Procyanidin B2 3,3^″-di-O-gallate, a Biologically Active Constituent of Grape Seed Extract, Induces Apoptosis in Human Prostate Cancer Cells Via Targeting NF-κB, Stat3, and AP1 Transcription Factors

REFERENCES

• Siegel R, Naishadham D, and Jemal A: Cancer statistics, 2012. CA Cancer J Clin 62, 10–29, 2012.
   PubMed Web of Science ®Google Scholar
• Abdulla M and Gruber P: Role of diet modification in cancer prevention. Biofactors 12, 45–51, 2000.
   PubMed Web of Science ®Google Scholar
• Singh RP and Agarwal R: Mechanisms of action of novel agents for prostate cancer chemoprevention. Endocr Relat Cancer 13, 751–778, 2006.
   PubMed Web of Science ®Google Scholar
• Kaur M, Agarwal C, and Agarwal R: Anticancer and cancer chemopreventive potential of grape seed extract and other grape-based products. J Nutr 139, 1806S–1812S, 2009.
   PubMed Web of Science ®Google Scholar
• Agarwal C, Singh RP, and Agarwal R: Grape seed extract induces apoptotic death of human prostate carcinoma DU145 cells via caspases activation accompanied by dissipation of mitochondrial membrane potential and cytochrome c release. Carcinogenesis 23, 1869–1876, 2002.
   PubMed Web of Science ®Google Scholar
• Dhanalakshmi S, Agarwal R, and Agarwal C: Inhibition of NF-kappaB pathway in grape seed extract-induced apoptotic death of human prostate carcinoma DU145 cells. Int J Oncol 23, 721–727, 2003.
   PubMed Web of Science ®Google Scholar
• Kaur M, Agarwal R, and Agarwal C: Grape seed extract induces anoikis and caspase-mediated apoptosis in human prostate carcinoma LNCaP cells: possible role of ataxia telangiectasia mutated-p53 activation. Mol Cancer Ther 5, 1265–1274, 2006.
   PubMed Web of Science ®Google Scholar
• Kaur M, Singh RP, Gu M, Agarwal R, and Agarwal C: Grape seed extract inhibits in vitro and in vivo growth of human colorectal carcinoma cells. Clin Cancer Res 12, 6194–6202, 2006.
   PubMed Web of Science ®Google Scholar
• Raina K, Singh RP, Agarwal R, and Agarwal C: Oral grape seed extract inhibits prostate tumor growth and progression in TRAMP mice. Cancer Res 67, 5976–5982, 2007.
   PubMed Web of Science ®Google Scholar
• Sharma G, Tyagi AK, Singh RP, Chan DC, and Agarwal R: Synergistic anti-cancer effects of grape seed extract and conventional cytotoxic agent doxorubicin against human breast carcinoma cells. Breast Cancer Res Treat 85, 1–12, 2004.
   PubMed Web of Science ®Google Scholar
• Singh RP, Tyagi AK, Dhanalakshmi S, Agarwal R, and Agarwal C: Grape seed extract inhibits advanced human prostate tumor growth and angiogenesis and upregulates insulin-like growth factor binding protein-3. Int J Cancer 108, 733–740, 2004.
   PubMed Web of Science ®Google Scholar
• Song X, Siriwardhana N, Rathore K, Lin D, and Wang HC: Grape seed proanthocyanidin suppression of breast cell carcinogenesis induced by chronic exposure to combined 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and benzo[a]pyrene. Mol Carcinog 49, 450–463, 2010.
   PubMed Web of Science ®Google Scholar
• Tyagi A, Agarwal R, and Agarwal C: Grape seed extract inhibits EGF-induced and constitutively active mitogenic signaling but activates JNK in human prostate carcinoma DU145 cells: possible role in antiproliferation and apoptosis. Oncogene 22, 1302–1316, 2003.
   PubMed Web of Science ®Google Scholar
• Velmurugan B, Singh RP, Agarwal R, and Agarwal C: Dietary-feeding of grape seed extract prevents azoxymethane-induced colonic aberrant crypt foci formation in fischer 344 rats. Mol Carcinog 49, 641–652, 2010.
   PubMed Web of Science ®Google Scholar
• Velmurugan B, Singh RP, Kaul N, Agarwal R, and Agarwal C: Dietary feeding of grape seed extract prevents intestinal tumorigenesis in APCmin/ +mice. Neoplasia 12, 95–102, 2010.
   PubMed Web of Science ®Google Scholar
• Zhao J, Wang J, Chen Y, and Agarwal R: Anti-tumor-promoting activity of a polyphenolic fraction isolated from grape seeds in the mouse skin two-stage initiation-promotion protocol and identification of procyanidin B5–3′-gallate as the most effective antioxidant constituent. Carcinogenesis 20, 1737–1745, 1999.
   PubMed Web of Science ®Google Scholar
• Agarwal C, Veluri R, Kaur M, Chou SC, Thompson JA, et al.: Fractionation of high molecular weight tannins in grape seed extract and identification of procyanidin B2–3,3’-di-O-gallate as a major active constituent causing growth inhibition and apoptotic death of DU145 human prostate carcinoma cells. Carcinogenesis 28, 1478–1484, 2007.
   PubMed Web of Science ®Google Scholar
• Chou SC, Kaur M, Thompson JA, Agarwal R, and Agarwal C: Influence of gallate esterification on the activity of procyanidin B2 in androgen-dependent human prostate carcinoma LNCaP cells. Pharm Res 27, 619–627, 2010.
   PubMed Web of Science ®Google Scholar
• Veluri R, Singh RP, Liu Z, Thompson JA, Agarwal R, et al.: Fractionation of grape seed extract and identification of gallic acid as one of the major active constituents causing growth inhibition and apoptotic death of DU145 human prostate carcinoma cells. Carcinogenesis 27, 1445–1453, 2006.
   PubMed Web of Science ®Google Scholar
• Kaur M, Velmurugan B, Rajamanickam S, Agarwal R, and Agarwal C: Gallic acid, an active constituent of grape seed extract, exhibits anti-proliferative, pro-apoptotic and anti-tumorigenic effects against prostate carcinoma xenograft growth in nude mice. Pharm Res 26, 2133–2140, 2009.
   PubMed Web of Science ®Google Scholar
• Raina K, Rajamanickam S, Deep G, Singh M, Agarwal R, et al.: Chemopreventive effects of oral gallic acid feeding on tumor growth and progression in TRAMP mice. Mol Cancer Ther 7, 1258–1267, 2008.
   PubMed Web of Science ®Google Scholar
• Agarwal R: Cell signaling and regulators of cell cycle as molecular targets for prostate cancer prevention by dietary agents. Biochem Pharmacol 60, 1051–1059, 2000.
   PubMed Web of Science ®Google Scholar
• Goel HL, Li J, Kogan S, and Languino LR: Integrins in prostate cancer progression. Endocr Relat Cancer 15, 657–664, 2008.
   PubMed Web of Science ®Google Scholar
• Vermeulen K, Van Bockstaele DR, and Berneman ZN: The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 36, 131–149, 2003.
   PubMed Web of Science ®Google Scholar
• Gilmore TD: Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25, 6680–6684, 2006.
   PubMed Web of Science ®Google Scholar
• Gu L, Dagvadorj A, Lutz J, Leiby B, Bonuccelli G, et al.: Transcription factor Stat3 stimulates metastatic behavior of human prostate cancer cells in vivo, whereas Stat5b has a preferential role in the promotion of prostate cancer cell viability and tumor growth. Am J Pathol 176, 1959–1972, 2010.
   PubMed Web of Science ®Google Scholar
• Hsu A, Bray TM, and Ho E: Anti-inflammatory activity of soy and tea in prostate cancer prevention. Exp Biol Med (Maywood) 235, 659–667, 2012.
   Web of Science ®Google Scholar
• Ouyang X, Jessen WJ, Al-Ahmadie H, Serio AM, Lin Y, et al.: Activator protein-1 transcription factors are associated with progression and recurrence of prostate cancer. Cancer Res 68, 2132–2144, 2008.
   PubMed Web of Science ®Google Scholar
• Raina K, Agarwal C, and Agarwal R: Effect of silibinin in human colorectal cancer cells: Targeting the activation of NF-kappaB signaling. Mol Carcinog 52, 195–206, 2013.
   PubMed Web of Science ®Google Scholar
• Sun M, Liu C, Nadiminty N, Lou W, Zhu Y, et al.: Inhibition of Stat3 activation by sanguinarine suppresses prostate cancer cell growth and invasion. Prostate 72, 82–89, 2012.
   PubMed Web of Science ®Google Scholar
• Gritsko T, Williams A, Turkson J, Kaneko S, Bowman T, et al.: Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin Cancer Res 12, 11–19, 2006.
   PubMed Web of Science ®Google Scholar
• Wang K, Brems JJ, Gamelli RL, and Holterman AX: Survivin signaling is regulated through nuclear factor-kappa B pathway during glycochenodeoxycholate-induced hepatocyte apoptosis. Biochim Biophys Acta 1803, 1368–1375, 2010.
   PubMed Web of Science ®Google Scholar
• Rodel F, Sprenger T, Kaina B, Liersch T, Rodel C, et al.: Survivin as a prognostic/predictive marker and molecular target in cancer therapy. Curr Med Chem 19, 3679–3688, 2012.
   PubMed Web of Science ®Google Scholar
• Rubio N, Garcia-Segura LM, and Arevalo MA: Survivin prevents apoptosis by binding to caspase-3 in astrocytes infected with the BeAn strain of Theiler's murine encephalomyelitis virus. J Neurovirol 18, 354–363, 2012.
   PubMed Web of Science ®Google Scholar
• Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, et al.: An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 40, 1117–1123, 2001.
   PubMed Web of Science ®Google Scholar
• Nomura T, Yamasaki M, Nomura Y, and Mimata H: Expression of the inhibitors of apoptosis proteins in cisplatin-resistant prostate cancer cells. Oncol Rep 14, 993–997, 2005.
   PubMed Web of Science ®Google Scholar
• Saito A, Emoto M, Tanaka A, Doi Y, Shoji K, et al.: Stereoselective synthesis of procyanidin B3–3-O-gallate and 3,3′′;-di-O-gallate, and their abilities as antioxidant and DNA polymerase inhibitor. Tetrahedron 60, 12043–12049, 2004.
   Web of Science ®Google Scholar
• Saito A, Nakajima N, Tanaka A, and Ubukata M: Synthetic studies of proanthocyanidins. Part 2: Stereoselective gram-scale synthesis of procyanidin-B3. Tetrahedron 58, 7829–7837, 2002.
   Web of Science ®Google Scholar
• Tüeckmantel W, Kozikowski AP, and Romanczyk LJJ: Studies in Polyphenol chemistry and bioactivity: 1. Preparation of Building blocks from (+)-catechin. procyanidin formation; synthesis of the cancer cell growth inhibitor, 3-o-galloyl-(2R,3R)-epicatechin-4b,8-[3-O-galloyl-(2R,3R)-epicatechin]. Journal of the American Chemical Society 121, 12073–12081, 1999.
   Web of Science ®Google Scholar
• Saito A, Mizushina Y, Ikawa H, Yoshida H, Doi Y, et al.: Systematic synthesis of galloyl-substituted procyanidin B1 and B2, and their ability of DPPH radical scavenging activity and inhibitory activity of DNA polymerases. Bioorganic & Medicinal Chemistry 13, 2759–2771, 2005.
   PubMed Web of Science ®Google Scholar
• Viton F, Landreau C, Rustidge D, Robert F, Williamson G, et al.: First Total synthesis of 14c-labeled procyanidin b2: a milestone toward understanding cocoa polyphenol metabolism. Eur J Org Chem 36, 6069–6078, 2008.
   Web of Science ®Google Scholar
• Tyagi A, Agarwal C, Dwyer-Nield LD, Singh RP, Malkinson AM, et al.: Silibinin modulates TNF-alpha and IFN-gamma mediated signaling to regulate COX2 and iNOS expression in tumorigenic mouse lung epithelial LM2 cells. Mol Carcinog 51, 832–842, 2012.
   PubMed Web of Science ®Google Scholar
• Agarwal C, Tyagi A, Kaur M, and Agarwal R: Silibinin inhibits constitutive activation of Stat3, and causes caspase activation and apoptotic death of human prostate carcinoma DU145 cells. Carcinogenesis 28, 1463–1470, 2007.
   PubMed Web of Science ®Google Scholar
• Brand TC, Canby-Hagino ED, Pratap Kumar A, Ghosh R, Leach RJ, et al.: Chemoprevention of prostate cancer. Hematol Oncol Clin North Am 20, 831–843, 2006.
   PubMed Web of Science ®Google Scholar
• Klein EA: Chemoprevention of prostate cancer. Annu Rev Med 57, 49–63, 2006.
   PubMed Web of Science ®Google Scholar
• Bhatt RS, and Bubley GJ: The challenge of herbal therapies for prostate cancer. Clin Cancer Res 14, 7581–7582, 2008.
   PubMed Web of Science ®Google Scholar
• Shrestha SP, Thompson JA, Wempe MF, Gu M, Agarwal R, et al.: Glucuronidation and methylation of procyanidin dimers b2 and 3,3′′;-di-o-galloyl-b2 and corresponding monomers epicatechin and 3-o-galloyl-epicatechin in mouse liver. Pharm Res 29, 856–865, 2012.
   PubMed Web of Science ®Google Scholar
• Sfanos KS and De Marzo AM: Prostate cancer and inflammation: the evidence. Histopathology 60, 199–215, 2012.
   PubMed Web of Science ®Google Scholar
• De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, et al.: Inflammation in prostate carcinogenesis. Nat Rev Cancer 7, 256–269, 2007.
   PubMed Web of Science ®Google Scholar
• James ND, Sydes MR, Mason MD, Clarke NW, Anderson J, et al.: Celecoxib plus hormone therapy versus hormone therapy alone for hormone-sensitive prostate cancer: first results from the STAMPEDE multiarm, multistage, randomised controlled trial. Lancet Oncol 13, 549–558, 2012.
   PubMed Web of Science ®Google Scholar
• Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, et al.: Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann N Y Acad Sci 1171, 59–76, 2009.
   PubMed Web of Science ®Google Scholar
• Ambrosini G, Adida C, and Altieri DC: A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3, 917–921, 1997.
   PubMed Web of Science ®Google Scholar
• Reed JC: The Survivin saga goes in vivo. J Clin Invest 108, 965–969, 2001.
   PubMed Web of Science ®Google Scholar
• Miyachi K, Sasaki K, Onodera S, Taguchi T, Nagamachi M, et al.: Correlation between survivin mRNA expression and lymph node metastasis in gastric cancer. Gastric Cancer 6, 217–224, 2003.
   PubMedGoogle Scholar
• Paydas S, Tanriverdi K, Yavuz S, Disel U, Sahin B, et al.: Survivin and aven: two distinct antiapoptotic signals in acute leukemias. Ann Oncol 14, 1045–1050, 2003.
   PubMed Web of Science ®Google Scholar