Suppression of the Inflammatory Cascade is Implicated in Resveratrol Chemoprevention of Experimental Hepatocarcinogenesis (original) (raw)

• Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–105.
  Article PubMed Google Scholar
• Sherman M. Hepatocellular carcinoma: epidemiology, risk factors, and screening. Semin Liver Dis. 2005;25:143–54.
  Article PubMed Google Scholar
• El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology. 2004;127:S27–34.
  Article PubMed Google Scholar
• American Cancer Society. Cancer Facts and Figures 2009. Atlanta, GA, 2009.
• Wu L, Tang Z-Y, Li Y. Experimental models of hepatocellular carcinoma: developments and evolution. J Cancer Res Clin Oncol. 2009;135:969–81.
  Article PubMed Google Scholar
• Schütte K, Bornschein J, Malfertheiner P. Hepatocellular carcinoma—epidemiological trends and risk factors. Dig Dis. 2009;27:80–92.
  PubMed Google Scholar
• Bartsch H, Montesano R. Relevance of nitrosamines to human cancer. Carcinogenesis. 1984;5:1381–93.
  Article PubMed CAS Google Scholar
• Kensler TW, Egner PA, Wang JB, Zhu YR, Zhang BC, Lu PX et al. Chemoprevention of hepatocellular carcinoma in aflatoxin endemic areas. Gastroenterology. 2004;127:S310–8.
  Article PubMed CAS Google Scholar
• Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003;362:1907–17.
  Article PubMed Google Scholar
• Je Y, Schutz FAB, Choueiri TK. Risk of bleeding with vascular endothelial growth factor receptor tyrosine-kinase inhibitors sunitinib and sorafenib: a systematic review and mata-analysis of clinical trials. Lancet Oncol. 2009;10:967–74.
  Article PubMed CAS Google Scholar
• Okuno M, Kojima S, Moriwaki H. Chemoprevention of hepatocellular carcinoma: concept, progress and perspectives. J Gastroenterol Hepatol. 2001;16:1329–35.
  Article PubMed CAS Google Scholar
• Yates MS, Kensler TW. Keap1 eye on the target: chemoprevention of liver cancer. Acta Pharmacol Sin. 2007;28:1331–42.
  Article PubMed CAS Google Scholar
• Berasain C, Casillo J, Perugorria MJ, Latasa MU, Prieto J, Avila MA. Inflammation and liver cancer: new molecular links. Ann NY Acad Sci. 2009;1155:206–21.
  Article PubMed CAS Google Scholar
• Joo M, Chi JG, Hyucksang L. Expressions of HSP70 and HSP27 in hepatocellular carcinoma. J Korean Med Sci. 2005;20:829–34.
  Article PubMed CAS Google Scholar
• Murakami A, Ashida H, Terao J. Multitargeted cancer prevention by quercetin. Cancer Lett. 2008;269:315–25.
  Article PubMed CAS Google Scholar
• Wu T. Cyclooxygenase-2 in hepatocellular carcinoma. Cancer Treat Rev. 2006;32:28–44.
  Article PubMed CAS Google Scholar
• Giannitrapani L, Ingrao S, Soresi M, Maria Florena A, La Spada E, Sandonato L et al. Cyclooxygenase-2 expression in chronic liver diseases and hepatocellular carcinoma. Ann NY Acad Sci. 2009;1155:293–9.
  Article PubMed CAS Google Scholar
• Yildirim Y, Ozyilkan O, Bilezikci B, Akcali Z, Haberal M. Lack of influence of cyclooxygenase-2 expression in hepatocellular carcinomas on patient survival. Asian Pac J Cancer Prev. 2008;9:295–8.
  PubMed Google Scholar
• Karin M. The IκB kinase-a bridge between inflammation and cancer. Cell Res. 2008;18:334–432.
  Article PubMed CAS Google Scholar
• Muriel P. NF-κB in liver diseases: a target for drug therapy. J Appl Toxicol. 2009;29:91–100.
  Article PubMed CAS Google Scholar
• Elsharkawy AM, Mann DA. Nuclear factor-κB and the hepatic inflammation-fibrosis-cancer axis. Hepatology. 2007;46:590–7.
  Article PubMed CAS Google Scholar
• Aggarwal BB, Vijayalekshmi RV, Sung B. Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res. 2009;15:425–30.
  Article PubMed CAS Google Scholar
• Aggarwal BB, Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol. 2006;71:1397–421.
  Article PubMed CAS Google Scholar
• Naithani R, Huma LC, Moriarty RM, McCormick DL, Mehta RG. Comprehensive review of cancer chemopreventive agents evaluated in experimental carcinogenesis models and clinical trials. Curr Med Chem. 2008;15:1044–71.
  Article PubMed CAS Google Scholar
• Rahman I, Biswas SK, Kirkham PA. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol. 2005;72:1439–52.
  Article CAS Google Scholar
• Kim YS, Young MR, Bobe G, Colbum NH, Milner JA. Bioactive food components, inflammatory targets, and cancer prevention. Cancer Prev Res. 2009;2:200–8.
  Article Google Scholar
• Mann CD, Neal CP, Garcea G, Manson MM, Dennison AR, Berry DP. Phytochemicals as potential chemopreventive and chemotherapeutic agents in hepatocarcinogenesis. Eur J Cancer Prev. 2009;18:13–25.
  Article PubMed CAS Google Scholar
• Vidavalur R, Otani H, Singal PK, Maulik N. Significance of wine and resveratrol in cardiovascular disease: French paradox revisited. Exp Clin Cardiol. 2006;11:217–25.
  PubMed CAS Google Scholar
• Shakibaei M, Harikumar KB, Aggarwal BB. Resveratrol addiction: to die or not to die. Mol Nutr Food Res. 2009;53:115–28.
  Article PubMed CAS Google Scholar
• Athar M, Back JH, Kopelovich L, Bickers DR, Kim AL. Multiple molecular targets of resveratrol: anti-carcinogenic mechanisms. Arch Biochem Biophys. 2009;486:95–102.
  Article PubMed CAS Google Scholar
• Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S, Takada Y. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res. 2004;24:2783–840.
  PubMed CAS Google Scholar
• Kundu JK, Surh Y-J. Cancer chemopreventive and therapeutic potential of resveratrol: mechanistic perspectives. Cancer Lett. 2008;269:243–61.
  Article PubMed CAS Google Scholar
• Bishayee A. Cancer prevention and treatment with resveratrol: from rodent studies to clinical trials. Cancer Prev Res. 2009;2:409–18.
  Article Google Scholar
• Bishayee A, Politis T, Darvesh AS. Resveratrol in the chemoprevention and treatment of hepatocellular carcinoma. Cancer Treat Rev. 2010;36:43–53.
  Article PubMed CAS Google Scholar
• Bishayee A, Dhir N. Resveratrol-mediated chemoprevention of diethylnitrosamine-initiated hepatocarcinogenesis: inhibition of cell proliferation and induction of apoptosis. Chem-Biol Interact. 2009;179:131–44.
  Article PubMed CAS Google Scholar
• Farber E, Sarma DS. Hepatocarcinogenesis: a dynamic cellular perspective. Lab Invest. 1987;56:4–22.
  PubMed CAS Google Scholar
• Das S, Das DK. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Target. 2007;6:168–73.
  Article CAS Google Scholar
• Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acid Res. 1983;11:1475–89.
  Article PubMed CAS Google Scholar
• Morimoto RI. Cells in stress: transcriptional activation of heat shock genes. Science. 1993;259:1409–10.
  Article PubMed CAS Google Scholar
• Jolly C, Morimoto RI. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst. 2000;92:1564–72.
  Article PubMed CAS Google Scholar
• Lim SO, Park SG, Yoo J-H, Park YM, Kim H-J, Jang K-T et al. Expression of heat shock proteins (HSP27, HSP60, HSP70, HSP90, GRP78, GRP94) in hepatitis B virus-related hepatocellular carcinomas and dysplastic nodules. World J Gastroenterol. 2005;11:2072–9.
  PubMed CAS Google Scholar
• Yoshida S, Hazama S, Tokuno K, Sakamoto K, Takashima M, Tamesa T et al. Concomitant overexpression of heat-shock protein 70 and HLA class-I in hepatitis C virus-related hepatocellular carcinoma. Anticancer Res. 2009;29:539–44.
  PubMed Google Scholar
• Chuma M, Sakamoto M, Yamazaki K, Ohta T, Ohki M, Hirohashi S. Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology. 2003;37:198–207.
  Article PubMed CAS Google Scholar
• Carr BI, Huang TH, Buzin CH, Itakura K. Induction of heat shock gene expression without heat shock by hepatocarcinogenesis. Cancer Res. 1986;46:5106–11.
  PubMed CAS Google Scholar
• Tacchini L, Schiaffonati L, Rappocciolo E, Cairo G, Bernelli-Zazzera A. Expression pattern of the genes for the different members of the heat-shock protein 70 family, ornithine decarboxylase, and c-Ha-ras during the early stages of hepatocarcinogenesis. Mol Carcinog. 1989;2:233–6.
  Article PubMed CAS Google Scholar
• Takami T, Kaposi-Novak P, Uchida K, Gomez-Quiroz LE, Conner EA, Factor VM et al. Loss of hepatocyte growth factor/c-Met signaling pathway accelerates early stages of _N_–nitrosodiethylamine-induced hepatocarcinogenesis. Cancer Res. 2007;67:9844–51.
  Article PubMed CAS Google Scholar
• Cardile V, Scifo C, Russo A, Falsaperla M, Morgia G, Motta M et al. Involvement of HSP70 in resveratrol-induced apoptosis of human prostate cancer. Anticancer Res. 2003;23:4921–6.
  PubMed CAS Google Scholar
• Chakraborty PK, Mustafi SB, Ganguly S, Chatterjee M, Raha S. Resveratrol induces apoptosis in K562 (chronic myelogenous leukemia) cells by targeting a key survival protein, heat shock protein 70. Cancer Sci. 2008;99:1109–16.
  Article PubMed CAS Google Scholar
• Sengottuvelan M, Deeptha K, Nalini N. Influences of dietary resveratrol on early and late molecular markers of 1, 2-dimethylhydrazine-induced colon carcinogenesis. Nutrition. 2009;25:1169–76.
  Article PubMed CAS Google Scholar
• Hla T, Nielson K. Human cyclooxygenase-2 cDNA. Proc Natl Acad Sci USA. 1992;89:7384–8.
  Article PubMed CAS Google Scholar
• Fosselin E. Biochemistry of cyclooxygenase (COX)-2 inhibitors and molecular pathology of COX-2 in neoplasia. Crit Rev Clin Lab Sci. 2000;37:431–502.
  Article Google Scholar
• Prescott SM, Fitzpatrick FA. Cyclooxygenase-2 and carcinogenesis. Biochim Biophys Acta. 2000;1470:M69–78.
  PubMed CAS Google Scholar
• Koga H, Sakisaka S, Ohishi M, Kawaguchi T, Taniguchi E, Sasatomi K et al. Expression of cyclooxygenase-2 in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Hepatology. 1999;29:688–96.
  Article PubMed CAS Google Scholar
• Sung YK, Hwang SY, Kim JO, Bae HI, Kim JC, Kim MK. The correlation between cyclooxygenase-2 expression and hepatocellular carcinogenesis. Mol Cells. 2004;17:35–8.
  PubMed CAS Google Scholar
• Hu KQ. Rationale and feasibility of chemoprevention of hepatocellular carcinoma by cyclooxygenase-2 inhibitors. J Lab Clin Med. 2002;139:234–43.
  Article PubMed CAS Google Scholar
• Koga H. Hepatocellular carcinoma: is there a potential for chemoprevention using cyclooxygenase-2 inhibitors? Cancer. 2003;98:661–7.
  Article PubMed CAS Google Scholar
• Ramakrishnan G, Elinos-Báez CM, Jagan S, Augustine TA, Kamaraj S, Anandakumar P et al. Silymarin downregulates COX-2 expression and attenuates hyperlipidemia during NDEA-induced rat hepatocellular carcinoma. Mol Cell Biochem. 2008;313:53–61.
  Article PubMed CAS Google Scholar
• Sivaramakrishnan V, Niranjali Devaraj S. Morin regulates the expression of NF-kappaB-p65, COX-2 and matrix metalloproteinases in diethylnitrosamine induced rat hepatocellular carcinoma. Chem-Biol Interact. 2009;180:353–9.
  Article PubMed CAS Google Scholar
• Bishayee A, Barnes KF, Bhatia D, Darvesh AS, Carroll RT. Resveratrol suppresses oxidative stress and inflammatory response in diethylnitrosamine-initiated rat hepatocarcinogenesis. Cancer Prev Res. 2010;in press.
• Khanduja KL, Bhardwai A, Kaushik G. Resveratrol inhibits N-nitrosodiethylamine-induced ornithine decarboxylase and cyclooxygenase in mice. J Nutr Sci Vitaminol. 2004;50:61–5.
  PubMed CAS Google Scholar
• Tsujii M, DuBois RN. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell. 1995;83:493–501.
  Article PubMed CAS Google Scholar
• Zycova TA, Zhu F, Zhai X, Ma W-Y, Ermakova SP, Lee KW et al. Resveratrol directly targets COX-2 to inhibit carcinogenesis. Mol Carcinog. 2008;47:797–805.
  Article CAS Google Scholar
• Cervello M, Montalto G. Cyclooxygenase in hepatocellular carcinoma. World J Gastroenterol. 2006;12:5113–21.
  PubMed CAS Google Scholar
• Luther DJ, Ohanyan V, Shamhart PE, Hodnichak CM, Sisakian H, Booth TD, et al. Chemopreventive doses of resveratrol do not affect cardiac function in a rodent model of hepatocellular carcinoma. Invest New Drugs. 2010; in press. doi: 10.1007/s10637-009-9332-7.
• Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221–7.
  Article PubMed CAS Google Scholar
• Rahman MA, Dhar DK, Yamaguchi E, Maruyama S, Sato T, Hayashi H et al. Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clin Cancer Res. 2001;7:1325–32.
  PubMed CAS Google Scholar
• Calvisi DF, Pinna F, Ladu S, Pellegrino R, Muroni MR, Simile MM et al. Aberrant iNOS signaling is under genetic control in rodent liver cancer and potentially prognostic for the human disease. Carcinogenesis. 2008;29:1639–47.
  Article PubMed CAS Google Scholar
• Tazawa R, Xu XM, Wu KK, Wang LH. Characterization of the genomic structure, chromosomal location and promoter of human prostaglandin H synthase-2 gene. Biochem Biophys Res Commun. 1994;203:190–9.
  Article PubMed CAS Google Scholar
• Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-B/Rel in induction of nitric oxide synthase. J Biol Chem. 1994;269:4705–8.
  PubMed CAS Google Scholar
• Ueno S, Aoki D, Kubo F, Hiwatashi K, Matsushita K, Oyama T et al. Roxithromyc inhibits constitutive activation of nuclear factor κB by diminishing oxidative stress in a rat model of hepatocellular carcinoma. Clin Cancer Res. 2005;11:5645–50.
  Article PubMed CAS Google Scholar
• Yang Z, Yang S, Misner BJ, Chiu R, Liu F, Meyskens FL. Nitric oxide initiates progression of human melanoma via a feedback loop mediated by apurinic/apyrimidinic endonuclease-1/redox factor-1, which is inhibited by resveratrol. Mol Cancer Ther. 2008;7:3751–60.
  Article PubMed CAS Google Scholar
• Kang O-H, Jang H-J, Chae H-S, Oh Y-C, Choi J-G, Lee Y-S et al. Anti-inflammatory mechanisms of resveratrol in activated HMC-1 cells: pivotal roles of NF-κB and MAPK. Pharmacol Res. 2009;59:330–7.
  Article PubMed CAS Google Scholar
• Cichocki M, Paluszczak J, Szaefer H, Piechowiak A, Rimando AM, Baer-Dubowska W. Pterostilbene is equally potent as resveratrol in inhibiting 12-_O_-tetradecanoylphorbol-13-acetate activated NFκB, AP-1, COX-2, and iNOS in mouse epidermis. Mol Nutr Food Res. 2008;52:S62–70.
  Article PubMed CAS Google Scholar
• Chávez E, Reyes-Gordillo K, Segovia J, Shibayama M, Tsutsumi V, Vergara P et al. Resveratrol prevents fibrosis, NF-κB activation and TGF-β increases by chronic CCl4 treatment in rats. J Appl Toxicol. 2008;28:35–43.
  Article PubMed CAS Google Scholar
• Holmes-McNary M, Baldwin Jr AS. Chemopreventive properties of _trans_-resveratrol are associated with inhibition of activation of the IkappaB kinase. Cancer Res. 2000;60:3477–83.
  PubMed CAS Google Scholar
• Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003;425:191–6.
  Article PubMed CAS Google Scholar