.4113] [PMID: 26998052]
[85]
Iwatsuki, M.; Mimori, K.; Yokobori, T.; Ishi, H.; Beppu, T.; Nakamori, S.; Baba, H.; Mori, M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci., 2010, 101(2), 293-299.
[http://dx.doi.org/10.1111/j.1349-7006.2009.01419.x] [PMID: 19961486]
[86]
Gomes, L.R.; Terra, L.F.; Sogayar, M.C.; Labriola, L. Epithelial-mesenchymal transition: Implications in cancer progression and metastasis. Curr. Pharm. Biotechnol., 2011, 12(11), 1881-1890.
[http://dx.doi.org/10.2174/138920111798377102] [PMID: 21470131]
[87]
Iser, I.C.; Pereira, M.B.; Lenz, G.; Wink, M.R. The epithelial-to-mesenchymal transition-like process in glioblastoma: An updated systematic review and in silico investigation. Med. Res. Rev., 2017, 37(2), 271-313.
[http://dx.doi.org/10.1002/med.21408] [PMID: 27617697]
[88]
Thiery, J.P.; Acloque, H.; Huang, R.Y.; Nieto, M.A. Epithelial-mesenchymal transitions in development and disease. Cell, 2009, 139(5), 871-890.
[89]
Polyak, K.; Weinberg, R.A. Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat. Rev. Cancer, 2009, 9(4), 265-273.
[http://dx.doi.org/10.1038/nrc2620] [PMID: 19262571]
[90]
Thiery, J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer, 2002, 2(6), 442-454.
[http://dx.doi.org/10.1038/nrc822] [PMID: 12189386]
[91]
Saika, S.; Kono-Saika, S.; Tanaka, T.; Yamanaka, O.; Ohnishi, Y.; Sato, M.; Muragaki, Y.; Ooshima, A.; Yoo, J.; Flanders, K.C.; Roberts, A.B. Smad3 is required for dedifferentiation of retinal pigment epithelium following retinal detachment in mice. Lab. Invest., 2004, 84(10), 1245-1258.
[http://dx.doi.org/10.1038/labinvest.3700156] [PMID: 15273699]
[92]
Derynck, R.; Zhang, Y.E. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature, 2003, 425(6958), 577-584.
[http://dx.doi.org/10.1038/nature02006] [PMID: 14534577]
[93]
Blobe, G.C.; Schiemann, W.P.; Lodish, H.F. Role of transforming growth factor β in human disease. N. Engl. J. Med., 2000, 342(18), 1350-1358.
[http://dx.doi.org/10.1056/NEJM200005043421807] [PMID: 10793168]
[94]
Lv, S.; Zhang, J.; He, Y.; Liu, Q.; Wang, Z.; Liu, B.; Shi, L.; Wu, Y. MicroRNA-520e targets AEG-1 to suppress the proliferation and invasion of colorectal cancer cells through Wnt/GSK-3beta/beta-catenin signaling. Clin. Exp. Pharmacol. Physiol., 2020, 47(1), 158-167.
[PMID: 31574178]
[95]
Xue, D.; Yang, P.; Wei, Q.; Li, X.; Lin, L.; Lin, T. IL 21/IL 21R inhibit tumor growth and invasion in non small cell lung cancer cells via suppressing Wnt/β catenin signaling and PD L1 expression. Int. J. Mol. Med., 2019, 44(5), 1697-1706.
[http://dx.doi.org/10.3892/ijmm.2019.4354] [PMID: 31573051]
[96]
Lei, C.; Yao, Y.; Shen, B.; Liu, J.; Pan, Q.; Liu, N.; Li, L.; Huang, J.; Long, Z.; Shao, L. Columbamine suppresses the proliferation and malignization of colon cancer cells via abolishing Wnt/β-catenin signaling pathway. Cancer Manag. Res., 2019, 11, 8635-8645.
[http://dx.doi.org/10.2147/CMAR.S209861] [PMID: 31572013]
[97]
Ghasemi, F.; Shafiee, M.; Banikazemi, Z.; Pourhanifeh, M.H.; Khanbabaei, H.; Shamshirian, A.; Amiri Moghadam, S. ArefNezhad, R.; Sahebkar, A.; Avan, A.; Mirzaei, H. Curcumin inhibits NF-kB and Wnt/β-catenin pathways in cervical cancer cells. Pathol. Res. Pract., 2019, 215(10), 152556.
[http://dx.doi.org/10.1016/j.prp.2019.152556] [PMID: 31358480]
[98]
Vallee, A.; Lecarpentier, Y.; Vallee, J.N. Curcumin: A therapeutic strategy in cancers by inhibiting the canonical WNT/beta-catenin pathway. J. Exp. Clin. Cancer Res., 2019, 38(1), 323.
[http://dx.doi.org/10.1186/s13046-019-1320-y.]
[99]
Srivastava, N.S.; Srivastava, R.A.K. Curcumin and quercetin synergistically inhibit cancer cell proliferation in multiple cancer cells and modulate Wnt/beta-catenin signaling and apoptotic pathways in A375 cells. Phytomedicine, 2019, 52, 117-128.
[100]
Götze, S.; Wolter, M.; Reifenberger, G.; Müller, O.; Sievers, S. Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas. Int. J. Cancer, 2010, 126(11), 2584-2593.
[PMID: 19847810]
[101]
Kim, K.H.; Seol, H.J.; Kim, E.H.; Rheey, J.; Jin, H.J.; Lee, Y.; Joo, K.M.; Lee, J.; Nam, D-H. Wnt/β-catenin signaling is a key downstream mediator of MET signaling in glioblastoma stem cells. Neuro-oncol., 2013, 15(2), 161-171.
[http://dx.doi.org/10.1093/neuonc/nos299] [PMID: 23258844]
[102]
Liu, C.; Tu, Y.; Sun, X.; Jiang, J.; Jin, X.; Bo, X.; Li, Z.; Bian, A.; Wang, X.; Liu, D.; Wang, Z.; Ding, L. Wnt/beta-Catenin pathway in human glioma: Expression pattern and clinical/prognostic correlations. Clin. Exp. Med., 2011, 11(2), 105-112.
[http://dx.doi.org/10.1007/s10238-010-0110-9] [PMID: 20809334]
[103]
Paul, I.; Bhattacharya, S.; Chatterjee, A.; Ghosh, M.K. Current understanding on EGFR and Wnt/β-catenin signaling in glioma and their possible crosstalk. Genes Cancer, 2013, 4(11-12), 427-446.
[http://dx.doi.org/10.1177/1947601913503341] [PMID: 24386505]
[104]
Sandberg, C.J.; Altschuler, G.; Jeong, J.; Strømme, K.K.; Stangeland, B.; Murrell, W.; Grasmo-Wendler, U-H.; Myklebost, O.; Helseth, E.; Vik-Mo, E.O.; Hide, W.; Langmoen, I.A. Comparison of glioma stem cells to neural stem cells from the adult human brain identifies dysregulated Wnt-signaling and a fingerprint associated with clinical outcome. Exp. Cell Res., 2013, 319(14), 2230-2243.
[http://dx.doi.org/10.1016/j.yexcr.2013.06.004] [PMID: 23791939]
[105]
Cilibrasi, C.; Riva, G.; Romano, G.; Cadamuro, M.; Bazzoni, R.; Butta, V.; Paoletta, L.; Dalprà, L.; Strazzabosco, M.; Lavitrano, M.; Giovannoni, R.; Bentivegna, A. Resveratrol impairs glioma stem cells proliferation and motility by modulating the wnt signaling pathway. PLoS One, 2017, 12(1), e0169854.
[http://dx.doi.org/10.1371/journal.pone.0169854] [PMID: 28081224]
[106]
Rodriguez-Ruiz, M.E.; Buqué, A.; Hensler, M.; Chen, J.; Bloy, N.; Petroni, G.; Sato, A.; Yamazaki, T.; Fucikova, J.; Galluzzi, L. Apoptotic caspases inhibit abscopal responses to radiation and identify a new prognostic biomarker for breast cancer patients. OncoImmunology, 2019, 8(11), e1655964.
[http://dx.doi.org/10.1080/2162402X.2019.1655964] [PMID: 31646105]
[107]
Buqué, A.; Rodriguez-Ruiz, M.E.; Fucikova, J.; Galluzzi, L. Apoptotic caspases cut down the immunogenicity of radiation. OncoImmunology, 2019, 8(11), e1655364.
[http://dx.doi.org/10.1080/2162402X.2019.1655364] [PMID: 31646103]
[108]
Wu, L.Y.; Chen, C.W.; Chen, L.K.; Chou, H.Y.; Chang, C.L.; Juan, C.C. Curcumin attenuates adipogenesis by inducing preadipocyte apoptosis and inhibiting adipocyte differentiation. Nutrients, 2019, 11(10), E2307.
[http://dx.doi.org/10.3390/nu11102307] [PMID: 31569380]
[109]
Qin, Q.P.; Wang, Z.F.; Huang, X.L.; Tan, M.X.; Luo, Z.H.; Wang, S.L.; Zou, B.Q.; Liang, H. Two telomerase-targeting Pt(ii) com- plexes of jatrorrhizine and berberine derivatives induce apoptosis in human bladder tumor cells. Dalton Trans., 2019, 48(40), 15247-15254.
[http://dx.doi.org/10.1039/c9dt02381j.]
[110]
Huang, K.; Liu, X.; Li, Y.; Wang, Q.; Zhou, J.; Wang, Y.; Dong, F.; Yang, C.; Sun, Z.; Fang, C.; Liu, C.; Tan, Y.; Wu, X.; Jiang, T.; Kang, C. Genome-wide CRISPR-Cas9 screening identifies NF-kappaB/E2F6 responsible for EGFRvIII-associated temozolomide resistance in glioblastoma. Adv. Sci. (Weinh.), 2019, 6(17), 1900782.
[http://dx.doi.org/10.1002/advs.201900782.]
[111]
Du, F.; Zhao, T.; Ji, H.C.; Luo, Y.B.; Wang, F.; Mao, G.H.; Feng, W.W.; Chen, Y.; Wu, X.Y.; Yang, L.Q. Dioxin-like (DL-) polychlorinated biphenyls induced immunotoxicity through apoptosis in mice splenocytes via the AhR mediated mitochondria dependent signaling pathways. Food Chem. Toxicol., 2019, 134, 110803.
[http://dx.doi.org/10.1016/j.fct.2019.110803.]
[112]
Arya, J.S.; Joseph, M.M.; Sherin, D.R.; Nair, J.B.; Manojkumar, T.K.; Maiti, K.K. Exploring mitochondria-mediated intrinsic apoptosis by new phytochemical entities: An explicit observation of cytochrome c dynamics on lung and melanoma cancer cells. J. Med. Chem., 2019, 62(17), 8311-8329.
[http://dx.doi.org/10.1021/acs.jmedchem.9b01098] [PMID: 31393121]
[113]
Liu, Y.; Shao, E.; Zhang, Z.; Yang, D.; Li, G.; Cao, H.; Huang, H. A novel indolizine derivative induces apoptosis through the mitochondria p53 pathway in HepG2 cells. Front. Pharmacol., 2019, 10, 762.
[http://dx.doi.org/10.3389/fphar.2019.00762] [PMID: 31354481]
[114]
Zielińska-Przyjemska, M.; Kaczmarek, M.; Krajka-Kuźniak, V.; Łuczak, M.; Baer-Dubowska, W. The effect of resveratrol, its naturally occurring derivatives and tannic acid on the induction of cell cycle arrest and apoptosis in rat C6 and human T98G glioma cell lines. Toxicol. In Vitro, 2017, 43, 69-75.
[http://dx.doi.org/10.1016/j.tiv.2017.06.004] [PMID: 28595835]
[115]
Aggarwal, B.B.; Bhardwaj, A.; Aggarwal, R.S.; Seeram, N.P.; Shishodia, S.; Takada, Y. Role of resveratrol in prevention and therapy of cancer: Preclinical and clinical studies. Anticancer Res., 2004, 24(5A), 2783-2840.
[PMID: 15517885]
[116]
Athar, M.; Back, J.H.; Kopelovich, L.; Bickers, D.R.; Kim, A.L. Multiple molecular targets of resveratrol: Anti-carcinogenic mechanisms. Arch. Biochem. Biophys., 2009, 486(2), 95-102.
[http://dx.doi.org/10.1016/j.abb.2009.01.018] [PMID: 19514131]
[117]
Eyler, C.E.; Foo, W.C.; LaFiura, K.M.; McLendon, R.E.; Hjelmeland, A.B.; Rich, J.N. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells, 2008, 26(12), 3027-3036.
[http://dx.doi.org/10.1634/stemcells.2007-1073] [PMID: 18802038]
[118]
Gallia, G.L.; Tyler, B.M.; Hann, C.L.; Siu, I-M.; Giranda, V.L.; Vescovi, A.L.; Brem, H.; Riggins, G.J. Inhibition of Akt inhibits growth of glioblastoma and glioblastoma stem-like cells. Mol. Cancer Ther., 2009, 8(2), 386-393.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-0680] [PMID: 19208828]
[119]
Clark, P.A.; Bhattacharya, S.; Elmayan, A.; Darjatmoko, S.R.; Thuro, B.A.; Yan, M.B.; van Ginkel, P.R.; Polans, A.S.; Kuo, J.S. Resveratrol targeting of AKT and p53 in glioblastoma and glioblastoma stem-like cells to suppress growth and infiltration. J. Neurosurg., 2017, 126(5), 1448-1460.
[http://dx.doi.org/10.3171/2016.1.JNS152077] [PMID: 27419830]
[120]
Ashrafizadeh, M.; Ahmadi, Z.; Kotla, N.G.; Afshar, E.G.; Samarghandian, S.; Mandegary, A.; Pardakhty, A.; Mohammadinejad, R.; Sethi, G. Nanoparticles targeting STATs in cancer therapy. Cells, 2019, 8(10), 1158.
[http://dx.doi.org/10.3390/cells8101158] [PMID: 31569687]
[121]
Dong, Z.; Chen, Y.; Yang, C.; Zhang, M.; Chen, A.; Yang, J.; Huang, Y. STAT gene family mRNA expression and prognostic value in hepatocellular carcinoma. OncoTargets Ther., 2019, 12, 7175-7191.
[http://dx.doi.org/10.2147/OTT.S202122] [PMID: 31564902]
[122]
Wang, X.; Liao, X.; Yu, T.; Gong, Y.; Zhang, L.; Huang, J.; Yang, C.; Han, C.; Yu, L.; Zhu, G.; Qin, W.; Liu, Z.; Zhou, X.; Liu, J.; Han, Q.; Peng, T. Analysis of clinical significance and prospective molecular mechanism of main elements of the JAK/STAT pathway in hepatocellular carcinoma. Int. J. Oncol., 2019, 55(4), 805-822.
[http://dx.doi.org/10.3892/ijo.2019.4862] [PMID: 31485610]
[123]
Xue, S.; Xiao-Hong, S.; Lin, S.; Jie, B.; Li-Li, W.; Jia-Yao, G.; Shun, S.; Pei-Nan, L.; Mo-Li, W.; Qian, W.; Xiao-Yan, C.; Qing-You, K.; Peng, Z.; Hong, L.; Jia, L. Lumbar puncture-administered resveratrol inhibits STAT3 activation, enhancing autophagy and apoptosis in orthotopic rat glioblastomas. Oncotarget, 2016, 7(46), 75790-75799.
[http://dx.doi.org/10.18632/oncotarget.12414] [PMID: 27716625]
[124]
Song, X.; Shu, X.H.; Wu, M.L.; Zheng, X.; Jia, B.; Kong, Q.Y.; Liu, J.; Li, H. Postoperative resveratrol administration improves prognosis of rat orthotopic glioblastomas. BMC Cancer, 2018, 18(1), 871.
[http://dx.doi.org/10.1186/s12885-018-4771-1] [PMID: 30176837]
[125]
Uzzaman, M.; Keller, G.; Germano, I.M. Enhanced proapoptotic effects of tumor necrosis factor-related apoptosis-inducing ligand on temozolomide-resistant glioma cells. J. Neurosurg., 2007, 106(4), 646-651.
[http://dx.doi.org/10.3171/jns.2007.106.4.646] [PMID: 17432717]
[126]
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]
[127]
Yuan, Y.; Xue, X.; Guo, R.B.; Sun, X.L.; Hu, G. Resveratrol enhances the antitumor effects of temozolomide in glioblastoma via ROS-dependent AMPK-TSC-mTOR signaling pathway. CNS Neurosci. Ther., 2012, 18(7), 536-546.
[http://dx.doi.org/10.1111/j.1755-5949.2012.00319.x] [PMID: 22530672]
[128]
Li, H.; Liu, Y.; Jiao, Y.; Guo, A.; Xu, X.; Qu, X.; Wang, S.; Zhao, J.; Li, Y.; Cao, Y. Resveratrol sensitizes glioblastoma-initiating cells to temozolomide by inducing cell apoptosis and promoting differentiation. Oncol. Rep., 2016, 35(1), 343-351.
[http://dx.doi.org/10.3892/or.2015.4346] [PMID: 26498391]
[129]
Gilbert, M.R.; Friedman, H.S.; Kuttesch, J.F.; Prados, M.D.; Olson, J.J.; Reaman, G.H.; Zaknoen, S.L. A phase II study of temozolomide in patients with newly diagnosed supratentorial malignant glioma before radiation therapy. Neuro-oncol., 2002, 4(4), 261-267.
[http://dx.doi.org/10.1093/neuonc/4.4.261] [PMID: 12356356]
[130]
Yoshino, A.; Ogino, A.; Yachi, K.; Ohta, T.; Fukushima, T.; Watanabe, T.; Katayama, Y.; Okamoto, Y.; Naruse, N.; Sano, E.; Tsumoto, K. Gene expression profiling predicts response to temozolomide in malignant gliomas. Int. J. Oncol., 2010, 36(6), 1367-1377.
[http://dx.doi.org/10.3892/ijo_00000621] [PMID: 20428759]
[131]
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]
[132]
Lavon, I.; Fuchs, D.; Zrihan, D.; Efroni, G.; Zelikovitch, B.; Fellig, Y.; Siegal, T. Novel mechanism whereby nuclear factor kappaB mediates DNA damage repair through regulation of O(6)-methylguanine-DNA-methyltransferase. Cancer Res., 2007, 67(18), 8952-8959.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3820] [PMID: 17875738]
[133]
Huang, H.; Lin, H.; Zhang, X.; Li, J. Resveratrol reverses temozolomide resistance by downregulation of MGMT in T98G glioblastoma cells by the NF-κB-dependent pathway. Oncol. Rep., 2012, 27(6), 2050-2056.
[PMID: 22426504]
[134]
Wei, F.; Shi, L.; Wang, Q.; Zhao, Y. Fast and accurate separation of the paclitaxel from yew extracum by a pseudo simulated moving bed with solvent gradient. J. Chromatogr. A, 2018, 1564, 120-127.
[http://dx.doi.org/10.1016/j.chroma.2018.06.009] [PMID: 29895410]
[135]
Ganipineni, L.P.; Ucakar, B.; Joudiou, N.; Bianco, J.; Danhier, P.; Zhao, M.; Bastiancich, C.; Gallez, B.; Danhier, F.; Préat, V. Magnetic targeting of paclitaxel-loaded poly(lactic-co-glycolic acid)-based nanoparticles for the treatment of glioblastoma. Int. J. Nanomedicine, 2018, 13, 4509-4521.
[http://dx.doi.org/10.2147/IJN.S165184] [PMID: 30127603]
[136]
Xu, J.; Su, C.; Zhao, F.; Tao, J.; Hu, D.; Shi, A.; Pan, J.; Zhang, Y. Paclitaxel promotes lung cancer cell apoptosis via MEG3-P53 pathway activation. Biochem. Biophys. Res. Commun., 2018, 504(1), 123-128.
[http://dx.doi.org/10.1016/j.bbrc.2018.08.142] [PMID: 30173893]
[137]
Ho, C-M.; Lee, F-K.; Huang, S-H.; Cheng, W-F. Everolimus following 5-aza-2-deoxycytidine is a promising therapy in paclitaxel-resistant clear cell carcinoma of the ovary. Am. J. Cancer Res., 2018, 8(1), 56-69.
[PMID: 29416920]
[138]
Zhang, Y.; Wang, Y.; Xue, J. Paclitaxel inhibits breast cancer metastasis via suppression of Aurora kinase-mediated cofilin-1 activity. Exp. Ther. Med., 2018, 15(2), 1269-1276.
[PMID: 29434713]
[139]
Öztürk, Y.; Günaydın, C.; Yalçın, F.; Nazıroğlu, M.; Braidy, N. Resveratrol enhances apoptotic and oxidant effects of paclitaxel through TRPM2 channel activation in DBTRG glioblastoma cells. Oxid. Med. Cell. Longev., 2019, 2019, 4619865-4619865.
[http://dx.doi.org/10.1155/2019/4619865] [PMID: 30984336]
[140]
Ahmadi, Z.; Mohammadinejad, R.; Ashrafizadeh, M. Drug delivery systems for resveratrol, a non-flavonoid polyphenol: Emerging evidence in last decades. J. Drug Deliv. Sci. Technol., 2019, 51, 591-604.
[http://dx.doi.org/10.1016/j.jddst.2019.03.017]
[141]
Singh, M. Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Des., 1999, 5(6), 443-451.
[PMID: 10390608]
[142]
Daniels, T.R.; Delgado, T.; Rodriguez, J.A.; Helguera, G.; Penichet, M.L. The transferrin receptor part I: Biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin. Immunol., 2006, 121(2), 144-158.
[http://dx.doi.org/10.1016/j.clim.2006.06.010] [PMID: 16904380]
[143]
Calzolari, A.; Larocca, L.M.; Deaglio, S.; Finisguerra, V.; Boe, A.; Raggi, C.; Ricci-Vitani, L.; Pierconti, F.; Malavasi, F.; De Maria, R.; Testa, U.; Pallini, R. Transferrin receptor 2 is frequently and highly expressed in glioblastomas. Transl. Oncol., 2010, 3(2), 123-134.
[http://dx.doi.org/10.1593/tlo.09274] [PMID: 20360937]
[144]
Jhaveri, A.; Deshpande, P.; Pattni, B.; Torchilin, V. Transferrin-targeted, resveratrol-loaded liposomes for the treatment of glioblastoma. J. Control. Release, 2018, 277, 89-101.
[http://dx.doi.org/10.1016/j.jconrel.2018.03.006] [PMID: 29522834]
[145]
Jhaveri, A.; Luther, E.; Torchilin, V. The effect of transferrin-targeted, resveratrol-loaded liposomes on neurosphere cultures of glioblastoma: Implications for targeting tumour-initiating cells. J. Drug Target., 2019, 27(5-6), 601-613.
[http://dx.doi.org/10.1080/1061186X.2018.1550647] [PMID: 30475084]
[146]
Hatters, D.M.; Peters-Libeu, C.A.; Weisgraber, K.H. Apolipoprotein E structure: Insights into function. Trends Biochem. Sci., 2006, 31(8), 445-454.
[http://dx.doi.org/10.1016/j.tibs.2006.06.008] [PMID: 16820298]
[147]
Phillips, M.C. Apolipoprotein E isoforms and lipoprotein metabolism. IUBMB Life, 2014, 66(9), 616-623.
[http://dx.doi.org/10.1002/iub.1314] [PMID: 25328986]
[148]
Weisgraber, K.H.; Apolipoprotein, E.; Apolipoprotein, E. Structure-function relationships. Adv. Protein Chem., 1994, 45, 249-302.
[149]
Kim, S.H.; Adhikari, B.B.; Cruz, S.; Schramm, M.P.; Vinson, J.A.; Narayanaswami, V. Targeted intracellular delivery of resveratrol to glioblastoma cells using apolipoprotein E-containing reconstituted HDL as a nanovehicle. PLoS One, 2015, 10(8), e0135130-e0135130.
[http://dx.doi.org/10.1371/journal.pone.0135130] [PMID: 26258481]
[150]
Hall, A. Rho GTPases and the actin cytoskeleton. Science, 1998, 279(5350), 509-514.
[http://dx.doi.org/10.1126/science.279.5350.509] [PMID: 9438836]
[151]
Nutt, C.L.; Mani, D.R.; Betensky, R.A.; Tamayo, P.; Cairncross, J.G.; Ladd, C.; Pohl, U.; Hartmann, C.; McLaughlin, M.E.; Batchelor, T.T.; Black, P.M.; von Deimling, A.; Pomeroy, S.L.; Golub, T.R.; Louis, D.N. Gene expression-based classification of malignant gliomas correlates better with survival than histological classification. Cancer Res., 2003, 63(7), 1602-1607.
[PMID: 12670911]
[152]
Forget, M-A.; Desrosiers, R.R.; Del, M.; Moumdjian, R.; Shedid, D.; Berthelet, F.; Béliveau, R. The expression of rho proteins decreases with human brain tumor progression: Potential tumor markers. Clin. Exp. Metastasis, 2002, 19(1), 9-15.
[http://dx.doi.org/10.1023/A:1013884426692] [PMID: 11918088]
[153]
Malchinkhuu, E.; Sato, K.; Maehama, T.; Mogi, C.; Tomura, H.; Ishiuchi, S.; Yoshimoto, Y.; Kurose, H.; Okajima, F. S1P(2) receptors mediate inhibition of glioma cell migration through Rho signaling pathways independent of PTEN. Biochem. Biophys. Res. Commun., 2008, 366(4), 963-968.
[http://dx.doi.org/10.1016/j.bbrc.2007.12.054] [PMID: 18088600]
[154]
Goldberg, L.; Kloog, Y. A Ras inhibitor tilts the balance between Rac and Rho and blocks phosphatidylinositol 3-kinase-dependent glioblastoma cell migration. Cancer Res., 2006, 66(24), 11709-11717.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1878] [PMID: 17178866]
[155]
Xiong, W.; Yin, A.; Mao, X.; Zhang, W.; Huang, H.; Zhang, X. Resveratrol suppresses human glioblastoma cell migration and invasion via activation of RhoA/ROCK signaling pathway. Oncol. Lett., 2016, 11(1), 484-490.
[http://dx.doi.org/10.3892/ol.2015.3888] [PMID: 26870238]
[156]
Khoei, S.; Shoja, M.; Mostaar, A.; Faeghi, F. Effects of resveratrol and methoxyamine on the radiosensitivity of iododeoxyuridine in U87MG glioblastoma cell line. Exp. Biol. Med. (Maywood), 2016, 241(11), 1229-1236.
[http://dx.doi.org/10.1177/1535370215622583] [PMID: 26748400]
[157]
Yang, Y.P.; Chang, Y.L.; Huang, P.I.; Chiou, G.Y.; Tseng, L.M.; Chiou, S.H.; Chen, M.H.; Chen, M.T.; Shih, Y.H.; Chang, C.H.; Hsu, C.C.; Ma, H.I.; Wang, C.T.; Tsai, L.L.; Yu, C.C.; Chang, C.J. Resveratrol suppresses tumorigenicity and enhances radiosensitivity in primary glioblastoma tumor initiating cells by inhibiting the STAT3 axis. J. Cell. Physiol., 2012, 227(3), 976-993.
[http://dx.doi.org/10.1002/jcp.22806] [PMID: 21503893]
[158]
Leone, S.; Fiore, M.; Lauro, M.G.; Pino, S.; Cornetta, T.; Cozzi, R. Resveratrol and X rays affect gap junction intercellular communications in human glioblastoma cells. Mol. Carcinog., 2008, 47(8), 587-598.
[http://dx.doi.org/10.1002/mc.20416]
[159]
Kundu, J.K.; Surh, Y-J. Cancer chemopreventive and therapeutic potential of resveratrol: Mechanistic perspectives. Cancer Lett., 2008, 269(2), 243-261.
[http://dx.doi.org/10.1016/j.canlet.2008.03.057] [PMID: 18550275]
[160]
Stamenkovic, I. In Matrix metalloproteinases in tumor invasion and metastasis. Semin. Cancer Biol., 2000, 10(6), 415-433.
[161]
Vu, T.H.; Werb, Z. Matrix metalloproteinases: Effectors of development and normal physiology. Genes Dev., 2000, 14(17), 2123-2133.
[http://dx.doi.org/10.1101/gad.815400] [PMID: 10970876]
[162]
Tai, K.Y.; Shieh, Y.S.; Lee, C.S.; Shiah, S.G.; Wu, C.W. Axl promotes cell invasion by inducing MMP-9 activity through activation of NF-kappaB and Brg-1. Oncogene, 2008, 27(29), 4044-4055.
[http://dx.doi.org/10.1038/onc.2008.57] [PMID: 18345028]
[163]
Sheth, S.; Jajoo, S.; Kaur, T.; Mukherjea, D.; Sheehan, K.; Rybak, L.P.; Ramkumar, V. Resveratrol reduces prostate cancer growth and metastasis by inhibiting the Akt/MicroRNA-21 pathway. PLoS One, 2012, 7(12), e51655.
[http://dx.doi.org/10.1371/journal.pone.0051655] [PMID: 23272133]
[164]
Jiao, Y.; Li, H.; Liu, Y.; Guo, A.; Xu, X.; Qu, X.; Wang, S.; Zhao, J.; Li, Y.; Cao, Y. Resveratrol inhibits the invasion of glioblastoma-initiating cells via down-regulation of the PI3K/Akt/NF-κB signaling pathway. Nutrients, 2015, 7(6), 4383-4402.
[http://dx.doi.org/10.3390/nu7064383] [PMID: 26043036]
[165]
Kanamori, M.; Kawaguchi, T.; Nigro, J.M.; Feuerstein, B.G.; Berger, M.S.; Miele, L.; Pieper, R.O. Contribution of Notch signaling activation to human glioblastoma multiforme. J. Neurosurg., 2007, 106(3), 417-427.
[http://dx.doi.org/10.3171/jns.2007.106.3.417] [PMID: 17367064]
[166]
Lino, M.M.; Merlo, A.; Boulay, J-L. Notch signaling in glioblastoma: A developmental drug target? BMC Med., 2010, 8(1), 72.
[http://dx.doi.org/10.1186/1741-7015-8-72] [PMID: 21078177]
[167]
Margareto, J.; Leis, O.; Larrarte, E.; Idoate, M.A.; Carrasco, A.; Lafuente, J.V. Gene expression profiling of human gliomas reveals differences between GBM and LGA related to energy metabolism and notch signaling pathways. J. Mol. Neurosci., 2007, 32(1), 53-63.
[http://dx.doi.org/10.1007/s12031-007-0008-5] [PMID: 17873288]
[168]
Lin, H.; Xiong, W.; Zhang, X.; Liu, B.; Zhang, W.; Zhang, Y.; Cheng, J.; Huang, H. Notch-1 activation-dependent p53 restoration contributes to resveratrol-induced apoptosis in glioblastoma cells. Oncol. Rep., 2011, 26(4), 925-930.
[PMID: 21743969]
[169]
Tavakol, S.; Ashrafizadeh, M.; Deng, S.; Azarian, M.; Abdoli, A.; Motavaf, M.; Poormoghadam, D.; Khanbabaei, H.; Afshar, E.G.; Mandegary, A.; Pardakhty, A.; Yap, C.T.; Mohammadinejad, R.; Kumar, A.P. Autophagy modulators: Mechanistic aspects and drug delivery systems. Biomolecules, 2019, 9(10), 530.
[http://dx.doi.org/10.3390/biom9100530] [PMID: 31557936]
[170]
Ashrafizadeh, M.; Yaribeygi, H.; Atkin, S.L.; Sahebkar, A. Effects of newly introduced antidiabetic drugs on autophagy. Diabetes Metab. Syndr., 2019, 13(4), 2445-2449.
[http://dx.doi.org/10.1016/j.dsx.2019.06.028] [PMID: 31405658]
[171]
Mohammadinejad, R.; Ahmadi, Z.; Tavakol, S.; Ashrafizadeh, M. Berberine as a potential autophagy modulator. J. Cell. Physiol., 2019, Ahead of Print.
[http://dx.doi.org/10.1002/jcp.28325 ] [PMID: 30770555]
[172]
Filippi-Chiela, E.C.; Villodre, E.S.; Zamin, L.L.; Lenz, G. Autophagy interplay with apoptosis and cell cycle regulation in the growth inhibiting effect of resveratrol in glioma cells. PLoS One, 2011, 6(6), e20849-e20849.
[http://dx.doi.org/10.1371/journal.pone.0020849] [PMID: 21695150]
[173]
Nitiss, J.L. DNA topoisomerase II and its growing repertoire of biological functions. Nat. Rev. Cancer, 2009, 9(5), 327-337.
[http://dx.doi.org/10.1038/nrc2608] [PMID: 19377505]
[174]
McClendon, A.K.; Osheroff, N. DNA topoisomerase II, genotoxicity, and cancer. Mutat. Res., 2007, 623(1-2), 83-97.
[http://dx.doi.org/10.1016/j.mrfmmm.2007.06.009] [PMID: 17681352]
[175]
Leone, S.; Cornetta, T.; Basso, E.; Cozzi, R. Resveratrol induces DNA double-strand breaks through human topoisomerase II interaction. Cancer Lett., 2010, 295(2), 167-172.
[http://dx.doi.org/10.1016/j.canlet.2010.02.022] [PMID: 20304553]
[176]
George, J.; Banik, N.L.; Ray, S.K. Knockdown of hTERT and concurrent treatment with interferon-gamma inhibited proliferation and invasion of human glioblastoma cell lines. Int. J. Biochem. Cell Biol., 2010, 42(7), 1164-1173.
[http://dx.doi.org/10.1016/j.biocel.2010.04.002] [PMID: 20394835]
[177]
Boldrini, L.; Pistolesi, S.; Gisfredi, S.; Ursino, S.; Ali, G.; Pieracci, N.; Basolo, F.; Parenti, G.; Fontanini, G. Telomerase activity and hTERT mRNA expression in glial tumors. Int. J. Oncol., 2006, 28(6), 1555-1560.
[http://dx.doi.org/10.3892/ijo.28.6.1555] [PMID: 16685456]
[178]
Sprouse, A.A.; Steding, C.E.; Herbert, B.S. Pharmaceutical regulation of telomerase and its clinical potential. J. Cell. Mol. Med., 2012, 16(1), 1-7.
[http://dx.doi.org/10.1111/j.1582-4934.2011.01460.x] [PMID: 21973217]
[179]
Mirzazadeh, A.; Kheirollahi, M.; Farashahi, E.; Sadeghian-Nodoushan, F.; Sheikhha, M.H.; Aflatoonian, B. Assessment effects of resveratrol on human telomerase reverse transcriptase messenger ribonucleic acid transcript in human glioblastoma. Adv. Biomed. Res., 2017, 6, 73.
[http://dx.doi.org/10.4103/2277-9175.209047] [PMID: 28706881]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy