Dietary pterostilbene is a novel MTA1-targeted chemopreventive and therapeutic agent in prostate cancer

Oncotarget

Volumn 7, Issue 14, 2016, Pages 18469-18484

  Dhar, Swati ^a   Kumar, Avinash ^a   Zhang, Liangfen ^a,b   Rimando, Agnes M ^c   Lage, Janice M ^b   Lewin, Jack R ^b   Atfi, Azeddine ^a   Zhang, Xu ^a   Levenson, Anait S ^a,b,d  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c NATURAL PRODUCTS UTILIZATION RESEARCH UNIT   (United States)

^d LONG ISLAND UNIVERSITY   (United States)

Author keywords

Chemoprevention; MTA1; Prostate cancer; Pterostilbene; Therapy

Indexed keywords

CALVASCULIN; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BAK; PROTEIN KINASE B; PROTEIN P53; PTEROSTILBENE; HISTONE DEACETYLASE; MTA1 PROTEIN, HUMAN; MTA1 PROTEIN, MOUSE; REPRESSOR PROTEIN; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR;

AGE; AKT GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOWN REGULATION; DRUG DETERMINATION; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOSS; HETEROZYGOTE; HUMAN; HUMAN CELL; MALE; MOUSE; MTA1 GENE; NONHUMAN; ONCOGENE; ONCOGENE C MYC; PROSTATE CANCER; PROTEIN ACETYLATION; PROTEIN EXPRESSION; PROTEIN TARGETING; THERAPY EFFECT; TUMOR SUPPRESSOR GENE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; KNOCKOUT MOUSE; METABOLISM; MOLECULARLY TARGETED THERAPY; PROSTATIC NEOPLASMS; RANDOMIZATION;

ANIMALS; CHEMOPREVENTION; HISTONE DEACETYLASES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR TARGETED THERAPY; PROSTATIC NEOPLASMS; RANDOM ALLOCATION; REPRESSOR PROTEINS; STILBENES; TRANSCRIPTION FACTORS;

EID: 84966275971     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7841     Document Type: Article

References (64)

1. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, Drake CG, Nakai Y, Isaacs WB, Nelson WG. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007; 7:256-269.
2. Nelson WG, Yegnasubramanian S, Agoston AT, Bastian PJ, Lee BH, Nakayama M, De Marzo AM. Abnormal DNA methylation, epigenetics, and prostate cancer. Front Biosci. 2007; 12:4254-4266.
3. Powell IJ, Meyskens FL, Jr. African American men and hereditary/familial prostate cancer: Intermediate-risk populations for chemoprevention trials. Urology. 2001; 57:178-181.
4. Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell. 1998; 2: 851-861.
5. Jang KS, Paik SS, Chung H, Oh YH, Kong G. MTA1 overexpression correlates significantly with tumor grade and angiogenesis in human breast cancers. Cancer Sci. 2006; 97:374-379.
6. Toh Y, Kuwano H, Mori M, Nicolson GL, Sugimachi K. Overexpression of metastasis-associated MTA1 mRNA in invasive oesophageal carcinomas. Br J Cancer. 1999; 79:1723-1726.
7. Sasaki H, Moriyama S, Nakashima Y, Kobayashi Y, Yukiue H, Kaji M, Fukai I, Kiriyama M, Yamakawa Y, Fujii Y. Expression of the MTA1 mRNA in advanced lung cancer. Lung Cancer. 2002; 35:149-154.
8. Hofer MD, Kuefer R, Varambally S, Li H, Ma J, Shapiro GI, Gschwend JE, Hautmann RE, Sanda MG, Giehl K, Menke A, Chinnaiyan AM, Rubin MA. The role of metastasis-associated protein 1 in prostate cancer progression. Cancer Res. 2004; 64:825-829.
9. Kai L, Wang J, Ivanovic M, Chung YT, Laskin WB, Schulze-Hoepfner F, Mirochnik Y, Satcher RL, Jr., Levenson AS. Targeting prostate cancer angiogenesis through metastasisassociated protein 1 (MTA1). Prostate. 2011; 71:268-280.
10. Dias SJ, Zhou X, Ivanovic M, Gailey MP, Dhar S, Zhang L, He Z, Penman AD, Vijayakumar S, Levenson AS. Nuclear MTA1 overexpression is associated with aggressive prostate cancer, recurrence and metastasis in African Americans. Sci Rep. 2013; 3:2331.
11. Levenson AS, Kumar A, Zhang X. MTA family of proteins in prostate cancer: biology, significance, and therapeutic opportunities. Cancer Metastasis Rev. 2014; 33:929-942.
12. Nair SS, Li DQ, Kumar R. A core chromatin remodeling factor instructs global chromatin signaling through multivalent reading of nucleosome codes. Mol Cell. 2013; 49:704-718.
13. Li K, Dias SJ, Rimando AM, Dhar S, Mizuno CS, Penman AD, Lewin JR, Levenson AS. Pterostilbene acts through metastasis-associated protein 1 to inhibit tumor growth, progression and metastasis in prostate cancer. PLoS One. 2013; 8:e57542.
14. Moon HE, Cheon H, Lee MS. Metastasis-associated protein 1 inhibits p53-induced apoptosis. Oncol Rep. 2007; 18:1311-1314.
15. Kai L, Samuel SK, Levenson AS. Resveratrol enhances p53 acetylation and apoptosis in prostate cancer by inhibiting MTA1/NuRD complex. Int J Cancer. 2010; 126:1538-1548.
16. Yoo YG, Kong G, Lee MO. Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1alpha protein by recruiting histone deacetylase 1. EMBO J. 2006; 25:1231-1241.
17. Dhar S, Kumar A, Li K, Tzivion G, Levenson AS. Resveratrol regulates PTEN/Akt pathway through inhibition of MTA1/HDAC unit of the NuRD complex in prostate cancer. Biochim Biophys Acta. 2015; 1853:265-275.
18. Ho E, Beaver LM, Williams DE, Dashwood RH. Dietary factors and epigenetic regulation for prostate cancer prevention. Adv Nutr. 2011; 2:497-510.
19. Azzolini M, La Spina M, Mattarei A, Paradisi C, Zoratti M, Biasutto L. Pharmacokinetics and tissue distribution of pterostilbene in the rat. Mol Nutr Food Res. 2014; 58: 2122-2132.
20. Yeo SC, Ho PC, Lin HS. Pharmacokinetics of pterostilbene in Sprague-Dawley rats: the impacts of aqueous solubility, fasting, dose escalation, and dosing route on bioavailability. Mol Nutr Food Res. 2013; 57:1015-1025.
21. Kapetanovic IM, Muzzio M, Huang Z, Thompson TN, McCormick DL. Pharmacokinetics, oral bioavailability, and metabolic profile of resveratrol and its dimethylether analog, pterostilbene, in rats. Cancer Chemother Pharmacol. 2011; 68:593-601.
22. Dellinger RW, Garcia AM, Meyskens FL, Jr. Differences in the glucuronidation of resveratrol and pterostilbene: altered enzyme specificity and potential gender differences. Drug Metab Pharmacokinet. 2014; 29:112-119.
23. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J, Thomas GV, Li G, Roy-Burman P, Nelson PS, Liu X, Wu H. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell. 2003; 4:209-221.
24. Manavathi B, Kumar R. Metastasis tumor antigens, an emerging family of multifaceted master coregulators. J Biol Chem. 2007; 282:1529-1533.
25. Toh Y, Nicolson GL. The role of the MTA family and their encoded proteins in human cancers: molecular functions and clinical implications. Clin Exp Metastasis. 2009; 26:215-227.
26. Varmus HE. The molecular genetics of cellular oncogenes. Annu Rev Genet. 1984; 18:553-612.
27. Testa JR, Bellacosa A. AKT plays a central role in tumorigenesis. Proc Natl Acad Sci U S A. 2001; 98: 10983-10985.
28. Radtke F, Raj K. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer. 2003; 3:756-767.
29. Dhulipal PD. Ets oncogene family. Indian J Exp Biol. 1997; 35:315-322.
30. Neckers L. Chaperoning oncogenes: Hsp90 as a target of geldanamycin. Handb Exp Pharmacol. 2006; 259-277.
31. Bates S, Peters G. Cyclin D1 as a cellular proto-oncogene. Semin Cancer Biol. 1995; 6:73-82.
32. Pakala SB, Bui-Nguyen TM, Reddy SD, Li DQ, Peng S, Rayala SK, Behringer RR, Kumar R. Regulation of NFkappaB circuitry by a component of the nucleosome remodeling and deacetylase complex controls inflammatory response homeostasis. J Biol Chem. 2010; 285:23590-23597.
33. Bui-Nguyen TM, Pakala SB, Sirigiri RD, Xia W, Hung MC, Sarin SK, Kumar V, Slagle BL, Kumar R. NF-kappaB signaling mediates the induction of MTA1 by hepatitis B virus transactivator protein HBx. Oncogene. 2010; 29:1179-1189.
34. Bohonowych JE, Hance MW, Nolan KD, Defee M, Parsons CH, Isaacs JS. Extracellular Hsp90 mediates an NF-kappaB dependent inflammatory stromal program: implications for the prostate tumor microenvironment. Prostate. 2014; 74:395-407.
35. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 2000; 14:2501-2514.
36. Zhang XY, DeSalle LM, Patel JH, Capobianco AJ, Yu D, Thomas-Tikhonenko A, McMahon SB. Metastasis-associated protein 1 (MTA1) is an essential downstream effector of the c-MYC oncoprotein. Proc Natl Acad Sci U S A. 2005; 102:13968-13973.
37. Zhu W, Cai MY, Tong ZT, Dong SS, Mai SJ, Liao YJ, Bian XW, Lin MC, Kung HF, Zeng YX, Guan XY, Xie D. Overexpression of EIF5A2 promotes colorectal carcinoma cell aggressiveness by upregulating MTA1 through C-myc to induce epithelial-mesenchymaltransition. Gut. 2012; 61:562-575.
38. Powell IJ, Dyson G, Land S, Ruterbusch J, Bock CH, Lenk S, Herawi M, Everson R, Giroux CN, Schwartz AG, Bollig-Fischer A. Genes associated with prostate cancer are differentially expressed in African American and European American men. Cancer Epidemiol Biomarkers Prev. 2013; 22:891-897.
39. Reddy SD, Pakala SB, Molli PR, Sahni N, Karanam NK, Mudvari P, Kumar R. Metastasis-associated protein 1/histone deacetylase 4-nucleosome remodeling and deacetylase complex regulates phosphatase and tensin homolog gene expression and function. J Biol Chem. 2012; 287: 27843-27850.
40. Pakala SB, Singh K, Reddy SD, Ohshiro K, Li DQ, Mishra L, Kumar R. TGF-beta1 signaling targets metastasis-associated protein 1, a new effector in epithelial cells. Oncogene. 2011; 30: 2230-2241.
41. Wong SC, Chan JK, Lee KC, Hsiao WL. Differential expression of p16/p21/p27 and cyclin D1/D3, and their relationships to cell proliferation, apoptosis, and tumour progression in invasive ductal carcinoma of the breast. J Pathol. 2001; 194:35-42.
42. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. p21 is a universal inhibitor of cyclin kinases. Nature. 1993; 366:701-704.
43. Gartel AL, Tyner AL. The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther. 2002; 1:639-649.
44. Nicholson B, Schaefer G, Theodorescu D. Angiogenesis in prostate cancer: biology and therapeutic opportunities. Cancer Metastasis Rev. 2001; 20:297-319.
45. Kinkade CW, Castillo-Martin M, Puzio-Kuter A, Yan J, Foster TH, Gao H, Sun Y, Ouyang X, Gerald WL, Cordon-Cardo C, Abate-Shen C. Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. J Clin Invest. 2008; 118: 3051-3064.
46. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood. 2007; 109:1010-1017.
47. Cao R, Ji H, Feng N, Zhang Y, Yang X, Andersson P, Sun Y, Tritsaris K, Hansen AJ, Dissing S, Cao Y. Collaborative interplay between FGF-2 and VEGF-C promotes lymphangiogenesis and metastasis. Proc Natl Acad Sci U S A. 2012; 109:15894-15899.
48. Sfanos KS, De Marzo AM. Prostate cancer and inflammation: the evidence. Histopathology. 2012; 60:199-215.
49. Kumar A, Lin SY, Dhar S, Rimando AM, Levenson AS. Stilbenes Inhibit Androgen Receptor Expression in 22Rv1 Castrate-resistant Prostate Cancer Cells. Journal of Medicinally Active Plants. 2014; 3:1-8.
50. Jones PA. At the tipping point for epigenetic therapies in cancer. J Clin Invest. 2014; 124:14-16.
51. Ahuja N, Easwaran H, Baylin SB. Harnessing the potential of epigenetic therapy to target solid tumors. J Clin Invest. 2014; 124:56-63.
52. Campbell RM, Tummino PJ. Cancer epigenetics drug discovery and development: the challenge of hitting the mark. J Clin Invest. 2014; 124:64-69.
53. Lin VC, Tsai YC, Lin JN, Fan LL, Pan MH, Ho CT, Wu JY, Way TD. Activation of AMPK by pterostilbene suppresses lipogenesis and cell-cycle progression in p53 positive and negative human prostate cancer cells. J Agric Food Chem. 2012; 60:6399-6407.
54. Chakraborty A, Gupta N, Ghosh K, Roy P. In vitro evaluation of the cytotoxic, anti-proliferative and anti-oxidant properties of pterostilbene isolated from Pterocarpus marsupium. Toxicol In vitro. 2010; 24:1215-1228.
55. Wang TT, Schoene NW, Kim YS, Mizuno CS, Rimando AM. Differential effects of resveratrol and its naturally occurring methylether analogs on cell cycle and apoptosis in human androgen-responsive LNCaP cancer cells. Mol Nutr Food Res. 2010; 54:335-344.
56. Chang J, Rimando A, Pallas M, Camins A, Porquet D, Reeves J, Shukitt-Hale B, Smith MA, Joseph JA, Casadesus G. Low-dose pterostilbene, but not resveratrol, is a potent neuromodulator in aging and Alzheimer's disease. Neurobiol Aging. 2012; 33:2062-2071.
57. Remsberg CM, Yanez JA, Ohgami Y, Vega-Villa KR, Rimando AM, Davies NM. Pharmacometrics of pterostilbene: preclinical pharmacokinetics and metabolism, anticancer, antiinflammatory, antioxidant and analgesic activity. Phytother Res. 2008; 22:169-179.
58. Riche DM, Riche KD, Blackshear CT, McEwen CL, Sherman JJ, Wofford MR, Griswold ME. Pterostilbene on metabolic parameters: a randomized, double-blind, and placebo-controlled trial. Evid Based Complement Alternat Med. 2014; 2014: 459165.
59. Riche DM, McEwen CL, Riche KD, Sherman JJ, Wofford MR, Deschamp D, Griswold M. Analysis of safety from a human clinical trial with pterostilbene. J Toxicol. 2013; 2013: 463595.
60. Joseph JA, Fisher DR, Cheng V, Rimando AM, Shukitt-Hale B. Cellular and behavioral effects of stilbene resveratrol analogues: implications for reducing the deleterious effects of aging. J Agric Food Chem. 2008; 56:10544-10551.
61. Patel KR, Brown VA, Jones DJ, Britton RG, Hemingway D, Miller AS, West KP, Booth TD, Perloff M, Crowell JA, Brenner DE, Steward WP, Gescher AJ, et al. Clinical pharmacology of resveratrol and its metabolites in colorectal cancer patients. Cancer Res. 2010; 70: 7392-7399.
62. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008; 22:659-661.
63. Harrell MI, Iritani BM, Ruddell A. Lymph node mapping in the mouse. J Immunol Methods. 2008; 332:170-174.
64. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods. 2001; 25:402-408.