Combination treatment of angiotensin II type I receptor blocker and new oral iron chelator attenuates progression of nonalcoholic steatohepatitis in rats

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 6, 2011, Pages

  Kaji, Kosuke ^a   Yoshiji, Hitoshi ^a   Kitade, Mitsuteru ^a   Ikenaka, Yasuhide ^a   Noguchi, Ryuichi ^a   Shirai, Yusaku ^a   Aihara, Yosuke ^a   Namisaki, Tadashi ^a   Yoshii, Junichi ^a   Yanase, Koji ^a   Tsujimoto, Tatsuhiro ^a   Kawaratani, Hideto ^a   Fukui, Hiroshi ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Hepatic stellate cells; Oxidative stress; Vascular endothelial growth factor

Indexed keywords

AMINO ACID; ANGIOTENSIN 2 RECEPTOR ANTAGONIST; CHOLINE; DEFERASIROX; IRON CHELATING AGENT; LOSARTAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET; DISEASE COURSE; HUMAN; LIVER CARCINOGENESIS; LIVER FIBROSIS; MALE; NEOVASCULARIZATION (PATHOLOGY); NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; VITAMIN DEFICIENCY;

ADMINISTRATION, ORAL; ANGIOGENESIS INHIBITORS; ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANTIOXIDANTS; BENZOIC ACIDS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELLS, CULTURED; CHOLINE DEFICIENCY; DISEASE PROGRESSION; DRUG THERAPY, COMBINATION; FATTY LIVER; HEPATIC STELLATE CELLS; IRON CHELATING AGENTS; LIVER CIRRHOSIS, EXPERIMENTAL; LIVER NEOPLASMS, EXPERIMENTAL; LOSARTAN; MALE; NEOVASCULARIZATION, PATHOLOGIC; OXIDATIVE STRESS; RATS; RATS, INBRED F344; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TRIAZOLES;

EID: 79957930356     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00365.2010     Document Type: Article

References (55)

1. Agarwal MB. Deferasirox: oral, once daily iron chelator-an expert opinion. Indian J Pediatr 77: 185-191, 2010.
2. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 346: 1221- 1231, 2002.
3. Bruin GJ, Faller T, Wiegand H, Schweitzer A, Nick H, Schneider J, Boernsen KO, Waldmeier F. Pharmacokinetics, distribution, metabolism, and excretion of deferasirox and its iron complex in rats. Drug Metab Dispos 36: 2523-2538, 2008.
4. Bugianesi E, Manzini P, D'Antico S, Vanni E, Longo F, Leone N, Massarenti P, Piga A, Marchesini G, Rizzetto M. Relative contribution of iron burden, HFE mutations, and insulin resistance to fibrosis in nonalcoholic fatty liver. Hepatology 39: 179-187, 2004.
5. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438: 932-936, 2005.
6. Chong TW, Horwitz LD, Moore JW, Sowter HM, Harris AL. A mycobacterial iron chelator, desferri-exochelin, induces hypoxia-inducible factors 1 and 2, NIP3, and vascular endothelial growth factor in cancer cell lines. Cancer Res 62: 6924-6927, 2002.
7. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology 114: 842-845, 1998.
8. Dongiovanni P, Valenti L, Ludovica Fracanzani A, Gatti S, Cairo G, Fargion S. Iron depletion by deferoxamine up-regulates glucose uptake and insulin signaling in hepatoma cells and in rat liver. Am J Pathol 172: 738-747, 2008.
9. Fargion S, Mattioli M, Fracanzani AL, Sampietro M, Tavazzi D, Fociani P, Taioli E, Valenti L, Fiorelli G. Hyperferritinemia, iron overload, and multiple metabolic alterations identify patients at risk for nonalcoholic steatohepatitis. Am J Gastroenterol 96: 2448-2455, 2001.
10. Fu Y, Zhang R, Lu D, Liu H, Chandrashekar K, Juncos LA, Liu R. NOX2 is the primary source of angiotensin II-induced superoxide in the macula densa. Am J Physiol Regul Integr Comp Physiol 298: R707-R712, 2010.
11. Fujita N, Miyachi H, Tanaka H, Takeo M, Nakagawa N, Kobayashi Y, Iwasa M, Watanabe S, Takei Y. Iron overload is associated with hepatic oxidative damage to DNA in nonalcoholic steatohepatitis. Cancer Epidemiol Biomarkers Prev 18: 424-432, 2009.
12. Galaris D, Pantopoulos K. Oxidative stress and iron homeostasis: mechanistic and health aspects. Crit Rev Clin Lab Sci 45: 1-23, 2008.
13. Gatlin CL, Schaberg ES, Jordan WH, Kuyatt BL, Smith WC. Point counting on the Macintosh. A semiautomated image analysis technique. Anal Quant Cytol Histol 15: 345-350, 1993.
14. George DK, Goldwurm S, MacDonald GA, Cowley LL, Walker NI, Ward PJ, Jazwinska EC, Powell LW. Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosis. Gastroenterology 114: 311-318, 1998.
15. Hirose A, Ono M, Saibara T, Nozaki Y, Masuda K, Yoshioka A, Takahashi M, Akisawa N, Iwasaki S, Oben JA, Onishi S. Angiotensin II type 1 receptor blocker inhibits fibrosis in rat nonalcoholic steatohepatitis. Hepatology 45: 1375-1381, 2007.
16. Ishizaka N, Saito K, Noiri E, Sata M, Ikeda H, Ohno A, Ando J, Mori I, Ohno M, Nagai R. Administration of ANG II induces iron deposition and upregulation of TGF-beta 1 mRNA in the rat liver. Am J Physiol Regul Integr Comp Physiol 288: R1063-R1070, 2005.
17. Kang DH, Hughes J, Mazzali M, Schreiner GF, Johnson RJ. Impaired angiogenesis in the remnant kidney model. II. Vascular endothelial growth factor administration reduces renal fibrosis and stabilizes renal function. J Am Soc Nephrol 12: 1448-1457, 2001.
18. Kawada N, Imanaka K, Kawaguchi T, Tamai C, Ishihara R, Matsunaga T, Gotoh K, Yamada T, Tomita Y. Hepatocellular carcinoma arising from non-cirrhotic nonalcoholic steatohepatitis. J Gastroenterol 44: 1190-1194, 2009.
19. Kirsch R, Sijtsema HP, Tlali M, Marais AD, Hall PL. Effects of iron overload in a rat nutritional model of non-alcoholic fatty liver disease. Liver Int 26: 1258-1267, 2006.
20. Kitade M, Yoshiji H, Kojima H, Ikenaka Y, Noguchi R, Kaji K, Yoshii J, Yanase K, Namisaki T, Asada K, Yamazaki M, Tsujimoto T, Akahane T, Uemura M, Fukui H. Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology 44: 983-991, 2006.
21. Kitade M, Yoshiji H, Noguchi R, Ikenaka Y, Kaji K, Shirai Y, Yamazaki M, Uemura M, Yamao J, Fujimoto M, Mitoro A, Toyohara M, Sawai M, Yoshida M, Morioka C, Tsujimoto T, Kawaratani H, Fukui H. Crosstalk between angiogenesis, cytokeratin-18, and insulin resistance in the progression of non-alcoholic steatohepatitis. World J Gastroenterol 15: 5193-5199, 2009.
22. Murata K, Moriyama M. Isoleucine, an essential amino acid, prevents liver metastases of colon cancer by antiangiogenesis. Cancer Res 67: 3263-3268, 2007.
23. Nahon P, Sutton A, Rufat P, Ziol M, Thabut G, Schischmanoff PO, Vidaud D, Charnaux N, Couvert P, Ganne-Carrie N, Trinchet JC, Gattegno L, Beaugrand M. Liver iron, HFE gene mutations, and hepatocellular carcinoma occurrence in patients with cirrhosis. Gastroenterology 134: 102-110, 2008.
24. Nahon P, Ganne-Carrie N, Trinchet JC, Beaugrand M. Hepatic iron overload and risk of hepatocellular carcinoma in cirrhosis. Gastroenterol Clin Biol 34: 1-7, 2010.
25. Nakae D, Yoshiji H, Mizumoto Y, Horiguchi K, Shiraiwa K, Tamura K, Denda A, Konishi Y. High incidence of hepatocellular carcinoma induced by a choline deficient L-amino acid defined diet in rats. Cancer Res 52: 5042-5045, 1992.
26. Nomoto K, Tsuneyama K, Takahashi H, Murai Y, Takano Y. Cytoplasmic fine granular expression of 8-hydroxydeoxyguanosine reflects early mitochondrial oxidative DNA damage in nonalcoholic fatty liver disease. Appl Immunohistochem Mol Morphol 16: 71-75, 2008.
27. Page JM, Harrison SA. NASH and HCC. Clin Liver Dis 13: 631-647, 2009.
28. Patsenker E, Popov Y, Stickel F, Schneider V, Ledermann M, Sagesser H, Niedobitek G, Goodman SL, Schuppan D. Pharmacological inhibition of integrin alphavbeta3 aggravates experimental liver fibrosis and suppresses hepatic angiogenesis. Hepatology 50: 1501-1511, 2009.
29. Pscherer S, Heemann U, Frank H. Effect of renin-angiotensin system blockade on insulin resistance and inflammatory parameters in patients with impaired glucose tolerance. Diabetes Care 33: 914-919, 2010.
30. Reid AE. Nonalcoholic steatohepatitis. Gastroenterology 121: 710-723, 2001.
31. Sakaida I, Hironaka K, Uchida K, Okita K. Iron chelator deferoxamine reduces preneoplastic lesions in liver induced by choline-deficient L-amino acid-defined diet in rats. Dig Dis Sci 44: 560-569, 1999.
32. Seki S, Kitada T, Yamada T, Sakaguchi H, Nakatani K, Wakasa K. In situ detection of lipid peroxidation and oxidative DNA damage in nonalcoholic fatty liver diseases. J Hepatol 37: 56-62, 2002.
33. Shimizu I, Ma YR, Mizobuchi Y, Liu F, Miura T, Nakai Y, Yasuda M, Shiba M, Horie T, Amagaya S, Kawada N, Hori H, Ito S. Effects of Sho-saiko-to, a Japanese herbal medicine, on hepatic fibrosis in rats. Hepatology 29: 149-160, 1999.
34. Sorrentino P, D'Angelo S, Ferbo U, Micheli P, Bracigliano A, Vecchione R. Liver iron excess in patients with hepatocellular carcinoma developed on nonalcoholic steato-hepatitis. J Hepatol 50: 351-357, 2009.
35. Sumida Y, Nakashima T, Yoh T, Furutani M, Hirohama A, Kakisaka Y, Nakajima Y, Ishikawa H, Mitsuyoshi H, Okanoue T, Kashima K, Nakamura H, Yodoi J. Serum thioredoxin levels as a predictor of steatohepatitis in patients with nonalcoholic fatty liver disease. J Hepatol 38: 32-38, 2003.
36. Sumida Y, Yoshikawa T, Okanoue T. Role of hepatic iron in nonalcoholic steatohepatitis. Hepatol Res 39: 213-222, 2009.
37. Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 264: 85-97, 2004.
38. Valenti L, Fracanzani AL, Dongiovanni P, Bugianesi E, Marchesini G, Manzini P, Vanni E, Fargion S. Iron depletion by phlebotomy improves insulin resistance in patients with nonalcoholic fatty liver disease and hyperferritinemia: evidence from a case-control study. Am J Gastroenterol 102: 1251-1258, 2007.
39. Videla LA, Fernandez V, Tapia G, Varela P. Oxidative stress-mediated hepatotoxicity of iron and copper: role of Kupffer cells. Biometals 16: 103-111, 2003.
40. Villanueva A, Chiang DY, Newell P, Peix J, Thung S, Alsinet C, Tovar V, Roayaie S, Minguez B, Sole M, Battiston C, Van Laarhoven S, Fiel MI, Di Feo A, Hoshida Y, Yea S, Toffanin S, Ramos A, Martignetti JA, Mazzaferro V, Bruix J, Waxman S, Schwartz M, Meyerson M, Friedman SL, Llovet JM. Pivotal role of mTOR signaling in hepatocellular carcinoma. Gastroenterology 135: 1972-1983, 2008.
41. Wei Y, Clark SE, Morris EM, Thyfault JP, Uptergrove GM, Whaley-Connell AT, Ferrario CM, Sowers JR, Ibdah JA. Angiotensin II-induced non-alcoholic fatty liver disease is mediated by oxidative stress in transgenic TG(mRen2)27(Ren2) rats. J Hepatol 49: 417-428, 2008.
42. Weiskirchen R, Gressner AM. Isolation and culture of hepatic stellate cells. Methods Mol Med 117: 99-113, 2005.
43. Woo KJ, Lee TJ, Park JW, Kwon TK. Desferrioxamine, an iron chelator, enhances HIF-1alpha accumulation via cyclooxygenase-2 signaling pathway. Biochem Biophys Res Commun 343: 8-14, 2006.
44. Yamamoto M, Iwasa M, Iwata K, Kaito M, Sugimoto R, Urawa N, Mifuji R, Konishi M, Kobayashi Y, Adachi Y. Restriction of dietary calories, fat and iron improves non-alcoholic fatty liver disease. J Gastroenterol Hepatol 22: 498-503, 2007.
45. Yesilova Z, Yaman H, Oktenli C, Ozcan A, Uygun A, Cakir E, Sanisoglu SY, Erdil A, Ates Y, Aslan M, Musabak U, Erbil MK, Karaeren N, Dagalp K. Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic fatty liver disease. Am J Gastroenterol 100: 850-855, 2005.
46. Yokohama S, Yoneda M, Haneda M, Okamoto S, Okada M, Aso K, Hasegawa T, Tokusashi Y, Miyokawa N, Nakamura K. Therapeutic efficacy of an angiotensin II receptor antagonist in patients with nonalcoholic steatohepatitis. Hepatology 40: 1222-1225, 2004.
47. Yoshiji H, Nakae D, Mizumoto Y, Horiguchi K, Tamura K, Denda A, Tsujii T, Konishi Y. Inhibitory effect of dietary iron deficiency on inductions of putative preneoplastic lesions as well as 8-hydroxydeoxyguanosine in DNA and lipid peroxidation in the livers of rats caused by exposure to a choline-deficient L-amino acid defined diet. Carcinogenesis 13: 1227-1233, 1992.
48. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Nakatani T, Tsujinoue H, Fukui H. Angiotensin-II type 1 receptor interaction is a major regulator for liver fibrosis development in rats. Hepatology 34: 745-750, 2001.
49. Yoshiji H, Yoshii J, Ikenaka Y, Noguchi R, Tsujinoue H, Nakatani T, Imazu H, Yanase K, Kuriyama S, Fukui H. Inhibition of reninangiotensin system attenuates liver enzyme-altered preneoplastic lesions and fibrosis development in rats. J Hepatol 37: 22-30, 2002.
50. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, Wu Y, Yanase K, Namisaki T, Yamazaki M, Tsujinoue H, Imazu H, Masaki T, Fukui H. Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrosis. Gut 52: 1347-1354, 2003.
51. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, Wu Y, Yanase K, Namisaki T, Kitade M, Yamazaki M, Tsujinoue H, Masaki T, Fukui H. Halting the interaction between vascular endothelial growth factor and its receptors attenuates liver carcinogenesis in mice. Hepatology 39: 1517-1524, 2004.
52. Yoshiji H, Kuriyama S, Noguchi R, Yoshii J, Ikenaka Y, Yanase K, Namisaki T, Kitade M, Yamazaki M, Masaki T, Fukui H. Combination of vitamin K2 and the angiotensin-converting enzyme inhibitor, perindopril, attenuates the liver enzyme-altered preneoplastic lesions in rats via angiogenesis suppression. J Hepatol 42: 687-693, 2005.
53. Yoshiji H, Kuriyama S, Noguchi R, Yoshii J, Ikenaka Y, Yanase K, Namisaki T, Kitade M, Yamazaki M, Tsujinoue H, Fukui H. Combination of interferon-beta and angiotensin-converting enzyme inhibitor, perindopril, attenuates the murine liver fibrosis development. Liver Int 25: 153-161, 2005.
54. Yoshiji H, Kuriyama S, Noguchi R, Ikenaka Y, Kitade M, Kaji K, Yoshii J, Yanase K, Yamazaki M, Asada K, Tsujimoto T, Akahane T, Uemura M, Fukui H. Angiotensin-II and vascular endothelial growth factor interaction plays an important role in rat liver fibrosis development. Hepatol Res 36: 124-129, 2006.
55. Yoshiji H, Noguchi R, Ikenaka Y, Namisaki T, Kitade M, Kaji K, Shirai Y, Yoshii J, Yanase K, Yamazaki M, Tsujimoto T, Kawaratani H, Akahane T, Aihara Y, Fukui H. Losartan, an angiotensin-II type 1 receptor blocker, attenuates the liver fibrosis development of non-alcoholic steatohepatitis in the rat. BMC Res Notes 2: 70, 2009.