Resveratrol as an Adjuvant for Normal Tissues Protection and Tumor Sensitization

Author(s): Keywan Mortezaee, Masoud Najafi*, Bagher Farhood*, Amirhossein Ahmadi*, Dheyauldeen Shabeeb, Ahmed E. Musa.

Journal Name: Current Cancer Drug Targets

Volume 20 , Issue 2 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Cancer is one of the most complicated diseases in present-day medical science. Yearly, several studies suggest various strategies for preventing carcinogenesis. Furthermore, experiments for the treatment of cancer with low side effects are ongoing. Chemotherapy, targeted therapy, radiotherapy and immunotherapy are the most common non-invasive strategies for cancer treatment. One of the most challenging issues encountered with these modalities is low effectiveness, as well as normal tissue toxicity for chemo-radiation therapy. The use of some agents as adjuvants has been suggested to improve tumor responses and also alleviate normal tissue toxicity. Resveratrol, a natural flavonoid, has attracted a lot of attention for the management of both tumor and normal tissue responses to various modalities of cancer therapy. As an antioxidant and anti-inflammatory agent, in vitro and in vivo studies show that it is able to mitigate chemo-radiation toxicity in normal tissues. However, clinical studies to confirm the usage of resveratrol as a chemo-radioprotector are lacking. In addition, it can sensitize various types of cancer cells to both chemotherapy drugs and radiation. In recent years, some clinical studies suggested that resveratrol may have an effect on inducing cancer cell killing. Yet, clinical translation of resveratrol has not yielded desirable results for the combination of resveratrol with radiotherapy, targeted therapy or immunotherapy. In this paper, we review the potential role of resveratrol for preserving normal tissues and sensitization of cancer cells in combination with different cancer treatment modalities.

Keywords: Resveratrol, neoplasm, radiation, radiotherapy, chemotherapy, tumor microenvironment, molecular targeted therapy.

[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Cats, A.; Jansen, E.P.M.; van Grieken, N.C.T.; Sikorska, K.; Lind, P.; Nordsmark, M.; Meershoek-Klein Kranenbarg, E.; Boot, H.; Trip, A.K.; Swellengrebel, H.A.M.; van Laarhoven, H.W.M.; Putter, H.; van Sandick, J.W.; van Berge Henegouwen, M.I.; Hartgrink, H.H.; van Tinteren, H.; van de Velde, C.J.H.; Verheij, M. Chemotherapy versus chemoradiotherapy after surgery and preoperative chemotherapy for resectable gastric cancer (CRITICS): an international, open-label, randomised phase 3 trial. Lancet Oncol., 2018, 19(5), 616-628.
[http://dx.doi.org/10.1016/S1470-2045(18)30132-3] [PMID: 29650363]
[3]
Hart, T.L.; Charles, S.T.; Gunaratne, M.; Baxter, N.N.; Cotterchio, M.; Cohen, Z.; Gallinger, S. Symptom severity and quality of life among long-term colorectal Cancer survivors compared with matched control subjects: a population-based study. Dis. Colon Rectum, 2018, 61(3), 355-363.
[http://dx.doi.org/10.1097/DCR.0000000000000972] [PMID: 29377871]
[4]
Tao, J.J.; Visvanathan, K.; Wolff, A.C. Long term side effects of adjuvant chemotherapy in patients with early breast cancer. Breast, 2015, 24(Suppl. 2), S149-S153.
[http://dx.doi.org/10.1016/j.breast.2015.07.035] [PMID: 26299406]
[5]
De Marzo, A.M.; Platz, E.A.; Sutcliffe, S.; Xu, J.; Grönberg, H.; Drake, C.G.; Nakai, Y.; Isaacs, W.B.; Nelson, W.G. Inflammation in prostate carcinogenesis. Nat. Rev. Cancer, 2007, 7(4), 256-269.
[http://dx.doi.org/10.1038/nrc2090] [PMID: 17384581]
[6]
Viennois, E.; Merlin, D.; Gewirtz, A.T.; Chassaing, B. Dietary emulsifier-induced low-grade inflammation promotes colon carcinogenesis. Cancer Res., 2017, 77(1), 27-40.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-1359] [PMID: 27821485]
[7]
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. Oxidative medicine and cellular longevity, 2016.
[http://dx.doi.org/10.1155/2016/6235641]
[8]
Gao, Q.; Zhou, G.; Lin, S.J.; Paus, R.; Yue, Z. How chemotherapy and radiotherapy damage the tissue: Comparative biology lessons from feather and hair models. Exp. Dermatol., 2018.
[PMID: 30457678]
[9]
Schaue, D.; Micewicz, E.D.; Ratikan, J.A.; Xie, M.W.; Cheng, G.; McBride, W.H. Radiation and inflammation. Semin. Radiat. Oncol., 2015, 25(1), 4-10.
[http://dx.doi.org/10.1016/j.semradonc.2014.07.007] [PMID: 25481260]
[10]
Mortezaee, K.; Salehi, E.; Mirtavoos-Mahyari, H.; Motevaseli, E.; Najafi, M.; Farhood, B.; Rosengren, R.J.; Sahebkar, A. Mechanisms of apoptosis modulation by curcumin: Implications for cancer therapy. J. Cell. Physiol., 2019, 234(8), 12537-12550.
[http://dx.doi.org/10.1002/jcp.28122] [PMID: 30623450]
[11]
Mortezaee, K.; Shabeeb, D.; Musa, A.E.; Najafi, M.; Farhood, B. Metformin as a radiation modifier; implications to normal tissue protection and tumor sensitization. Curr. Clin. Pharmacol., 2019, 14(1), 41-53.
[http://dx.doi.org/10.2174/1574884713666181025141559] [PMID: 30360725]
[12]
Movsas, B.; Scott, C.; Langer, C.; Werner-Wasik, M.; Nicolaou, N.; Komaki, R.; Machtay, M.; Smith, C.; Axelrod, R.; Sarna, L.; Wasserman, T.; Byhardt, R. Randomized trial of amifostine in locally advanced non-small-cell lung cancer patients receiving chemotherapy and hyperfractionated radiation: radiation therapy oncology group trial 98-01. J. Clin. Oncol., 2005, 23(10), 2145-2154.
[http://dx.doi.org/10.1200/JCO.2005.07.167] [PMID: 15800308]
[13]
Santini, V. Amifostine: chemotherapeutic and radiotherapeutic protective effects. Expert Opin. Pharmacother., 2001, 2(3), 479-489.
[http://dx.doi.org/10.1517/14656566.2.3.479] [PMID: 11336600]
[14]
Rades, D.; Fehlauer, F.; Bajrovic, A.; Mahlmann, B.; Richter, E.; Alberti, W. Serious adverse effects of amifostine during radiotherapy in head and neck cancer patients. Radiother. Oncol., 2004, 70(3), 261-264.
[http://dx.doi.org/10.1016/j.radonc.2003.10.005] [PMID: 15064010]
[15]
Azzam, E.I.; Jay-Gerin, J-P.; Pain, D. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett., 2012, 327(1-2), 48-60.
[http://dx.doi.org/10.1016/j.canlet.2011.12.012] [PMID: 22182453]
[16]
Reisz, J.A.; Bansal, N.; Qian, J.; Zhao, W.; Furdui, C.M. Effects of ionizing radiation on biological molecules—mechanisms of damage and emerging methods of detection. Antioxidants & redox signaling, 2014, 21(2), 260-292.
[17]
Hekim, N.; Cetin, Z.; Nikitaki, Z.; Cort, A.; Saygili, E.I. Radiation triggering immune response and inflammation. Cancer Lett., 2015, 368(2), 156-163.
[http://dx.doi.org/10.1016/j.canlet.2015.04.016] [PMID: 25911239]
[18]
Kaur, P.; Asea, A. Radiation-induced effects and the immune system in cancer. Front. Oncol., 2012, 2, 191-191.
[http://dx.doi.org/10.3389/fonc.2012.00191] [PMID: 23251903]
[19]
Laube, M.; Kniess, T.; Pietzsch, J. Development of antioxidant COX-2 inhibitors as radioprotective agents for radiation therapy-A hypothesis-driven review. Antioxidants, 2016, 5(2), 14.
[http://dx.doi.org/10.3390/antiox5020014] [PMID: 27104573]
[20]
Fernández-Gil, B.; Moneim, A.E.A.; Ortiz, F.; Shen, Y-Q.; Soto-Mercado, V.; Mendivil-Perez, M.; Guerra-Librero, A.; Acuña-Castroviejo, D.; Molina-Navarro, M.M.; García-Verdugo, J.M.; Sayed, R.K.A.; Florido, J.; Luna, J.D.; López, L.C.; Escames, G. Melatonin protects rats from radiotherapy-induced small intestine toxicity. PLoS One, 2017, 12(4)e0174474
[http://dx.doi.org/10.1371/journal.pone.0174474] [PMID: 28403142]
[21]
García, J.A.; Volt, H.; Venegas, C.; Doerrier, C.; Escames, G.; López, L.C.; Acuña-Castroviejo, D. Disruption of the NF-κB/NLRP3 connection by melatonin requires retinoid-related orphan receptor-α and blocks the septic response in mice. FASEB J., 2015, 29(9), 3863-3875.
[http://dx.doi.org/10.1096/fj.15-273656] [PMID: 26045547]
[22]
Hatoum, O.A.; Otterson, M.F.; Kopelman, D.; Miura, H.; Sukhotnik, I.; Larsen, B.T.; Selle, R.M.; Moulder, J.E.; Gutterman, D.D. Radiation induces endothelial dysfunction in murine intestinal arterioles via enhanced production of reactive oxygen species. Arterioscler. Thromb. Vasc. Biol., 2006, 26(2), 287-294.
[http://dx.doi.org/10.1161/01.ATV.0000198399.40584.8c] [PMID: 16322529]
[23]
Datta, K.; Suman, S.; Kallakury, B.V.; Fornace, A.J., Jr Exposure to heavy ion radiation induces persistent oxidative stress in mouse intestine. PLoS One, 2012, 7(8)e42224
[http://dx.doi.org/10.1371/journal.pone.0042224] [PMID: 22936983]
[24]
Chang, J.; Feng, W.; Wang, Y.; Luo, Y.; Allen, A.R.; Koturbash, I.; Turner, J.; Stewart, B.; Raber, J.; Hauer-Jensen, M.; Zhou, D.; Shao, L. Whole-body proton irradiation causes long-term damage to hematopoietic stem cells in mice. Radiat. Res., 2015, 183(2), 240-248.
[http://dx.doi.org/10.1667/RR13887.1] [PMID: 25635345]
[25]
Chatterjee, A.; Kosmacek, E.A.; Oberley-Deegan, R.E. MnTE-2-PyP treatment, or NOX4 inhibition, protects against radiation-induced damage in mouse primary prostate fibroblasts by inhibiting the TGF-Beta 1 Signaling Pathway. Radiat. Res., 2017, 187(3), 367-381.
[http://dx.doi.org/10.1667/RR14623.1] [PMID: 28225655]
[26]
Pazhanisamy, S.K.; Li, H.; Wang, Y.; Batinic-Haberle, I.; Zhou, D. NADPH oxidase inhibition attenuates total body irradiation-induced haematopoietic genomic instability. Mutagenesis, 2011, 26(3), 431-435.
[http://dx.doi.org/10.1093/mutage/ger001] [PMID: 21415439]
[27]
Choi, S-H.; Kim, M.; Lee, H-J.; Kim, E-H.; Kim, C-H.; Lee, Y-J. Effects of NOX1 on fibroblastic changes of endothelial cells in radiation-induced pulmonary fibrosis. Mol. Med. Rep., 2016, 13(5), 4135-4142.
[http://dx.doi.org/10.3892/mmr.2016.5090] [PMID: 27053172]
[28]
Park, S.; Ahn, J-Y.; Lim, M-J.; Kim, M-H.; Yun, Y-S.; Jeong, G.; Song, J-Y. Sustained expression of NADPH oxidase 4 by p38 MAPK-Akt signaling potentiates radiation-induced differentiation of lung fibroblasts. J. Mol. Med. (Berl.), 2010, 88(8), 807-816.
[http://dx.doi.org/10.1007/s00109-010-0622-5] [PMID: 20396861]
[29]
Ahmad, S.S.; Reinius, M.A.; Hatcher, H.M.; Ajithkumar, T.V. Anticancer chemotherapy in teenagers and young adults: managing long term side effects. BMJ, 2016, 354, i4567.
[http://dx.doi.org/10.1136/bmj.i4567] [PMID: 27604249]
[30]
Berenson, J.R.; Rajdev, L.; Broder, M. Treatment strategies for skeletal complications of cancer. Cancer Biol. Ther., 2006, 5(9), 1074-1077.
[http://dx.doi.org/10.4161/cbt.5.9.3305] [PMID: 16969118]
[31]
Yao, Q.; Ye, X.; Wang, L.; Gu, J.; Fu, T.; Wang, Y.; Lai, Y.; Wang, Y.; Wang, X.; Jin, H.; Guo, Y. Protective effect of curcumin on chemotherapy-induced intestinal dysfunction. Int. J. Clin. Exp. Pathol., 2013, 6(11), 2342-2349.
[PMID: 24228095]
[32]
Lohr, L. Chemotherapy-induced nausea and vomiting. Cancer J., 2008, 14(2), 85-93.
[http://dx.doi.org/10.1097/PPO.0b013e31816a0f07] [PMID: 18391612]
[33]
Lindley, C.; Goodin, S.; McCune, J.; Kane, M.; Amamoo, M.A.; Shord, S.; Pham, T.; Yowell, S.; Laliberte, K.; Schell, M.; Bernard, S.; Socinski, M.A. Prevention of delayed chemotherapy-induced nausea and vomiting after moderately high to highly emetogenic chemotherapy: comparison of ondansetron, prochlorperazine, and dexamethasone. Am. J. Clin. Oncol., 2005, 28(3), 270-276.
[http://dx.doi.org/10.1097/01.coc.0000145983.35929.2a] [PMID: 15923800]
[34]
Yeo, W.; Mo, F.K.; Suen, J.J.; Ho, W.M.; Chan, S.L.; Lau, W.; Koh, J.; Yeung, W.K.; Kwan, W.H.; Lee, K.K.; Mok, T.S.; Poon, A.N.; Lam, K.C.; Hui, E.K.; Zee, B. A randomized study of aprepitant, ondansetron and dexamethasone for chemotherapy-induced nausea and vomiting in Chinese breast cancer patients receiving moderately emetogenic chemotherapy. Breast Cancer Res. Treat., 2009, 113(3), 529-535.
[http://dx.doi.org/10.1007/s10549-008-9957-9] [PMID: 18327706]
[35]
Arpornwirat, W.; Albert, I.; Hansen, V.L.; Levin, J.; Bandekar, R.R.; Grunberg, S.M. Phase 2 trial results with the novel neurokinin-1 receptor antagonist casopitant in combination with ondansetron and dexamethasone for the prevention of chemotherapy-induced nausea and vomiting in cancer patients receiving moderately emetogenic chemotherapy. Cancer, 2009, 115(24), 5807-5816.
[http://dx.doi.org/10.1002/cncr.24630] [PMID: 19834961]
[36]
Warr, D.G.; Hesketh, P.J.; Gralla, R.J.; Muss, H.B.; Herrstedt, J.; Eisenberg, P.D.; Raftopoulos, H.; Grunberg, S.M.; Gabriel, M.; Rodgers, A.; Bohidar, N.; Klinger, G.; Hustad, C.M.; Horgan, K.J.; Skobieranda, F. Efficacy and tolerability of aprepitant for the prevention of chemotherapy-induced nausea and vomiting in patients with breast cancer after moderately emetogenic chemotherapy. J. Clin. Oncol., 2005, 23(12), 2822-2830.
[http://dx.doi.org/10.1200/JCO.2005.09.050] [PMID: 15837996]
[37]
Stein, A.; Voigt, W.; Jordan, K. Chemotherapy-induced diarrhea: pathophysiology, frequency and guideline-based management. Ther. Adv. Med. Oncol., 2010, 2(1), 51-63.
[http://dx.doi.org/10.1177/1758834009355164] [PMID: 21789126]
[38]
McQuade, R.M.; Stojanovska, V.; Abalo, R.; Bornstein, J.C.; Nurgali, K. Chemotherapy-induced constipation and diarrhea: Pathophysiology, current and emerging treatments. Front. Pharmacol., 2016, 7, 414-414.
[http://dx.doi.org/10.3389/fphar.2016.00414] [PMID: 27857691]
[39]
Mittra, I.; Pal, K.; Pancholi, N.; Shaikh, A.; Rane, B.; Tidke, P.; Kirolikar, S.; Khare, N.K.; Agrawal, K.; Nagare, H.; Nair, N.K. Prevention of chemotherapy toxicity by agents that neutralize or degrade cell-free chromatin. Ann. Oncol., 2017, 28(9), 2119-2127.
[http://dx.doi.org/10.1093/annonc/mdx318] [PMID: 28911066]
[40]
Naidu, M.U.R.; Ramana, G.V.; Rani, P.U.; Mohan, I.K.; Suman, A.; Roy, P. Chemotherapy-induced and/or radiation therapy-induced oral mucositis--complicating the treatment of cancer. Neoplasia, 2004, 6(5), 423-431.
[http://dx.doi.org/10.1593/neo.04169] [PMID: 15548350]
[41]
Peterson, D.E.; Cariello, A. Mucosal damage: a major risk factor for severe complications after cytotoxic therapy. Semin. Oncol., 2004, 31(3)(Suppl. 8), 35-44.
[http://dx.doi.org/10.1053/j.seminoncol.2004.04.006] [PMID: 15181607]
[42]
Demarosi, F.; Bez, C.; Carrassi, A. Prevention and treatment of chemo- and radiotherapy-induced oral mucositis. Minerva Stomatol., 2002, 51(5), 173-186.
[PMID: 12070468]
[43]
Nagarajan, K. Chemo-radiotherapy induced oral mucositis during IMRT for head and neck cancer - An assessment. Med. Oral Patol. Oral Cir. Bucal, 2015, 20(3), e273-e277.
[http://dx.doi.org/10.4317/medoral.20126] [PMID: 25662542]
[44]
Yazbeck, V.Y.; Villaruz, L.; Haley, M.; Socinski, M.A. Management of normal tissue toxicity associated with chemoradiation (primary skin, esophagus, and lung). Cancer J., 2013, 19(3), 231-237.
[http://dx.doi.org/10.1097/PPO.0b013e31829453fb] [PMID: 23708070]
[45]
Rancati, T.; Ceresoli, G.L.; Gagliardi, G.; Schipani, S.; Cattaneo, G.M. Factors predicting radiation pneumonitis in lung cancer patients: a retrospective study. Radiother. Oncol., 2003, 67(3), 275-283.
[http://dx.doi.org/10.1016/S0167-8140(03)00119-1] [PMID: 12865175]
[46]
Yamada, M.; Kudoh, S.; Hirata, K.; Nakajima, T.; Yoshikawa, J. Risk factors of pneumonitis following chemoradiotherapy for lung cancer. Eur. J. Cancer, 1998, 34(1), 71-75.
[http://dx.doi.org/10.1016/S0959-8049(97)00377-8] [PMID: 9624240]
[47]
Ataee, R.; Shokrzadeh, M.; Jafari-Sabet, M.; Nasrabadi Nasri, N.; Ataie, A.; Haghi Aminjan, H. The role of melatonin and melatonin receptors in pharmacology and pharmacotherapy of cancer. Austin Oncol, 2017, 2(1), 1015.
[48]
Haghi-Aminjan, H.; Asghari, M.H.; Farhood, B.; Rahimifard, M.; Hashemi Goradel, N.; Abdollahi, M. The role of melatonin on chemotherapy-induced reproductive toxicity. J. Pharm. Pharmacol., 2018, 70(3), 291-306.
[http://dx.doi.org/10.1111/jphp.12855] [PMID: 29168173]
[49]
Khalil Arjmandi, M.; Moslemi, D.; Sadati Zarrini, A.; Ebrahimnezhad Gorji, M.; Mosapour, A.; Haghhaghighi, A.; Halalkhor, S.; Bijani, A.; Parsian, H. Pre and post radiotherapy serum oxidant/antioxidant status in breast cancer patients: Impact of age, BMI and clinical stage of the disease. Rep. Pract. Oncol. Radiother., 2016, 21(3), 141-148.
[http://dx.doi.org/10.1016/j.rpor.2015.12.009] [PMID: 27601942]
[50]
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.
[http://dx.doi.org/10.1016/j.jddst.2019.03.017]
[51]
de la Lastra, C.A.; Villegas, I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem. Soc. Trans., 2007, 35(Pt 5), 1156-1160.
[http://dx.doi.org/10.1042/BST0351156] [PMID: 17956300]
[52]
Koohian, F.; Shanei, A.; Shahbazi-Gahrouei, D.; Hejazi, S.H.; Moradi, M-T. The radioprotective effect of resveratrol against genotoxicity induced by γ-irradiation in mice blood lymphocytes. Dose Response, 2017, 15(2), 1559325817705699-1559325817705699.
[http://dx.doi.org/10.1177/1559325817705699] [PMID: 28566983]
[53]
Carsten, R.E.; Bachand, A.M.; Bailey, S.M.; Ullrich, R.L. Resveratrol reduces radiation-induced chromosome aberration frequencies in mouse bone marrow cells. Radiat. Res., 2008, 169(6), 633-638.
[http://dx.doi.org/10.1667/RR1190.1] [PMID: 18494544]
[54]
Fabre, K.M.; Saito, K.; DeGraff, W.; Sowers, A.L.; Thetford, A.; Cook, J.A.; Krishna, M.C.; Mitchell, J.B. The effects of resveratrol and selected metabolites on the radiation and antioxidant response. Cancer Biol. Ther., 2011, 12(10), 915-923.
[http://dx.doi.org/10.4161/cbt.12.10.17714] [PMID: 22024758]
[55]
Picard, F.; Kurtev, M.; Chung, N.; Topark-Ngarm, A.; Senawong, T.; Machado De Oliveira, R.; Leid, M.; McBurney, M.W.; Guarente, L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature, 2004, 429(6993), 771-776.
[http://dx.doi.org/10.1038/nature02583] [PMID: 15175761]
[56]
Kobayashi, Y.; Furukawa-Hibi, Y.; Chen, C.; Horio, Y.; Isobe, K.; Ikeda, K.; Motoyama, N. SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int. J. Mol. Med., 2005, 16(2), 237-243.
[http://dx.doi.org/10.3892/ijmm.16.2.237] [PMID: 16012755]
[57]
Motta, M.C.; Divecha, N.; Lemieux, M.; Kamel, C.; Chen, D.; Gu, W.; Bultsma, Y.; McBurney, M.; Guarente, L. Mammalian SIRT1 represses forkhead transcription factors. Cell, 2004, 116(4), 551-563.
[http://dx.doi.org/10.1016/S0092-8674(04)00126-6] [PMID: 14980222]
[58]
Lee, J.T.; Gu, W. SIRT1: Regulator of p53 deacetylation. Genes Cancer, 2013, 4(3-4), 112-117.
[http://dx.doi.org/10.1177/1947601913484496] [PMID: 24020002]
[59]
Gonfloni, S.; Iannizzotto, V.; Maiani, E.; Bellusci, G.; Ciccone, S.; Diederich, M. P53 and Sirt1: Routes of metabolism and genome stability. Biochem. Pharmacol., 2014, 92(1), 149-156.
[http://dx.doi.org/10.1016/j.bcp.2014.08.034] [PMID: 25218422]
[60]
Hori, Y.S.; Kuno, A.; Hosoda, R.; Horio, Y. Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS One, 2013, 8(9)e73875
[http://dx.doi.org/10.1371/journal.pone.0073875] [PMID: 24040102]
[61]
Zhang, H.; Yan, H.; Zhou, X.; Wang, H.; Yang, Y.; Zhang, J.; Wang, H. The protective effects of Resveratrol against radiation-induced intestinal injury. BMC Complement. Altern. Med., 2017, 17(1), 410-410.
[http://dx.doi.org/10.1186/s12906-017-1915-9] [PMID: 28814292]
[62]
Zhang, H.; Zhai, Z.; Wang, Y.; Zhang, J.; Wu, H.; Wang, Y.; Li, C.; Li, D.; Lu, L.; Wang, X.; Chang, J.; Hou, Q.; Ju, Z.; Zhou, D.; Meng, A. Resveratrol ameliorates ionizing irradiation-induced long-term hematopoietic stem cell injury in mice. Free Radic. Biol. Med., 2013, 54, 40-50.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.10.530] [PMID: 23124026]
[63]
Azmoonfar, R.; Amini, P.; Yahyapour, R.; Rezaeyan, A.; Tavassoli, A.; Motevaseli, E.; Khodamoradi, E.; Shabeeb, D.; Musa, A.E.; Najafi, M. Mitigation of radiation-induced pneumonitis and lung fibrosis using alpha-lipoic acid and resveratrol. Antiinflamm. Antiallergy Agents Med. Chem., 2019.
[http://dx.doi.org/10.2174/1871523018666190319144020] [PMID: 30892165]
[64]
Gülçin, İ. Antioxidant properties of resveratrol: A structure–activity insight. Innov. Food Sci. Emerg. Technol., 2010, 11(1), 210-218.
[http://dx.doi.org/10.1016/j.ifset.2009.07.002]
[65]
Xia, N.; Daiber, A.; Förstermann, U.; Li, H. Antioxidant effects of resveratrol in the cardiovascular system. Br. J. Pharmacol., 2017, 174(12), 1633-1646.
[http://dx.doi.org/10.1111/bph.13492] [PMID: 27058985]
[66]
Hamlaoui, S.; Mokni, M.; Limam, N.; Carrier, A.; Limam, F.; Amri, M.; Marzouki, L.; Aouani, E. Resveratrol protects against acute chemotherapy toxicity induced by doxorubucin in rat erythrocyte and plasma. J. Physiol. Pharmacol., 2012, 63(3), 293-301.
[PMID: 22791644]
[67]
Dudka, J.; Gieroba, R.; Korga, A.; Burdan, F.; Matysiak, W.; Jodlowska-Jedrych, B.; Mandziuk, S.; Korobowicz, E.; Murias, M. Different effects of resveratrol on dose-related doxorubicin-induced heart and liver toxicity. Evidence-Based Complementary and Alternative Medicine, 2012.
[http://dx.doi.org/10.1155/2012/606183]
[68]
Singh, I.; Goyal, Y.; Ranawat, P. Potential chemoprotective role of resveratrol against cisplatin induced testicular damage in mice. Chem. Biol. Interact., 2017, 273, 200-211.
[http://dx.doi.org/10.1016/j.cbi.2017.05.024] [PMID: 28606469]
[69]
Reddy, K.P.; Madhu, P.; Reddy, P.S. Protective effects of resveratrol against cisplatin-induced testicular and epididymal toxicity in rats. Food Chem. Toxicol., 2016, 91, 65-72.
[http://dx.doi.org/10.1016/j.fct.2016.02.017] [PMID: 26925769]
[70]
Lee, A.M.; Shandala, T.; Soo, P.P.; Su, Y.W.; King, T.J.; Chen, K.M.; Howe, P.R.; Xian, C.J. Effects of resveratrol supplementation on methotrexate chemotherapy‐induced bone loss. Nutrients, 2017, 9(3), 255.
[http://dx.doi.org/10.3390/nu9030255] [PMID: 28282956]
[71]
Whiteside, T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene, 2008, 27(45), 5904-5912.
[http://dx.doi.org/10.1038/onc.2008.271] [PMID: 18836471]
[72]
Najafi, M.; Goradel, N.H.; Farhood, B.; Salehi, E.; Solhjoo, S.; Toolee, H.; Kharazinejad, E.; Mortezaee, K. Tumor microenvironment: Interactions and therapy. J. Cell. Physiol., 2019, 234(5), 5700-5721.
[http://dx.doi.org/10.1002/jcp.27425] [PMID: 30378106]
[73]
Shieh, Y.S.; Hung, Y.J.; Hsieh, C.B.; Chen, J.S.; Chou, K.C.; Liu, S.Y. Tumor-associated macrophage correlated with angiogenesis and progression of mucoepidermoid carcinoma of salivary glands. Ann. Surg. Oncol., 2009, 16(3), 751-760.
[http://dx.doi.org/10.1245/s10434-008-0259-6] [PMID: 19116756]
[74]
Chen, Y.; Tan, W.; Wang, C. Tumor-associated macrophage-derived cytokines enhance cancer stem-like characteristics through epithelial-mesenchymal transition. OncoTargets Ther., 2018, 11, 3817-3826.
[http://dx.doi.org/10.2147/OTT.S168317] [PMID: 30013362]
[75]
Shi, X.; Shiao, S.L. The role of macrophage phenotype in regulating the response to radiation therapy. Transl. Res., 2018, 191, 64-80.
[http://dx.doi.org/10.1016/j.trsl.2017.11.002] [PMID: 29175267]
[76]
Mantovani, A.; Sica, A.; Allavena, P.; Garlanda, C.; Locati, M. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Hum. Immunol., 2009, 70(5), 325-330.
[http://dx.doi.org/10.1016/j.humimm.2009.02.008] [PMID: 19236898]
[77]
Litviakov, N.; Tsyganov, M.; Larionova, I.; Ibragimova, M.; Deryusheva, I.; Kazantseva, P.; Slonimskaya, E.; Frolova, I.; Choinzonov, E.; Cherdyntseva, N.; Kzhyshkowska, J. Expression of M2 macrophage markers YKL-39 and CCL18 in breast cancer is associated with the effect of neoadjuvant chemotherapy. Cancer Chemother. Pharmacol., 2018, 82(1), 99-109.
[http://dx.doi.org/10.1007/s00280-018-3594-8] [PMID: 29728799]
[78]
Russell, J.S.; Brown, J.M. The irradiated tumor microenvironment: role of tumor-associated macrophages in vascular recovery. Front. Physiol., 2013, 4, 157-157.
[http://dx.doi.org/10.3389/fphys.2013.00157] [PMID: 23882218]
[79]
Chaudhary, B.; Elkord, E.; Regulatory, T. Regulatory T cells in the tumor microenvironment and cancer progression: Role and therapeutic targeting. Vaccines (Basel), 2016, 4(3), 28.
[http://dx.doi.org/10.3390/vaccines4030028] [PMID: 27509527]
[80]
Jang, M.; Cai, L.; Udeani, G.O.; Slowing, K.V.; Thomas, C.F.; Beecher, C.W.; Fong, H.H.; Farnsworth, N.R.; Kinghorn, A.D.; Mehta, R.G.; Moon, R.C.; Pezzuto, J.M. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science, 1997, 275(5297), 218-220.
[http://dx.doi.org/10.1126/science.275.5297.218] [PMID: 8985016]
[81]
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]
[82]
Shukla, Y.; Singh, R. Resveratrol and cellular mechanisms of cancer prevention. Ann. N. Y. Acad. Sci., 2011, 1215(1), 1-8.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05870.x] [PMID: 21261635]
[83]
Jang, M.; Pezzuto, J.M. Cancer chemopreventive activity of resveratrol. Drugs Exp. Clin. Res., 1999, 25(2-3), 65-77.
[PMID: 10370867]
[84]
Bhat, K.P.; Pezzuto, J.M. Cancer chemopreventive activity of resveratrol. Ann. N. Y. Acad. Sci., 2002, 957, 210-229.
[http://dx.doi.org/10.1111/j.1749-6632.2002.tb02918.x] [PMID: 12074974]
[85]
Hogg, S.J.; Chitcholtan, K.; Hassan, W.; Sykes, P.H.; Garrill, A. Resveratrol, acetyl-resveratrol, and polydatin exhibit antigrowth activity against 3D cell aggregates of the SKOV-3 and OVCAR-8 ovarian cancer cell lines. Obstet. Gynecol. Int., 2015.2015279591
[http://dx.doi.org/10.1155/2015/279591] [PMID: 26617640]
[86]
Subbaramaiah, K.; Chung, W.J.; Michaluart, P.; Telang, N.; Tanabe, T.; Inoue, H.; Jang, M.; Pezzuto, J.M.; Dannenberg, A.J. Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J. Biol. Chem., 1998, 273(34), 21875-21882.
[http://dx.doi.org/dx.d oi.org/10.1074/jbc.273.34.21875] [PMID: 9705326]
[87]
Fulda, S. Resveratrol and derivatives for the prevention and treatment of cancer. Drug Discov. Today, 2010, 15(17-18), 757-765.
[http://dx.doi.org/10.1016/j.drudis.2010.07.005] [PMID: 20692359]
[88]
Jiang, Z.; Chen, K.; Cheng, L.; Yan, B.; Qian, W.; Cao, J.; Li, J.; Wu, E.; Ma, Q.; Yang, W. Resveratrol and cancer treatment: updates. Ann. N. Y. Acad. Sci., 2017, 1403(1), 59-69.
[http://dx.doi.org/10.1111/nyas.13466] [PMID: 28945938]
[89]
Zhang, B.; Yin, X.; Sui, S. Resveratrol inhibited the progression of human hepatocellular carcinoma by inducing autophagy via regulating p53 and the phosphoinositide 3-kinase/protein kinase B pathway. Oncol. Rep., 2018, 40(5), 2758-2765.
[http://dx.doi.org/10.3892/or.2018.6648] [PMID: 30132535]
[90]
Park, D.; Jeong, H.; Lee, M.N.; Koh, A.; Kwon, O.; Yang, Y.R.; Noh, J.; Suh, P-G.; Park, H.; Ryu, S.H. Resveratrol induces autophagy by directly inhibiting mTOR through ATP competition. Sci. Rep., 2016, 6, 21772.
[http://dx.doi.org/10.1038/srep21772] [PMID: 26902888]
[91]
Hu, L.; Wang, H.; Huang, L.; Zhao, Y.; Wang, J. Crosstalk between autophagy and intracellular radiation response.(Review) Int. J. Oncol., 2016, 49(6), 2217-2226. [Review]
[http://dx.doi.org/ 10.3892/ijo.2016.3719] [PMID: 27748893]
[92]
Wu, S.Y.; Liu, Y.W.; Wang, Y.K.; Lin, T.H.; Li, Y.Z.; Chen, S.H.; Lee, Y.R. Ionizing radiation induces autophagy in human oral squamous cell carcinoma. J. BUON, 2014, 19(1), 137-144.
[PMID: 24659655]
[93]
Chen, Y.S.; Song, H.X.; Lu, Y.; Li, X.; Chen, T.; Zhang, Y.; Xue, J.X.; Liu, H.; Kan, B.; Yang, G.; Fu, T. Autophagy inhibition contributes to radiation sensitization of esophageal squamous carcinoma cells. Dis. Esophagus, 2011, 24(6), 437-443.
[http://dx.doi.org/10.1111/j.1442-2050.2010.01156.x] [PMID: 21166739]
[94]
Chen, Y.; Li, X.; Guo, L.; Wu, X.; He, C.; Zhang, S.; Xiao, Y.; Yang, Y.; Hao, D. Combining radiation with autophagy inhibition enhances suppression of tumor growth and angiogenesis in esophageal cancer. Mol. Med. Rep., 2015, 12(2), 1645-1652.
[http://dx.doi.org/10.3892/mmr.2015.3623] [PMID: 25891159]
[95]
Sun, Q.; Liu, T.; Yuan, Y.; Guo, Z.; Xie, G.; Du, S.; Lin, X.; Xu, Z.; Liu, M.; Wang, W.; Yuan, Q.; Chen, L. MiR-200c inhibits autophagy and enhances radiosensitivity in breast cancer cells by targeting UBQLN1. Int. J. Cancer, 2015, 136(5), 1003-1012.
[http://dx.doi.org/10.1002/ijc.29065] [PMID: 25044403]
[96]
Mo, N.; Lu, Y.K.; Xie, W.M.; Liu, Y.; Zhou, W.X.; Wang, H.X.; Nong, L.; Jia, Y.X.; Tan, A.H.; Chen, Y.; Li, S.S.; Luo, B.H. Inhibition of autophagy enhances the radiosensitivity of nasopharyngeal carcinoma by reducing Rad51 expression. Oncol. Rep., 2014, 32(5), 1905-1912.
[http://dx.doi.org/10.3892/or.2014.3427] [PMID: 25175062]
[97]
Li, F.; Zheng, X.; Liu, Y.; Li, P.; Liu, X.; Ye, F.; Zhao, T.; Wu, Q.; Jin, X.; Li, Q. Different roles of CHOP and JNK in mediating radiation-induced autophagy and apoptosis in breast cancer cells. Radiat. Res., 2016, 185(5), 539-548.
[http://dx.doi.org/10.1667/RR14344.1] [PMID: 27135967]
[98]
Lu, C.; Xie, C. Radiation-induced autophagy promotes esophageal squamous cell carcinoma cell survival via the LKB1 pathway. Oncol. Rep., 2016, 35(6), 3559-3565.
[http://dx.doi.org/10.3892/or.2016.4753] [PMID: 27109915]
[99]
Chiu, H.W.; Fang, W.H.; Chen, Y.L.; Wu, M.D.; Yuan, G.F.; Ho, S.Y.; Wang, Y.J. Monascuspiloin enhances the radiation sensitivity of human prostate cancer cells by stimulating endoplasmic reticulum stress and inducing autophagy. PLoS One, 2012, 7(7)e40462
[http://dx.doi.org/10.1371/journal.pone.0040462] [PMID: 22802963]
[100]
Zheng, R.; Yao, Q.; Du, S.; Ren, C.; Sun, Q.; Xu, Z.; Lin, X.; Yuan, Y. The status of p53 in cancer cells affects the role of autophagy in tumor radiosensitisation. J. BUON, 2014, 19(2), 336-341.
[PMID: 24965389]
[101]
Bristol, M.L.; Di, X.; Beckman, M.J.; Wilson, E.N.; Henderson, S.C.; Maiti, A.; Fan, Z.; Gewirtz, D.A. Dual functions of autophagy in the response of breast tumor cells to radiation: cytoprotective autophagy with radiation alone and cytotoxic autophagy in radiosensitization by vitamin D 3. Autophagy, 2012, 8(5), 739-753.
[http://dx.doi.org/10.4161/auto.19313] [PMID: 22498493]
[102]
Ko, A.; Kanehisa, A.; Martins, I.; Senovilla, L.; Chargari, C.; Dugue, D.; Mariño, G.; Kepp, O.; Michaud, M.; Perfettini, J.L.; Kroemer, G.; Deutsch, E. Autophagy inhibition radiosensitizes in vitro, yet reduces radioresponses in vivo due to deficient immunogenic signalling. Cell Death Differ., 2014, 21(1), 92-99.
[http://dx.doi.org/10.1038/cdd.2013.124] [PMID: 24037090]
[103]
Wang, L.; Long, L.; Wang, W.; Liang, Z. Resveratrol, a potential radiation sensitizer for glioma stem cells both in vitro and in vivo. J. Pharmacol. Sci., 2015, 129(4), 216-225.
[http://dx.doi.org/10.1016/j.jphs.2015.11.001] [PMID: 26698406]
[104]
Osman, A.M.; Bayoumi, H.M.; Al-Harthi, S.E.; Damanhouri, Z.A.; Elshal, M.F. Modulation of doxorubicin cytotoxicity by resveratrol in a human breast cancer cell line. Cancer Cell Int., 2012, 12(1), 47.
[http://dx.doi.org/10.1186/1475-2867-12-47] [PMID: 23153194]
[105]
Sprouse, A.A.; Herbert, B.S. Resveratrol augments paclitaxel treatment in MDA-MB-231 and paclitaxel-resistant MDA-MB-231 breast cancer cells. Anticancer Res., 2014, 34(10), 5363-5374.
[PMID: 25275030]
[106]
Fulda, S.; Debatin, K.M. Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene, 2004, 23(40), 6702-6711.
[http://dx.doi.org/10.1038/sj.onc.1207630] [PMID: 15273734]
[107]
Jazirehi, A.R.; Bonavida, B. Resveratrol modifies the expression of apoptotic regulatory proteins and sensitizes non-Hodgkin’s lymphoma and multiple myeloma cell lines to paclitaxel-induced apoptosis. Mol. Cancer Ther., 2004, 3(1), 71-84.
[PMID: 14749477]
[108]
Gatouillat, G.; Balasse, E.; Joseph-Pietras, D.; Morjani, H.; Madoulet, C. Resveratrol induces cell-cycle disruption and apoptosis in chemoresistant B16 melanoma. J. Cell. Biochem., 2010, 110(4), 893-902.
[http://dx.doi.org/10.1002/jcb.22601] [PMID: 20564188]
[109]
Buhrmann, C.; Shayan, P.; Kraehe, P.; Popper, B.; Goel, A.; Shakibaei, M. Resveratrol induces chemosensitization to 5-fluorouracil through up-regulation of intercellular junctions, Epithelial-to-mesenchymal transition and apoptosis in colorectal cancer. Biochem. Pharmacol., 2015, 98(1), 51-68.
[http://dx.doi.org/10.1016/j.bcp.2015.08.105] [PMID: 26310874]
[110]
Buhrmann, C.; Yazdi, M.; Popper, B.; Shayan, P.; Goel, A.; Aggarwal, B.B.; Shakibaei, M. Resveratrol chemosensitizes TNF-β-induced survival of 5-FU-treated colorectal cancer cells. Nutrients, 2018, 10(7)E888
[http://dx.doi.org/10.3390/nu10070888] [PMID: 30002278]
[111]
Chung, S.S.; Dutta, P.; Austin, D.; Wang, P.; Awad, A.; Vadgama, J.V. Combination of resveratrol and 5-flurouracil enhanced anti-telomerase activity and apoptosis by inhibiting STAT3 and Akt signaling pathways in human colorectal cancer cells. Oncotarget, 2018, 9(68), 32943-32957.
[http://dx.doi.org/10.18632/oncotarget.25993] [PMID: 30250641]
[112]
Quan, F.; Pan, C.; Ma, Q.; Zhang, S.; Yan, L. Reversal effect of resveratrol on multidrug resistance in KBv200 cell line. Biomed. Pharmacother., 2008, 62(9), 622-629.
[http://dx.doi.org/10.1016/j.biopha.2008.07.089] [PMID: 18804944]
[113]
Hernandez-Valencia, J.; Garcia-Villa, E.; Arenas-Hernandez, A.; Garcia-Mena, J.; Diaz-Chavez, J.; Gariglio, P. Induction of p53 phosphorylation at serine 20 by resveratrol is required to activate p53 target genes, restoring apoptosis in MCF-7 cells resistant to cisplatin. Nutrients, 2018, 10(9)E1148
[http://dx.doi.org/10.3390/nu10091148] [PMID: 30142917]
[114]
Khanzadeh, T.; Hagh, M.F.; Talebi, M.; Yousefi, B.; Azimi, A.; Hossein Pour Feizi, A.A.; Baradaran, B. Investigation of BAX and BCL2 expression and apoptosis in a resveratrol- and prednisolone-treated human T-ALL cell line, CCRF-CEM. Blood Res., 2018, 53(1), 53-60.
[http://dx.doi.org/10.5045/br.2018.53.1.53] [PMID: 29662863]
[115]
Zadi Heydarabad, M.; Vatanmakanian, M.; Abdolalizadeh, J.; Mohammadi, H.; Azimi, A.; Mousavi Ardehaie, R.; Movasaghpour, A.; Farshdousti Hagh, M. Apoptotic effect of resveratrol on human T-ALL cell line CCRF-CEM is unlikely exerted through alteration of BAX and BCL2 promoter methylation. J. Cell. Biochem., 2018, 119(12), 10033-10040.
[http://dx.doi.org/10.1002/jcb.27333] [PMID: 30132966]
[116]
Lin, C.J.; Lee, C.C.; Shih, Y.L.; Lin, T.Y.; Wang, S.H.; Lin, Y.F.; Shih, C.M. Resveratrol enhances the therapeutic effect of temozolomide against malignant glioma in vitro and in vivo by inhibiting autophagy. Free Radic. Biol. Med., 2012, 52(2), 377-391.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.10.487] [PMID: 22094224]
[117]
Vinod, B.S.; Nair, H.H.; Vijayakurup, V.; Shabna, A.; Shah, S.; Krishna, A.; Pillai, K.S.; Thankachan, S.; Anto, R.J. Resveratrol chemosensitizes HER-2-overexpressing breast cancer cells to docetaxel chemoresistance by inhibiting docetaxel-mediated activation of HER-2-Akt axis. Cell Death Discov., 2015, 1, 15061.
[http://dx.doi.org/10.1038/cddiscovery.2015.61] [PMID: 27551486]
[118]
Fukui, M.; Yamabe, N.; Zhu, B.T. Resveratrol attenuates the anticancer efficacy of paclitaxel in human breast cancer cells in vitro and in vivo. Eur. J. Cancer, 2010, 46(10), 1882-1891.
[http://dx.doi.org/10.1016/j.ejca.2010.02.004] [PMID: 20223651]
[119]
Zunino, S.J.; Storms, D.H.; Newman, J.W.; Pedersen, T.L.; Keen, C.L.; Ducore, J.M. Dietary resveratrol does not delay engraftment, sensitize to vincristine or inhibit growth of high-risk acute lymphoblastic leukemia cells in NOD/SCID mice. Int. J. Oncol., 2012, 41(6), 2207-2212.
[http://dx.doi.org/10.3892/ijo.2012.1650] [PMID: 23041950]
[120]
Benitez, D.A.; Pozo-Guisado, E.; Alvarez-Barrientos, A.; Fernandez-Salguero, P.M.; Castellón, E.A. Mechanisms involved in resveratrol-induced apoptosis and cell cycle arrest in prostate cancer-derived cell lines. J. Androl., 2007, 28(2), 282-293.
[http://dx.doi.org/10.2164/jandrol.106.000968] [PMID: 17050787]
[121]
Fang, Y.; Herrick, E.J.; Nicholl, M.B. A possible role for perforin and granzyme B in resveratrol-enhanced radiosensitivity of prostate cancer. J. Androl., 2012, 33(4), 752-760.
[http://dx.doi.org/10.2164/jandrol.111.015164] [PMID: 22096086]
[122]
Scarlatti, F.; Sala, G.; Ricci, C.; Maioli, C.; Milani, F.; Minella, M.; Botturi, M.; Ghidoni, R. Resveratrol sensitization of DU145 prostate cancer cells to ionizing radiation is associated to ceramide increase. Cancer Lett., 2007, 253(1), 124-130.
[http://dx.doi.org/10.1016/j.canlet.2007.01.014] [PMID: 17321671]
[123]
Fang, Y.; DeMarco, V.G.; Nicholl, M.B. Resveratrol enhances radiation sensitivity in prostate cancer by inhibiting cell proliferation and promoting cell senescence and apoptosis. Cancer Sci., 2012, 103(6), 1090-1098.
[http://dx.doi.org/10.1111/j.1349-7006.2012.02272.x] [PMID: 22417066]
[124]
Rashid, A.; Liu, C.; Sanli, T.; Tsiani, E.; Singh, G.; Bristow, R.G.; Dayes, I.; Lukka, H.; Wright, J.; Tsakiridis, T. Resveratrol enhances prostate cancer cell response to ionizing radiation. Modulation of the AMPK, Akt and mTOR pathways. Radiat. Oncol., 2011, 6(1), 144.
[http://dx.doi.org/10.1186/1748-717X-6-144] [PMID: 22029423]
[125]
Baatout, S.; Derradji, H.; Jacquet, P.; Ooms, D.; Michaux, A.; Mergeay, M. Enhanced radiation-induced apoptosis of cancer cell lines after treatment with resveratrol. Int. J. Mol. Med., 2004, 13(6), 895-902.
[http://dx.doi.org/10.3892/ijmm.13.6.895] [PMID: 15138632]
[126]
Baatout, S.; Derradji, H.; Jacquet, P.; Mergeay, M. Increased radiation sensitivity of an eosinophilic cell line following treatment with epigallocatechin-gallate, resveratrol and curcuma. Int. J. Mol. Med., 2005, 15(2), 337-352.
[http://dx.doi.org/10.3892/ijmm.15.2.337] [PMID: 15647852]
[127]
Sclafani, R.; Siriwardana, S.; Frederick, B.; Stahringer, S.; Tyagi, A.; Jimeno, A.; Agarwal, R.; Raben, D. Abstract #3989: Combined Resveratrol and radiation therapy in head and neck cancer. Cancer Res., 2009, 69(9)(Suppl.), 3989-3989.
[128]
Fang, Y.; Bradley, M.J.; Cook, K.M.; Herrick, E.J.; Nicholl, M.B. A potential role for resveratrol as a radiation sensitizer for melanoma treatment. J. Surg. Res., 2013, 183(2), 645-653.
[http://dx.doi.org/10.1016/j.jss.2013.02.037] [PMID: 23522452]
[129]
da Costa Araldi, I.C.; Bordin, F.P.R.; Cadoná, F.C.; Barbisan, F.; Azzolin, V.F.; Teixeira, C.F.; Baumhardt, T.; da Cruz, I.B.M.; Duarte, M.M.M.F.; Bauermann, L.F. The in vitro radiosensitizer potential of resveratrol on MCF-7 breast cancer cells. Chem. Biol. Interact., 2018, 282, 85-92.
[http://dx.doi.org/10.1016/j.cbi.2018.01.013] [PMID: 29336987]
[130]
Fiore, M.; Festa, F.; Cornetta, T.; Ricordy, R.; Cozzi, R. Resveratrol affects X-ray induced apoptosis and cell cycle delay in human cells in vitro. Int. J. Mol. Med., 2005, 15(6), 1005-1012.
[http://dx.doi.org/10.3892/ijmm.15.6.1005] [PMID: 15870907]
[131]
Zoberi, I.; Bradbury, C.M.; Curry, H.A.; Bisht, K.S.; Goswami, P.C.; Roti Roti, J.L.; Gius, D. Radiosensitizing and anti-proliferative effects of resveratrol in two human cervical tumor cell lines. Cancer Lett., 2002, 175(2), 165-173.
[http://dx.doi.org/10.1016/S0304-3835(01)00719-4] [PMID: 11741744]
[132]
Baek, S.H.; Ko, J-H.; Lee, H.; Jung, J.; Kong, M.; Lee, J.W.; Lee, J.; Chinnathambi, A.; Zayed, M.E.; Alharbi, S.A.; Lee, S-G.; Shim, B.S.; Sethi, G.; Kim, S-H.; Yang, W.M.; Um, J-Y.; Ahn, K.S. Resveratrol inhibits STAT3 signaling pathway through the induction of SOCS-1: Role in apoptosis induction and radiosensitization in head and neck tumor cells. Phytomedicine, 2016, 23(5), 566-577.
[http://dx.doi.org/10.1016/j.phymed.2016.02.011] [PMID: 27064016]
[133]
Luo, H.; Wang, L.; Schulte, B.A.; Yang, A.; Tang, S.; Wang, G.Y. Resveratrol enhances ionizing radiation-induced premature senescence in lung cancer cells. Int. J. Oncol., 2013, 43(6), 1999-2006.
[http://dx.doi.org/10.3892/ijo.2013.2141] [PMID: 24141489]
[134]
Kao, C-L.; Huang, P-I.; Tsai, P-H.; Tsai, M-L.; Lo, J-F.; Lee, Y-Y.; Chen, Y-J.; Chen, Y-W.; Chiou, S-H. Resveratrol-Induced Apoptosis and Increased Radiosensitivity in CD133-Positive Cells Derived From Atypical Teratoid/Rhabdoid Tumor. Int. J. Radiat. Oncol. Biol. Phys., 2009, 74(1), 219-228.
[135]
Bosch-Presegué, L.; Vaquero, A. The dual role of sirtuins in cancer. Genes Cancer, 2011, 2(6), 648-662.
[http://dx.doi.org/10.1177/1947601911417862] [PMID: 21941620]
[136]
Yang, Q.; Wang, B.; Zang, W.; Wang, X.; Liu, Z.; Li, W.; Jia, J. Resveratrol inhibits the growth of gastric cancer by inducing G1 phase arrest and senescence in a Sirt1-dependent manner. PLoS One, 2013, 8(11)e70627
[http://dx.doi.org/10.1371/journal.pone.0070627] [PMID: 24278101]
[137]
Ji, K.; Sun, X.; Liu, Y.; Du, L.; Wang, Y.; He, N.; Wang, J.; Xu, C.; Liu, Q. Regulation of apoptosis and radiation sensitization in lung cancer cells via the Sirt1/NF-κB/Smac pathway. Cell. Physiol. Biochem., 2018, 48(1), 304-316.
[http://dx.doi.org/10.1159/000491730] [PMID: 30016782]
[138]
Yan, L.; Rosen, N.; Arteaga, C. Targeted cancer therapies. Chin. J. Cancer, 2011, 30(1), 1-4.
[http://dx.doi.org/10.5732/cjc.010.10553] [PMID: 21192839]
[139]
Chan, C.C. In Gynecological Drug Therapy; CRC Press, 2016, pp. 105-110.
[140]
Giles, F.J.; Cortes, J.E.; Kantarjian, H.M. Targeting the kinase activity of the BCR-ABL fusion protein in patients with chronic myeloid leukemia. Curr. Mol. Med., 2005, 5(7), 615-623.
[http://dx.doi.org/10.2174/156652405774641115] [PMID: 16305488]
[141]
Chottanapund, S.; Van Duursen, M.B.; Navasumrit, P.; Hunsonti, P.; Timtavorn, S.; Ruchirawat, M.; Van den Berg, M. Anti-aromatase effect of resveratrol and melatonin on hormonal positive breast cancer cells co-cultured with breast adipose fibroblasts. Toxicol. In Vitro, 2014, 28(7), 1215-1221.
[http://dx.doi.org/10.1016/j.tiv.2014.05.015] [PMID: 24929094]
[142]
Kim, C.; Baek, S.H.; Um, J.Y.; Shim, B.S.; Ahn, K.S. Resveratrol attenuates constitutive STAT3 and STAT5 activation through induction of PTPε and SHP-2 tyrosine phosphatases and potentiates sorafenib-induced apoptosis in renal cell carcinoma. BMC Nephrol., 2016, 17, 19.
[http://dx.doi.org/10.1186/s12882-016-0233-7] [PMID: 26911335]
[143]
Perey, L.; Paridaens, R.; Hawle, H.; Zaman, K.; Nolé, F.; Wildiers, H.; Fiche, M.; Dietrich, D.; Clément, P.; Köberle, D.; Goldhirsch, A.; Thürlimann, B. Clinical benefit of fulvestrant in postmenopausal women with advanced breast cancer and primary or acquired resistance to aromatase inhibitors: final results of phase II Swiss Group for Clinical Cancer Research Trial (SAKK 21/00). Ann. Oncol., 2007, 18(1), 64-69.
[http://dx.doi.org/10.1093/annonc/mdl341] [PMID: 17030543]
[144]
Yang, J.; Weinberg, R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell, 2008, 14(6), 818-829.
[http://dx.doi.org/10.1016/j.devcel.2008.05.009] [PMID: 18539112]
[145]
Shi, X-P.; Miao, S.; Wu, Y.; Zhang, W.; Zhang, X-F.; Ma, H-Z.; Xin, H-L.; Feng, J.; Wen, A-D.; Li, Y. Resveratrol sensitizes tamoxifen in antiestrogen-resistant breast cancer cells with epithelial-mesenchymal transition features. Int. J. Mol. Sci., 2013, 14(8), 15655-15668.
[http://dx.doi.org/10.3390/ijms140815655] [PMID: 23896596]
[146]
El-Mowafy, A.M.; Alkhalaf, M. Resveratrol activates adenylyl-cyclase in human breast cancer cells: a novel, estrogen receptor-independent cytostatic mechanism. Carcinogenesis, 2003, 24(5), 869-873.
[http://dx.doi.org/10.1093/carcin/bgg015] [PMID: 12771030]
[147]
Nie, P.; Hu, W.; Zhang, T.; Yang, Y.; Hou, B.; Zou, Z. Synergistic induction of erlotinib-mediated apoptosis by resveratrol in human non-small-cell lung cancer cells by down-regulating survivin and up-regulating PUMA. Cell. Physiol. Biochem., 2015, 35(6), 2255-2271.
[http://dx.doi.org/10.1159/000374030] [PMID: 25895606]
[148]
Zhu, Y.; He, W.; Gao, X.; Li, B.; Mei, C.; Xu, R.; Chen, H. Resveratrol overcomes gefitinib resistance by increasing the intracellular gefitinib concentration and triggering apoptosis, autophagy and senescence in PC9/G NSCLC cells. Sci. Rep., 2015, 5, 17730.
[http://dx.doi.org/10.1038/srep17730] [PMID: 26635117]
[149]
Wu, X.P.; Xiong, M.; Xu, C.S.; Duan, L.N.; Dong, Y.Q.; Luo, Y.; Niu, T.H.; Lu, C.R. Resveratrol induces apoptosis of human chronic myelogenous leukemia cells in vitro through p38 and JNK-regulated H2AX phosphorylation. Acta Pharmacol. Sin., 2015, 36(3), 353-361.
[http://dx.doi.org/10.1038/aps.2014.132] [PMID: 25619392]
[150]
Abdel-Latif, G.A.; Al-Abd, A.M.; Tadros, M.G.; Al-Abbasi, F.A.; Khalifa, A.E.; Abdel-Naim, A.B. The chemomodulatory effects of resveratrol and didox on herceptin cytotoxicity in breast cancer cell lines. Sci. Rep., 2015, 5, 12054.
[http://dx.doi.org/10.1038/srep12054] [PMID: 26156237]
[151]
Feng, Y-H.; Zhou, W-L.; Wu, Q-L.; Li, X-Y.; Zhao, W-M.; Zou, J-P. Low dose of resveratrol enhanced immune response of mice. Acta Pharmacol. Sin., 2002, 23(10), 893-897.
[PMID: 12370094]
[152]
Trung, L.Q.; An, D.T.T. Is resveratrol a cancer immunomodulatory molecule? Front. Pharmacol., 2018, 9(1255), 1255.
[http://dx.doi.org/10.3389/fphar.2018.01255] [PMID: 30459616]
[153]
Soto, B.L.; Hank, J.A.; Van De Voort, T.J.; Subramanian, L.; Polans, A.S.; Rakhmilevich, A.L.; Yang, R.K.; Seo, S.; Kim, K.; Reisfeld, R.A.; Gillies, S.D.; Sondel, P.M. The anti-tumor effect of resveratrol alone or in combination with immunotherapy in a neuroblastoma model. Cancer Immunol. Immunother., 2011, 60(5), 731-738.
[http://dx.doi.org/10.1007/s00262-011-0971-0] [PMID: 21340652]
[154]
Soto, B.L.; Hank, J.A.; Darjatmoko, S.R.; Polans, A.S.; Yanke, E.M.; Rakhmilevich, A.L.; Seo, S.; Kim, K.; Reisfeld, R.A.; Gillies, S.D.; Sondel, P.M. Anti-tumor and immunomodulatory activity of resveratrol in vitro and its potential for combining with cancer immunotherapy. Int. Immunopharmacol., 2011, 11(11), 1877-1886.
[http://dx.doi.org/10.1016/j.intimp.2011.07.019] [PMID: 21854876]
[155]
Patel, K.R.; Brown, V.A.; Jones, D.J.; Britton, R.G.; Hemingway, D.; Miller, A.S.; West, K.P.; Booth, T.D.; Perloff, M.; Crowell, J.A.; Brenner, D.E.; Steward, W.P.; Gescher, A.J.; Brown, K. Clinical pharmacology of resveratrol and its metabolites in colorectal cancer patients. Cancer Res., 2010, 70(19), 7392-7399.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2027] [PMID: 20841478]
[156]
Howells, L.M.; Berry, D.P.; Elliott, P.J.; Jacobson, E.W.; Hoffmann, E.; Hegarty, B.; Brown, K.; Steward, W.P.; Gescher, A.J. Phase I randomized, double-blind pilot study of micronized resveratrol (SRT501) in patients with hepatic metastases--safety, pharmacokinetics, and pharmacodynamics. Cancer Prev. Res. (Phila.), 2011, 4(9), 1419-1425.
[http://dx.doi.org/10.1158/1940-6207.CAPR-11-0148] [PMID: 21680702]
[157]
Popat, R.; Plesner, T.; Davies, F.; Cook, G.; Cook, M.; Elliott, P.; Jacobson, E.; Gumbleton, T.; Oakervee, H.; Cavenagh, J. A phase 2 study of SRT501 (resveratrol) with bortezomib for patients with relapsed and or refractory multiple myeloma. Br. J. Haematol., 2013, 160(5), 714-717.
[http://dx.doi.org/10.1111/bjh.12154] [PMID: 23205612]
[158]
Paller, C.J.; Rudek, M.A.; Zhou, X.C.; Wagner, W.D.; Hudson, T.S.; Anders, N.; Hammers, H.J.; Dowling, D.; King, S.; Antonarakis, E.S.; Drake, C.G.; Eisenberger, M.A.; Denmeade, S.R.; Rosner, G.L.; Carducci, M.A. A phase I study of muscadine grape skin extract in men with biochemically recurrent prostate cancer: Safety, tolerability, and dose determination. Prostate, 2015, 75(14), 1518-1525.
[http://dx.doi.org/10.1002/pros.23024] [PMID: 26012728]


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 20
ISSUE: 2
Year: 2020
Page: [130 - 145]
Pages: 16
DOI: 10.2174/1568009619666191019143539
Price: $65

Article Metrics

PDF: 15
HTML: 2