Resveratrol and cancer: Challenges for clinical translation

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 6, 2015, Pages 1178-1185

  Singh, Chandra K ^a   Ndiaye, Mary A ^a   Ahmad, Nihal ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cancer; Clinical trial; Resveratrol

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; CASPASE 3; CYCLOOXYGENASE 1; PROSTAGLANDIN E2; RESVERATROL; STILBENE DERIVATIVE;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; BREAST CANCER; CANCER RISK; CANCER TISSUE; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CLINICAL TRIAL (TOPIC); COLON CANCER; COLORECTAL CANCER; CONTROLLED CLINICAL TRIAL (TOPIC); DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG EFFICACY; DRUG GLUCURONIDATION; DRUG INDUSTRY; DRUG SAFETY; DRUG SULFATION; HUMAN; IMMUNOREACTIVITY; INTESTINE FLORA; MONOAMINERGIC SYSTEM; NEOPLASM; PRIORITY JOURNAL; QUALITY CONTROL; REVIEW; STUDY; SUSTAINED DRUG RELEASE; TARGET ORGAN; WNT SIGNALING PATHWAY; ANIMAL; METABOLISM; NEOPLASMS; TRANSLATIONAL RESEARCH;

VITACEAE;

ANIMALS; ANTINEOPLASTIC AGENTS; CLINICAL TRIALS AS TOPIC; HUMANS; NEOPLASMS; STILBENES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84925680106     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.11.004     Document Type: Review

References (58)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
2. Siegel R., Ma J., Zou Z., Jemal A. Cancer statistics, 2014. CA Cancer J. Clin. 2014, 64:9-29.
3. La Vecchia C., Bosetti C. Diet and cancer risk in Mediterranean countries: open issues. Public Health Nutr. 2006, 9:1077-1082.
4. Zheng J., Yang B., Huang T., Yu Y., Yang J., Li D. Green tea and black tea consumption and prostate cancer risk: an exploratory meta-analysis of observational studies. Nutr. Cancer 2011, 63:663-672.
5. Vang O., Ahmad N., Baile C.A., Baur J.A., Brown K., Csiszar A., Das D.K., Delmas D., Gottfried C., Lin H.Y., Ma Q.Y., Mukhopadhyay P., Nalini N., Pezzuto J.M., Richard T., Shukla Y., Surh Y.J., Szekeres T., Szkudelski T., Walle T., Wu J.M. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 2011, 6:e19881.
6. Singh N., Agrawal M., Dore S. Neuroprotective properties and mechanisms of resveratrol in in vitro and in vivo experimental cerebral stroke models. ACS Chem. Neurosci. 2013, 4:1151-1162.
7. Timmers S., Konings E., Bilet L., Houtkooper R.H., van de Weijer T., Goossens G.H., Hoeks J., van der Krieken S., Ryu D., Kersten S., Moonen-Kornips E., Hesselink M.K., Kunz I., Schrauwen-Hinderling V.B., Blaak E.E., Auwerx J., Schrauwen P. Calorie restriction-like effects of 30days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab. 2011, 14:612-622.
8. Lam Y.Y., Peterson C.M., Ravussin E. Resveratrol vs. calorie restriction: data from rodents to humans. Exp. Gerontol. 2013, 48:1018-1024.
9. Dolinsky V.W., Dyck J.R. Calorie restriction and resveratrol in cardiovascular health and disease. Biochim. Biophys. Acta 2011, 1812:1477-1489.
10. 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, 275:218-220.
11. Aluyen J.K., Ton Q.N., Tran T., Yang A.E., Gottlieb H.B., Bellanger R.A. Resveratrol: potential as anticancer agent. J. Diet. Suppl. 2012, 9:45-56.
12. Francioso A., Mastromarino P., Masci A., d'Erme M., Mosca L. Chemistry, stability and bioavailability of resveratrol. Med. Chem. 2014, 10:237-245.
13. Walle T. Bioavailability of resveratrol. Ann. N. Y. Acad. Sci. 2011, 1215:9-15.
14. Singh C.K., George J., Ahmad N. Resveratrol-based combinatorial strategies for cancer management. Ann. N. Y. Acad. Sci. 2013, 1290:113-121.
15. Singh C.K., Pitschmann A., Ahmad N. Resveratrol-zinc combination for prostate cancer management. Cell Cycle 2014, 13:1867-1874.
16. Patel K.R., Scott E., Brown V.A., Gescher A.J., Steward W.P., Brown K. Clinical trials of resveratrol. Ann. N. Y. Acad. Sci. 2011, 1215:161-169.
17. Borriello A., Bencivenga D., Caldarelli I., Tramontano A., Borgia A., Zappia V., Della Ragione F. Resveratrol: from basic studies to bedside. Cancer Treat. Res. 2014, 159:167-184.
18. Tome-Carneiro J., Larrosa M., Gonzalez-Sarrias A., Tomas-Barberan F.A., Garcia-Conesa M.T., Espin J.C. Resveratrol and clinical trials: the crossroad from in vitro studies to human evidence. Curr. Pharm. Des. 2013, 19:6064-6093.
19. 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, 16:1246-1252.
20. Bode L.M., Bunzel D., Huch M., Cho G.S., Ruhland D., Bunzel M., Bub A., Franz C.M., Kulling S.E. In vivo and in vitro metabolism of trans-resveratrol by human gut microbiota. Am. J. Clin. Nutr. 2013, 97:295-309.
21. Almeida L., Vaz-da-Silva M., Falcao A., Soares E., Costa R., Loureiro A.I., Fernandes-Lopes C., Rocha J.F., Nunes T., Wright L., Soares-da-Silva P. Pharmacokinetic and safety profile of trans-resveratrol in a rising multiple-dose study in healthy volunteers. Mol. Nutr. Food Res. 2009, 53(Suppl. 1):S7-S15.
22. Ndiaye M., Kumar R., Ahmad N. Resveratrol in cancer management: where are we and where we go from here?. Ann. N. Y. Acad. Sci. 2011, 1215:144-149.
23. Johnson J.J., Nihal M., Siddiqui I.A., Scarlett C.O., Bailey H.H., Mukhtar H., Ahmad N. Enhancing the bioavailability of resveratrol by combining it with piperine. Mol. Nutr. Food Res. 2011, 55:1169-1176.
24. Huang W., Chen Z., Wang Q., Lin M., Wu S., Yan Q., Wu F., Yu X., Xie X., Li G., Xu Y., Pan J. Piperine potentiates the antidepressant-like effect of trans-resveratrol: involvement of monoaminergic system. Metab. Brain Dis. 2013, 28:585-595.
25. Wightman E.L., Reay J.L., Haskell C.F., Williamson G., Dew T.P., Kennedy D.O. Effects of resveratrol alone or in combination with piperine on cerebral blood flow parameters and cognitive performance in human subjects: a randomised, double-blind, placebo-controlled, cross-over investigation. Br. J. Nutr. 2014, 112:203-213.
26. Basu N.K., Kole L., Basu M., McDonagh A.F., Owens I.S. Targeted inhibition of glucuronidation markedly improves drug efficacy in mice - a model. Biochem. Biophys. Res. Commun. 2007, 360:7-13.
27. Malhotra A., Nair P., Dhawan D.K. Study to evaluate molecular mechanics behind synergistic chemo-preventive effects of curcumin and resveratrol during lung carcinogenesis. PLoS One 2014, 9:e93820.
28. De Santi C., Pietrabissa A., Spisni R., Mosca F., Pacifici G.M. Sulphation of resveratrol, a natural compound present in wine, and its inhibition by natural flavonoids. Xenobiotica 2000, 30:857-866.
29. McAnulty L.S., Miller L.E., Hosick P.A., Utter A.C., Quindry J.C., McAnulty S.R. Effect of resveratrol and quercetin supplementation on redox status and inflammation after exercise. Appl. Physiol. Nutr. Metab. 2013, 38:760-765.
30. Hoshino J., Park E.J., Kondratyuk T.P., Marler L., Pezzuto J.M., van Breemen R.B., Mo S., Li Y., Cushman M. Selective synthesis and biological evaluation of sulfate-conjugated resveratrol metabolites. J. Med. Chem. 2010, 53:5033-5043.
31. Patel K.R., Andreadi C., Britton R.G., Horner-Glister E., Karmokar A., Sale S., Brown V.A., Brenner D.E., Singh R., Steward W.P., Gescher A.J., Brown K. Sulfate metabolites provide an intracellular pool for resveratrol generation and induce autophagy with senescence. Sci. Transl. Med. 2013, 5:205ra133.
32. Andreadi C., Britton R.G., Patel K.R., Brown K. Resveratrol-sulfates provide an intracellular reservoir for generation of parent resveratrol, which induces autophagy in cancer cells. Autophagy 2014, 10:524-525.
33. Pezzuto J.M., Kondratyuk T.P., Ogas T. Resveratrol derivatives: a patent review (2009-2012). Expert Opin. Ther. Pat. 2013, 23:1529-1546.
34. Tříska J., Houška M. Physical methods of resveratrol induction in grapes and grape products - a review. Czech J. Food Sci. 2012, 30:489-502.
35. Larrosa M., Tome-Carneiro J., Yanez-Gascon M.J., Alcantara D., Selma M.V., Beltran D., Garcia-Conesa M.T., Urban C., Lucas R., Tomas-Barberan F., Morales J.C., Espin J.C. Preventive oral treatment with resveratrol pro-prodrugs drastically reduce colon inflammation in rodents. J. Med. Chem. 2010, 53:7365-7376.
36. Abderrezak A., Bourassa P., Mandeville J.S., Sedaghat-Herati R., Tajmir-Riahi H.A. Dendrimers bind antioxidant polyphenols and cisplatin drug. PLoS One 2012, 7:e33102.
37. Svenson S., Chauhan A.S. Dendrimers for enhanced drug solubilization. Nanomedicine (Lond.) 2008, 3:679-702.
38. Williams L.D., Burdock G.A., Edwards J.A., Beck M., Bausch J. Safety studies conducted on high-purity trans-resveratrol in experimental animals. Food Chem. Toxicol. 2009, 47:2170-2182.
39. van Ginkel P.R., Sareen D., Subramanian L., Walker Q., Darjatmoko S.R., Lindstrom M.J., Kulkarni A., Albert D.M., Polans A.S. Resveratrol inhibits tumor growth of human neuroblastoma and mediates apoptosis by directly targeting mitochondria. Clin. Cancer Res. 2007, 13:5162-5169.
40. Mukherjee S., Dudley J.I., Das D.K. Dose-dependency of resveratrol in providing health benefits. Dose Response 2010, 8:478-500.
41. Chachay V.S., Kirkpatrick C.M., Hickman I.J., Ferguson M., Prins J.B., Martin J.H. Resveratrol-pills to replace a healthy diet?. Br. J. Clin. Pharmacol. 2011, 72:27-38.
42. Brown V.A., Patel K.R., Viskaduraki M., Crowell J.A., Perloff M., Booth T.D., Vasilinin G., Sen A., Schinas A.M., Piccirilli G., Brown K., Steward W.P., Gescher A.J., Brenner D.E. Repeat dose study of the cancer chemopreventive agent resveratrol in healthy volunteers: safety, pharmacokinetics, and effect on the insulin-like growth factor axis. Cancer Res. 2010, 70:9003-9011.
43. Tome-Carneiro J., Gonzalvez M., Larrosa M., Yanez-Gascon M.J., Garcia-Almagro F.J., Ruiz-Ros J.A., Tomas-Barberan F.A., Garcia-Conesa M.T., Espin J.C. Grape resveratrol increases serum adiponectin and downregulates inflammatory genes in peripheral blood mononuclear cells: a triple-blind, placebo-controlled, one-year clinical trial in patients with stable coronary artery disease. Cardiovasc. Drugs Ther. 2013, 27:37-48.
44. 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, 160:714-717.
45. Youn H.S., Lee J.Y., Fitzgerald K.A., Young H.A., Akira S., Hwang D.H. Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: molecular targets are TBK1 and RIP1 in TRIF complex. J. Immunol. 2005, 175:3339-3346.
46. Nwachukwu J.C., Srinivasan S., Bruno N.E., Parent A.A., Hughes T.S., Pollock J.A., Gjyshi O., Cavett V., Nowak J., Garcia-Ordonez R.D., Houtman R., Griffin P.R., Kojetin D.J., Katzenellenbogen J.A., Conkright M.D., Nettles K.W. Resveratrol modulates the inflammatory response via an estrogen receptor-signal integration network. Elife 2014, 3:e02057.
47. Pandey P.R., Okuda H., Watabe M., Pai S.K., Liu W., Kobayashi A., Xing F., Fukuda K., Hirota S., Sugai T., Wakabayashi G., Koeda K., Kashiwaba M., Suzuki K., Chiba T., Endo M., Fujioka T., Tanji S., Mo Y.Y., Cao D., Wilber A.C., Watabe K. Resveratrol suppresses growth of cancer stem-like cells by inhibiting fatty acid synthase. Breast Cancer Res. Treat. 2011, 130:387-398.
48. Calamini B., Ratia K., Malkowski M.G., Cuendet M., Pezzuto J.M., Santarsiero B.D., Mesecar A.D. Pleiotropic mechanisms facilitated by resveratrol and its metabolites. Biochem. J. 2010, 429:273-282.
49. Zykova T.A., Zhu F., Zhai X., Ma W.Y., Ermakova S.P., Lee K.W., Bode A.M., Dong Z. Resveratrol directly targets COX-2 to inhibit carcinogenesis. Mol. Carcinog. 2008, 47:797-805.
50. 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, 4:1419-1425.
51. Nguyen A.V., Martinez M., Stamos M.J., Moyer M.P., Planutis K., Hope C., Holcombe R.F. Results of a phase I pilot clinical trial examining the effect of plant-derived resveratrol and grape powder on Wnt pathway target gene expression in colonic mucosa and colon cancer. Cancer Manag. Res. 2009, 1:25-37.
52. 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, 70:7392-7399.
53. Zhu W., Qin W., Zhang K., Rottinghaus G.E., Chen Y.C., Kliethermes B., Sauter E.R. Trans-resveratrol alters mammary promoter hypermethylation in women at increased risk for breast cancer. Nutr. Cancer 2012, 64:393-400.
54. Zhu W., Qin W., Hewett J.E., Sauter E.R. Quantitative evaluation of DNA hypermethylation in malignant and benign breast tissue and fluids. Int. J. Cancer 2010, 126:474-482.
55. Masferrer J.L., Leahy K.M., Koki A.T., Zweifel B.S., Settle S.L., Woerner B.M., Edwards D.A., Flickinger A.G., Moore R.J., Seibert K. Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res. 2000, 60:1306-1311.
56. Jogie-Brahim S., Feldman D., Oh Y. Unraveling insulin-like growth factor binding protein-3 actions in human disease. Endocr. Rev. 2009, 30:417-437.
57. Shan L., Aster J.C., Sklar J., Sunday M.E. Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L500-L509.
58. Kunnimalaiyaan M., Chen H. Tumor suppressor role of Notch-1 signaling in neuroendocrine tumors. Oncologist 2007, 12:535-542.