Acyclic retinoid inhibits diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BLKS/J- +Leprdb/+Leprdb mice

Cancer Prevention Research

Volumn 4, Issue 1, 2011, Pages 128-136

  Shimizu, Masahito ^a   Sakai, Hiroyasu ^a   Shirakami, Yohei ^a   Iwasa, Junpei ^a   Yasuda, Yoichi ^a   Kubota, Masaya ^a   Takai, Koji ^a   Tsurumi, Hisashi ^a   Tanaka, Takuji ^b   Moriwaki, Hisataka ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACYCLIC RETINOID; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; DIETHYLNITROSAMINE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS; PROTEIN C JUN; RAS PROTEIN; RETINOID; RETINOID X RECEPTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CHEMOPROPHYLAXIS; CHRONIC INFLAMMATION; CONTROLLED STUDY; DIABETES MELLITUS; EXPERIMENTAL MOUSE; HUMAN; HYPERTRIGLYCERIDEMIA; INSULIN SENSITIVITY; LIPID STORAGE; LIVER ADENOMA; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER DEVELOPMENT; MALE; MOUSE; NONHUMAN; OBESITY; ONCOGENE C FOS; ONCOGENE C JUN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; STEATOSIS;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CYTOKINES; DIABETES COMPLICATIONS; DIABETES MELLITUS; DIETHYLNITROSAMINE; INSULIN RESISTANCE; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; PHOSPHORYLATION; RAS PROTEINS; RECEPTORS, LEPTIN; RETINOID X RECEPTOR ALPHA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; TRETINOIN;

EID: 78650841188     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-10-0163     Document Type: Article

References (49)

1. El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 2004;126:460-8.
2. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007;132:2557-76.
3. Muto Y, Sato S, Watanabe A, Moriwaki H, Suzuki K, Kato A, et al. Overweight and obesity increase the risk for liver cancer in patients with liver cirrhosis and long-term oral supplementation with branchedchain amino acid granules inhibits liver carcinogenesis in heavier patients with liver cirrhosis. Hepatol Res 2006;35:204-14.
4. Iwasa J, Shimizu M, Shiraki M, Shirakami Y, Sakai H, Terakura Y, et al. Dietary supplementation with branched-chain amino acids suppresses diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BL/KsJ-db/db mice. Cancer Sci 2010;101:460-7.
5. El-Serag HB, Richardson PA, Everhart JE. The role of diabetes in hepatocellular carcinoma: a case-control study among United States Veterans. Am J Gastroenterol 2001;96:2462-7.
6. Imai K, Takai K, Nishigaki Y, Shimizu S, Naiki T, Hayashi H, et al. Insulin resistance raises the risk for recurrence of stage I hepatocellular carcinoma after curative radiofrequency ablation in hepatitis C virus-positive patients: a prospective, case series study. Hepatol Res 2010;40:376-82.
7. Siegel AB, Zhu AX. Metabolic syndrome and hepatocellular carcinoma: two growing epidemics with a potential link. Cancer 2009;115:5651-61.
8. Smedile A, Bugianesi E. Steatosis and hepatocellular carcinoma risk. Eur Rev Med Pharmacol Sci 2005;9:291-3.
9. Powell EE, Jonsson JR, Clouston AD. Steatosis: co-factor in other liver diseases. Hepatology 2005;42:5-13.
10. Shimizu M, Takai K, Moriwaki H. Strategy and mechanism for the prevention of hepatocellular carcinoma: phosphorylated retinoid X receptor alpha is a critical target for hepatocellular carcinoma chemoprevention. Cancer Sci 2009;100:369-74.
11. Muto Y, Moriwaki H. Antitumor activity of vitamin A and its derivatives. J Natl Cancer Inst 1984;73:1389-93.
12. Suzui M, Masuda M, Lim JT, Albanese C, Pestell RG, Weinstein IB. Growth inhibition of human hepatoma cells by acyclic retinoid is associated with induction of p21(CIP1) and inhibition of expression of cyclin D1. Cancer Res 2002;62:3997-4006.
13. Suzui M, Shimizu M, Masuda M, Lim JT, Yoshimi N, Weinstein IB. Acyclic retinoid activates retinoic acid receptor beta and induces transcriptional activation of p21(CIP1) in HepG2 human hepatoma cells. Mol Cancer Ther 2004;3:309-16. (Pubitemid 39193706)
14. Shimizu M, Suzui M, Deguchi A, Lim JT, Xiao D, Hayes JH, et al. Synergistic effects of acyclic retinoid and OSI-461 on growth inhibition and gene expression in human hepatoma cells. Clin Cancer Res 2004;10:6710-21.
15. Tatebe H, Shimizu M, Shirakami Y, Sakai H, Yasuda Y, Tsurumi H, et al. Acyclic retinoid synergises with valproic acid to inhibit growth in human hepatocellular carcinoma cells. Cancer Lett 2009;285:210-7.
16. Araki H, Shidoji Y, Yamada Y, Moriwaki H, Muto Y. Retinoid agonist activities of synthetic geranyl geranoic acid derivatives. Biochem Biophys Res Commun 1995;209:66-72.
17. Muto Y, Moriwaki H, Ninomiya M, Adachi S, Saito A, Takasaki KT, et al. Prevention of second primary tumors by an acyclic retinoid, polyprenoic acid, in patients with hepatocellular carcinoma. Hepatoma Prevention Study Group. N Engl J Med 1996;334:1561-7.
18. Muto Y, Moriwaki H, Saito A. Prevention of second primary tumors by an acyclic retinoid in patients with hepatocellular carcinoma. N Engl J Med 1999;340:1046-7.
19. Okita K, Matsui O, Kumada H, Tanaka K, Kaneko S, Moriwaki H, et al. Effect of peretinoin on recurrence of hepatocellular carcinoma (HCC): Results of a phase II/III randomized placebo-controlled trial. J Clin Oncol 2010;28Suppl 7s:4024.
20. Germain P, Chambon P, Eichele G, Evans RM, Lazar MA, Leid M, et al. International Union of Pharmacology. LXIII. Retinoid X receptors. Pharmacol Rev 2006;58:760-72.
21. Matsushima-Nishiwaki R, Okuno M, Adachi S, Sano T, Akita K, Moriwaki H, et al. Phosphorylation of retinoid X receptor alpha at serine 260 impairs its metabolism and function in human hepatocellular carcinoma. Cancer Res 2001;61:7675-82. (Pubitemid 32995065)
22. Yoshimura K, Muto Y, Shimizu M, Matsushima-Nishiwaki R, Okuno M, Takano Y, et al. Phosphorylated retinoid X receptor alpha loses its heterodimeric activity with retinoic acid receptor beta. Cancer Sci 2007;98:1868-74.
23. Matsushima-Nishiwaki R, Okuno M, Takano Y, Kojima S, Friedman SL, Moriwaki H. Molecular mechanism for growth suppression of human hepatocellular carcinoma cells by acyclic retinoid. Carcinogenesis 2003;24:1353-9.
24. Kanamori T, Shimizu M, Okuno M, Matsushima-Nishiwaki R, Tsurumi H, Kojima S, et al. Synergistic growth inhibition by acyclic retinoid and vitamin K2 in human hepatocellular carcinoma cells. Cancer Sci 2007;98:431-7.
25. Kagawa M, Sano T, Ishibashi N, Hashimoto M, Okuno M, Moriwaki H, et al. An acyclic retinoid, NIK-333, inhibits N-diethylnitrosamine-induced rat hepatocarcinogenesis through suppression of TGF-alpha expression and cell proliferation. Carcinogenesis 2004;25:979-85.
26. Sano T, Kagawa M, Okuno M, Ishibashi N, Hashimoto M, Yamamoto M, et al. Prevention of rat hepatocarcinogenesis by acyclic retinoid is accompanied by reduction in emergence of both TGF-alpha-expressing oval-like cells and activated hepatic stellate cells. Nutr Cancer 2005;51:197-206.
27. Frith CH, Ward JM, Turusov VS. Tumours of the liver. In: Turusor VS, Mohr U, editors. Pathology of Tumors in Laboratory Animals. Vol 2. Lyon, France: IARC Scientific Publications; 1994. p. 223-70.
28. Shimizu M, Suzui M, Deguchi A, Lim JT, Weinstein IB. Effects of acyclic retinoid on growth, cell cycle control, epidermal growth factor receptor signaling, and gene expression in human squamous cell carcinoma cells. Clin Cancer Res 2004;10:1130-40.
29. Yasuda Y, Shimizu M, Shirakami Y, Sakai H, Kubota M, Hata K, et al. Pitavastatin inhibits azoxymethane-induced colonic preneoplastic lesions in C57BL/KsJ-db/db obese mice. Cancer Sci 2010;101:555-66.
30. Sakai H, Yamada Y, Shimizu M, Saito K, Moriwaki H, Hara A. Genetic ablation of TNFalpha demonstrates no detectable suppressive effect on inflammation-related mouse colon tumorigenesis. Chem Biol Interact 2010;184:423-30.
31. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000;85:2402-10.
32. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957;226:497-509.
33. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007;8:774-85.
34. Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, et al. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010;140:197-208.
35. Kawaguchi T, Nagao Y, Matsuoka H, Ide T, Sata M. Branched-chain amino acid-enriched supplementation improves insulin resistance in patients with chronic liver disease. Int J Mol Med 2008;22:105-12.
36. Alvarez S, Germain P, Alvarez R, Rodriguez-Barrios F, Gronemeyer H, de Lera AR. Structure, function and modulation of retinoic acid receptor beta, a tumor suppressor. Int J Biochem Cell Biol 2007;39:1406-15. (Pubitemid 47031031)
37. Teraishi F, Kadowaki Y, Tango Y, Kawashima T, Umeoka T, Kagawa S, et al. Ectopic p21sdi1 gene transfer induces retinoic acid receptor beta expression and sensitizes human cancer cells to retinoid treatment. Int J Cancer 2003;103:833-9.
38. Senturk S, Mumcuoglu M, Gursoy-Yuzugullu O, Cingoz B, Akcali KC, Ozturk M. Transforming growth factor-beta induces senescence in hepatocellular carcinoma cells and inhibits tumor growth. Hepatology 2010;52:966-74.
39. Okuno M, Moriwaki H, Imai S, Muto Y, Kawada N, Suzuki Y, et al. Retinoids exacerbate rat liver fibrosis by inducing the activation of latent TGF-beta in liver stellate cells. Hepatology 1997;26:913-21.
40. Mukherjee R, Davies PJ, Crombie DL, Bischoff ED, Cesario RM, Jow L, et al. Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature 1997;386:407-10.
41. Yamazaki K, Shimizu M, Okuno M, Matsushima-Nishiwaki R, Kanemura N, Araki H, et al. Synergistic effects of RXR alpha and PPAR gamma ligands to inhibit growth in human colon cancer cells - phosphorylated RXR alpha is a critical target for colon cancer management. Gut 2007;56:1557-63.
42. Fay JR, Steele V, Crowell JA. Energy homeostasis and cancer prevention: the AMP-activated protein kinase. Cancer Prev Res 2009; 2:301-9.
43. Fogarty S, Hardie DG. Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim Biophys Acta 2010;1804:581-91.
44. Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD. Metformin and reduced risk of cancer in diabetic patients. BMJ 2005;330:1304-5.
45. Jiang W, Zhu Z, Thompson HJ. Dietary energy restriction modulates the activity of AMP-activated protein kinase, Akt, and mammalian target of rapamycin in mammary carcinomas, mammary gland, and liver. Cancer Res 2008;68:5492-9.
46. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 1996;271:665-8.
47. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007;317:121-4. (Pubitemid 47056470)
48. He G, Yu GY, Temkin V, Ogata H, Kuntzen C, Sakurai T, et al. Hepatocyte IKKbeta/NF-kappaB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 2010;17:286-97.
49. Calvisi DF, Ladu S, Gorden A, Farina M, Conner EA, Lee JS, et al. Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 2006;130:1117-28.