Combination of sorafenib and angiotensin-II receptor blocker attenuates preneoplastic lesion development in a non-diabetic rat model of steatohepatitis

Journal of Gastroenterology

Volumn 49, Issue 10, 2014, Pages 1421-1429

  Yoshiji, Hitoshi ^a   Noguchi, Ryuichi ^a   Namisaki, Tadashi ^a   Moriya, Kei ^a   Kitade, Mitsuteru ^a   Aihara, Yosuke ^a   Douhara, Akitoshi ^a   Kawaratani, Hideto ^a   Nishimura, Norihisa ^a   Fukui, Hiroshi ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Angiotensin II; Hepatocarcinogenesis; Non alcoholic steatohepatitis; Sorafenib

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ALPHA SMOOTH MUSCLE ACTIN; AMINO ACID; BILIRUBIN; CD31 ANTIGEN; CHOLINE; LOSARTAN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SORAFENIB; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DISEASE COURSE; ENZYME PHOSPHORYLATION; IN VITRO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER FIBROSIS; LIVER FUNCTION; LIVER WEIGHT; LOW DRUG DOSE; MALE; NEOVASCULARIZATION (PATHOLOGY); NONALCOHOLIC FATTY LIVER; NONHUMAN; OUTCOME ASSESSMENT; PRECANCER; RAT; TREATMENT DURATION; VITAMIN DEFICIENCY; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOMA, HEPATOCELLULAR; COMPLICATION; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; FISCHER 344 RAT; HEPG2 CELL LINE; HUMAN; LIVER NEOPLASMS, EXPERIMENTAL; PATHOLOGY; PRECANCEROUS CONDITIONS; PROCEDURES;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; LOSARTAN; MALE; NEOVASCULARIZATION, PATHOLOGIC; NIACINAMIDE; NON-ALCOHOLIC FATTY LIVER DISEASE; PHENYLUREA COMPOUNDS; PRECANCEROUS CONDITIONS; RATS, INBRED F344;

EID: 84919467172     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-013-0906-y     Document Type: Article

References (53)

1. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet. 2012;379:1245–55.
2. Yasui K, Hashimoto E, Tokushige K, Koike K, Shima T, Kanbara Y, et al. Clinical and pathological progression of non-alcoholic steatohepatitis to hepatocellular carcinoma. Hepatol Res. 2012;42:767–73.
3. Kerbel RS. Tumor angiogenesis: past, present and the near future. Carcinogenesis. 2000;21:505–15.
4. Shojaei F. Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett. 2012;320:130–7.
5. Guo RP, Zhong C, Shi M, Zhang CQ, Wei W, Zhang YQ, et al. Clinical value of apoptosis and angiogenesis factors in estimating the prognosis of hepatocellular carcinoma. J Cancer Res Clin Oncol. 2006;132:547–55.
6. Iavarone M, Lampertico P, Iannuzzi F, Manenti E, Donato MF, Arosio E, et al. Increased expression of vascular endothelial growth factor in small hepatocellular carcinoma. J Viral Hepat. 2007;14:133–9.
7. Dufour JF. Anti-angiogenic therapy for HCC. Minerva Gastroenterol Dietol. 2012;58:81–6.
8. Li CY, Shan S, Huang Q, Braun RD, Lanzen J, Hu K, et al. Initial stages of tumor cell-induced angiogenesis: evaluation via skin window chambers in rodent models. J Natl Cancer Inst. 2000;92:143–7.
9. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3:401–10.
10. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science. 1999;284:808–12.
11. Brandvold KA, Neiman P, Ruddell A. Angiogenesis is an early event in the generation of myc-induced lymphomas. Oncogene. 2000;19:2780–5.
12. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, et al. Halting the interaction between vascular endothelial growth factor and its receptors attenuates liver carcinogenesis in mice. Hepatology. 2004;39:1517–24.
13. Kerbel RS. Tumor angiogenesis. N Engl J Med. 2008;358:2039–49.
14. Romanque P, Piguet AC, Dufour JF. Targeting vessels to treat hepatocellular carcinoma. Clin Sci (Lond). 2008;114:467–77.
15. Wu XZ. New strategy of antiangiogenic therapy for hepatocellular carcinoma. Neoplasma. 2008;55:472–81.
16. Xie B, Wang DH, Spechler SJ. Sorafenib for treatment of hepatocellular carcinoma: a systematic review. Dig Dis Sci. 2012;57:1122–9.
17. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 2004;64:7099–109.
18. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359:378–90.
19. Eskens FA, Verweij J. The clinical toxicity profile of vascular endothelial growth factor (VEGF) and vascular endothelial growth factor receptor (VEGFR) targeting angiogenesis inhibitors; a review. Eur J Cancer. 2006;42:3127–39.
20. Verheul HM, Pinedo HM. Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition. Nat Rev Cancer. 2007;7:475–85.
21. Yoshiji H, Noguchi R, Ikenaka Y, Kitade M, Kaji K, Tsujimoto T, et al. Renin-angiotensin system inhibitors as therapeutic alternatives in the treatment of chronic liver diseases. Curr Med Chem. 2007;14:2749–54.
22. Nakai Y, Isayama H, Ijichi H, Sasaki T, Sasahira N, Hirano K, et al. Inhibition of renin-angiotensin system affects prognosis of advanced pancreatic cancer receiving gemcitabine. Br J Cancer. 2010;103:1644–8.
23. Yoshiji H, Noguchi R, Ikenaka Y, Namisaki T, Kitade M, Kaji K, et al. Losartan, an angiotensin-II type 1 receptor blocker, attenuates the liver fibrosis development of non-alcoholic steatohepatitis in the rat. BMC Res Notes. 2009;2:70.
24. Yoshiji H, Kuriyama S, Noguchi R, Yoshii J, Ikenaka Y, Yanase K, et al. Combination of vitamin K(2) and the angiotensin-converting enzyme inhibitor, perindopril, attenuates the liver enzyme-altered preneoplastic lesions in rats via angiogenesis suppression. J Hepatol. 2005;42:687–93.
25. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, et al. Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrogenesis. Gut. 2003;52:1347–54.
26. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, et al. Synergistic effect of basic fibroblast growth factor and vascular endothelial growth factor in murine hepatocellular carcinoma. Hepatology. 2002;35:834–42.
27. Yoshiji H, Kuriyama S, Noguchi R, Yoshii J, Ikenaka Y, Yanase K, et al. Angiopoietin 2 displays a vascular endothelial growth factor dependent synergistic effect in hepatocellular carcinoma development in mice. Gut. 2005;54:1768–75.
28. Saito M, Hamasaki M, Shibuya M. Induction of tube formation by angiopoietin-1 in endothelial cell/fibroblast co-culture is dependent on endogenous VEGF. Cancer Sci. 2003;94:782–90.
29. Saif MW. Anti-angiogenesis therapy in pancreatic carcinoma. Jop. 2006;7:163–73.
30. Feng YX, Wang T, Deng YZ, Yang P, Li JJ, Guan DX, et al. Sorafenib suppresses postsurgical recurrence and metastasis of hepatocellular carcinoma in an orthotopic mouse model. Hepatology. 2011;53:483–92.
31. Reiberger T, Angermayr B, Schwabl P, Rohr-Udilova N, Mitterhauser M, Gangl A, et al. Sorafenib attenuates the portal hypertensive syndrome in partial portal vein ligated rats. J Hepatol. 2009;51:865–73.
32. Wang Y, Gao J, Zhang D, Zhang J, Ma J, Jiang H. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J Hepatol. 2010;53:132–44.
33. Frachon S, Gouysse G, Dumortier J, Couvelard A, Nejjari M, Mion F, et al. Endothelial cell marker expression in dysplastic lesions of the liver: an immunohistochemical study. J Hepatol. 2001;34:850–7.
34. Iavarone M, Cabibbo G, Piscaglia F, Zavaglia C, Grieco A, Villa E, et al. Field-practice study of sorafenib therapy for hepatocellular carcinoma: a prospective multicenter study in Italy. Hepatology. 2011;54:2055–63.
35. Azad NS, Aragon-Ching JB, Dahut WL, Gutierrez M, Figg WD, Jain L, et al. Hand-foot skin reaction increases with cumulative sorafenib dose and with combination anti-vascular endothelial growth factor therapy. Clin Cancer Res Off J Am Assoc Cancer Res. 2009;15:1411–6.
36. Strumberg D, Awada A, Hirte H, Clark JW, Seeber S, Piccart P, et al. Pooled safety analysis of BAY 43-9006 (sorafenib) monotherapy in patients with advanced solid tumours: is rash associated with treatment outcome? Eur J Cancer. 2006;42:548–56.
37. Hora C, Romanque P, Dufour JF. Effect of sorafenib on murine liver regeneration. Hepatology. 2011;53:577–86.
38. Yoshiji H, Noguchi R, Kuriyama S, Yoshii J, Ikenaka Y. Combination of interferon and angiotensin-converting enzyme inhibitor, perindopril, suppresses liver carcinogenesis and angiogenesis in mice. Oncol Rep. 2005;13:491–5.
39. Yoshiji H, Noguchi R, Toyohara M, Ikenaka Y, Kitade M, Kaji K, et al. Combination of vitamin K2 and angiotensin-converting enzyme inhibitor ameliorates cumulative recurrence of hepatocellular carcinoma. J Hepatol. 2009;51:315–21.
40. Kaji K, Yoshiji H, Kitade M, Ikenaka Y, Noguchi R, Yoshii J, et al. Impact of insulin resistance on the progression of chronic liver diseases. Int J Mol Med. 2008;22:801–8.
41. Kaji K, Yoshiji H, Ikenaka Y, Noguchi R, Aihara Y, Shirai Y, et al. Possible involvement of angiogenesis in chronic liver diseases: interaction among renin-angiotensin-aldosterone system, insulin resistance and oxidative stress. Curr Med Chem. 2012;19:1889–98.
42. Paternostro C, David E, Novo E, Parola M. Hypoxia, angiogenesis and liver fibrogenesis in the progression of chronic liver diseases. World J Gastroenterol. 2010;16:281–8.
43. Valfre di Bonzo L, Novo E, Cannito S, Busletta C, Paternostro C, Povero D, et al. Angiogenesis and liver fibrogenesis. Histol Histopathol. 2009;24:1323–41.
44. Kitade M, Yoshiji H, Kojima H, Ikenaka Y, Noguchi R, Kaji K, et al. Leptin-mediated neovascularization is a prerequisite for progression of nonalcoholic steatohepatitis in rats. Hepatology. 2006;44:983–91.
45. Amarapurkar AD, Amarapurkar DN, Vibhav S, Patel ND. Angiogenesis in chronic liver disease. Ann Hepatol. 2007;6:170–3.
46. Ueno T, Nakamura T, Torimura T, Sata M. Angiogenic cell therapy for hepatic fibrosis. Med Mol Morphol. 2006;39:16–21.
47. Wang Y, Gao J, Zhang D, Zhang J, Ma J, Jiang H. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J Hepatol. 2010;53:132–44.
48. Sakaida I, Hironaka K, Uchida K, Suzuki C, Kayano K, Okita K. Fibrosis accelerates the development of enzyme-altered lesions in the rat liver. Hepatology. 1998;28:1247–52.
49. Zhang DY, Friedman SL. Fibrosis-dependent mechanisms of hepatocarcinogenesis. Hepatology. 2012;56:769–75.
50. Noguchi R, Yoshiji H, Ikenaka Y, Kaji K, Aihara Y, Shirai Y, et al. Dual blockade of angiotensin-II and aldosterone suppresses the progression of a non-diabetic rat model of steatohepatitis. Hepatol Res 2012.
51. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Nakatani T, et al. Angiotensin-II type 1 receptor interaction is a major regulator for liver fibrosis development in rats. Hepatology. 2001;34:745–50.
52. Tsujimoto T, Kawaratani H, Kitazawa T, Hirai T, Ohishi H, Kitade M, et al. Decreased phagocytic activity of Kupffer cells in a rat nonalcoholic steatohepatitis model. World J Gastroenterol. 2008;14:6036–43.
53. Nakae D, Yoshiji H, Mizumoto Y, Horiguchi K, Shiraiwa K, Tamura K, et al. High incidence of hepatocellular carcinomas induced by a choline deficient l-amino acid defined diet in rats. Cancer Res. 1992;52:5042–5.