Loss of c-Met accelerates development of liver fibrosis in response to CCl 4 exposure through deregulation of multiple molecular pathways

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 6, 2012, Pages 942-951

  Marquardt, Jens U ^a,b   Seo, Daekwan ^a   Gómez Quiroz, Luis E ^a,c   Uchida, Koichi ^a   Gillen, Matthew C ^a   Kitade, Mitsuteru ^a   Kaposi Novak, Pal ^a   Conner, Elizabeth A ^a   Factor, Valentina M ^a   Thorgeirsson, Snorri S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c DEPARTAMENTO DE QUÍMICA   (Mexico)

Author keywords

C met; CCl 4; Fibrosis; Microarray

Indexed keywords

CARBON TETRACHLORIDE; CELL CYCLE PROTEIN 6; CELL PROTEIN; CYCLIN G2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUTATHIONE TRANSFERASE A1; GLUTATHIONE TRANSFERASE A2; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN ACTB; PROTEIN ADAM8; PROTEIN C JUN; PROTEIN CDK10; PROTEIN CSNK2A; PROTEIN ERCC4; PROTEIN ICAM1; PROTEIN ITGB2; PROTEIN RAD9; PROTEIN TUBA1A; PROTEIN TUBA8; RAD52 PROTEIN; RANTES; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; FEMALE; FIBROGENESIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER FIBROSIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; STELLATE CELL; STRESS; TRANSCRIPTOMICS; WESTERN BLOTTING;

ANIMALS; CARBON TETRACHLORIDE; CELL ADHESION; CELL COMMUNICATION; CELL PROLIFERATION; DNA REPAIR; FEMALE; HEPATIC STELLATE CELLS; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; LIVER; LIVER CIRRHOSIS; LIVER REGENERATION; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

ANIMALIA; MUS;

EID: 84859073165     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.02.012     Document Type: Article

References (55)

1. Friedman S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008, 134:1655-1669.
2. Brunt E.M. Nonalcoholic steatohepatitis: definition and pathology. Semin. Liver Dis. 2001, 21:3-16.
3. Poynard T., Bedossa P., Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 1997, 349:825-832.
4. Brunt E.M. Nonalcoholic steatohepatitis. Semin. Liver Dis. 2004, 24:3-20.
5. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
6. Bataller R., North K.E., Brenner D.A. Genetic polymorphisms and the progression of liver fibrosis: a critical appraisal. Hepatology 2003, 37:493-503.
7. Friedman S.L., Rockey D.C., Bissell D.M. Hepatic fibrosis 2006: report of the Third AASLD Single Topic Conference. Hepatology 2007, 45:242-249.
8. Jiao J., Friedman S.L., Aloman C. Hepatic fibrosis. Curr. Opin. Gastroenterol. 2009, 25:223-229.
9. Borowiak M., Garratt A.N., Wustefeld T., Strehle M., Trautwein C., Birchmeier C. Met provides essential signals for liver regeneration. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10608-10613.
10. Huh C.G., Factor V.M., Sanchez A., Uchida K., Conner E.A., Thorgeirsson S.S. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4477-4482.
11. Sato M., Kakubari M., Kawamura M., Sugimoto J., Matsumoto K., Ishii T. The decrease in total collagen fibers in the liver by hepatocyte growth factor after formation of cirrhosis induced by thioacetamide. Biochem. Pharmacol. 2000, 59:681-690.
12. Ueki T., Kaneda Y., Tsutsui H., Nakanishi K., Sawa Y., Morishita R., Matsumoto K., Nakamura T., Takahashi H., Okamoto E., Fujimoto J. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat. Med. 1999, 5:226-230.
13. Inagaki Y., Higashi K., Kushida M., Hong Y.Y., Nakao S., Higashiyama R., Moro T., Itoh J., Mikami T., Kimura T., Shiota G., Kuwabara I., Okazaki I. Hepatocyte growth factor suppresses profibrogenic signal transduction via nuclear export of Smad3 with galectin-7. Gastroenterology 2008, 134:1180-1190.
14. Kim W.H., Matsumoto K., Bessho K., Nakamura T. Growth inhibition and apoptosis in liver myofibroblasts promoted by hepatocyte growth factor leads to resolution from liver cirrhosis. Am. J. Pathol. 2005, 166:1017-1028.
15. Matsuda Y., Matsumoto K., Ichida T., Nakamura T. Hepatocyte growth factor suppresses the onset of liver cirrhosis and abrogates lethal hepatic dysfunction in rats. J. Biochem. 1995, 118:643-649.
16. Ozaki I., Zhao G., Mizuta T., Ogawa Y., Hara T., Kajihara S., Hisatomi A., Sakai T., Yamamoto K. Hepatocyte growth factor induces collagenase (matrix metalloproteinase-1) via the transcription factor Ets-1 in human hepatic stellate cell line. J. Hepatol. 2002, 36:169-178.
17. Fausto N. Liver regeneration. J. Hepatol. 2000, 32:19-31.
18. Jamall I.S., Finelli V.N., Que Hee S.S. A simple method to determine nanogram levels of 4-hydroxyproline in biological tissues. Anal. Biochem. 1981, 112:70-75.
19. Scheuer P.J. Classification of chronic viral hepatitis: a need for reassessment. J. Hepatol. 1991, 13:372-374.
20. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
21. Gomez-Quiroz L.E., Factor V.M., Kaposi-Novak P., Coulouarn C., Conner E.A., Thorgeirsson S.S. Hepatocyte-specific c-Met deletion disrupts redox homeostasis and sensitizes to Fas-mediated apoptosis. J. Biol. Chem. 2008, 283:14581-14589.
22. Andersen J.B., Loi R., Perra A., Factor V.M., Ledda-Columbano G.M., Columbano A., Thorgeirsson S.S. Progenitor-derived hepatocellular carcinoma model in the rat. Hepatology 2010, 51:1401-1409.
23. Kaposi-Novak P., Lee J.S., Gomez-Quiroz L., Coulouarn C., Factor V.M., Thorgeirsson S.S. Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. J. Clin. Invest. 2006, 116:1582-1595.
24. Burr A.W., Toole K., Chapman C., Hines J.E., Burt A.D. Anti-hepatocyte growth factor antibody inhibits hepatocyte proliferation during liver regeneration. J. Pathol. 1998, 185:298-302.
25. Phaneuf D., Moscioni A.D., LeClair C., Raper S.E., Wilson J.M. Generation of a mouse expressing a conditional knockout of the hepatocyte growth factor gene: demonstration of impaired liver regeneration. DNA Cell Biol. 2004, 23:592-603.
26. Postic C., Magnuson M.A. DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis 2000, 26:149-150.
27. Giebeler A., Boekschoten M.V., Klein C., Borowiak M., Birchmeier C., Gassler N., Wasmuth H.E., Muller M., Trautwein C., Streetz K.L. c-Met confers protection against chronic liver tissue damage and fibrosis progression after bile duct ligation in mice. Gastroenterology 2009, 137:297-308. (308 e291-294).
28. Takami T., Kaposi-Novak P., Uchida K., Gomez-Quiroz L.E., Conner E.A., Factor V.M., Thorgeirsson S.S. Loss of hepatocyte growth factor/c-Met signaling pathway accelerates early stages of N-nitrosodiethylamine induced hepatocarcinogenesis. Cancer Res. 2007, 67:9844-9851.
29. Ishikawa T., Factor V.M., Marquardt J.U., Raggi C., Seo D., Kitade M., Conner E.A., Thorgeirsson S.S. Hepatocyte growth factor (HGF)/c-Met signaling is required for stem cell mediated liver regeneration. Hepatology 2011 Nov 16, [Epub ahead of print]. 10.1002/hep.24796.
30. Moreira R.K. Hepatic stellate cells and liver fibrosis. Arch. Pathol. Lab. Med. 2007, 131:1728-1734.
31. Han X., Sterling H., Chen Y., Saginario C., Brown E.J., Frazier W.A., Lindberg F.P., Vignery A. CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J. Biol. Chem. 2000, 275:37984-37992.
32. De Minicis S., Bataller R., Brenner D.A. NADPH oxidase in the liver: defensive, offensive, or fibrogenic?. Gastroenterology 2006, 131:272-275.
33. Kisseleva T., Brenner D.A. Fibrogenesis of parenchymal organs. Proc. Am. Thorac. Soc. 2008, 5:338-342.
34. Novo E., Parola M. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 2008, 1:5.
35. Sanchez A., Alvarez A.M., Benito M., Fabregat I. Transforming growth factor beta modulates growth and differentiation of fetal hepatocytes in primary culture. J. Cell. Physiol. 1995, 165:398-405.
36. Ramadori G., Neubauer K., Odenthal M., Nakamura T., Knittel T., Schwogler S., Meyer zum Buschenfelde K.H. The gene of hepatocyte growth factor is expressed in fat-storing cells of rat liver and is downregulated during cell growth and by transforming growth factor-beta. Biochem. Biophys. Res. Commun. 1992, 183:739-742.
37. Nakamura T., Tomita Y., Hirai R., Yamaoka K., Kaji K., Ichihara A. Inhibitory effect of transforming growth factor-beta on DNA synthesis of adult rat hepatocytes in primary culture. Biochem. Biophys. Res. Commun. 1985, 133:1042-1050.
38. Factor V.M., Seo D., Ishikawa T., Kaposi-Novak P., Marquardt J.U., Andersen J.B., Conner E.A., Thorgeirsson S.S. Loss of c-Met disrupts gene expression program required for G2/M progression during liver regeneration in mice. PLoS One 2010, 5.
39. Klaassen C.D., Aleksunes L.M. Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol. Rev. 2010, 62:1-96.
40. Katzmann D.J., Odorizzi G., Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 2002, 3:893-905.
41. Ramakrishna S., Suresh B., Baek K.H. The role of deubiquitinating enzymes in apoptosis. Cell. Mol. Life Sci. 2011, 68:15-26.
42. Lappano R., Maggiolini M. G protein-coupled receptors: novel targets for drug discovery in cancer. Nat. Rev. Drug Discov. 2011, 10:47-60.
43. Fan C., Fu Z., Su Q., Angelini D.J., Van Eyk J., Johns R.A. S100A11 mediates hypoxia-induced mitogenic factor (HIMF)-induced smooth muscle cell migration, vesicular exocytosis, and nuclear activation. Mol. Cell. Proteomics 2011, 10. (M110 000901).
44. Mastrodonato M., Calamita G., Rossi R., Mentino D., Bonfrate L., Portincasa P., Ferri D., Liquori G.E. Altered distribution of caveolin-1 in early liver steatosis. Eur. J. Clin. Invest. 2011, 41:642-651.
45. Xia J.L., Dai C., Michalopoulos G.K., Liu Y. Hepatocyte growth factor attenuates liver fibrosis induced by bile duct ligation. Am. J. Pathol. 2006, 168:1500-1512.
46. Dambach D.M., Watson L.M., Gray K.R., Durham S.K., Laskin D.L. Role of CCR2 in macrophage migration into the liver during acetaminophen-induced hepatotoxicity in the mouse. Hepatology 2002, 35:1093-1103.
47. Kyriakides T.R., Foster M.J., Keeney G.E., Tsai A., Giachelli C.M., Clark-Lewis I., Rollins B.J., Bornstein P. The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 2004, 165:2157-2166.
48. Kirovski G., Gabele E., Dorn C., Moleda L., Niessen C., Weiss T.S., Wobser H., Schacherer D., Buechler C., Wasmuth H.E., Hellerbrand C. Hepatic steatosis causes induction of the chemokine RANTES in the absence of significant hepatic inflammation. Int. J. Clin. Exp. Pathol. 2010, 3:675-680.
49. Giannopoulou M., Dai C., Tan X., Wen X., Michalopoulos G.K., Liu Y. Hepatocyte growth factor exerts its anti-inflammatory action by disrupting nuclear factor-kappaB signaling. Am. J. Pathol. 2008, 173:30-41.
50. Gong R., Rifai A., Tolbert E.M., Biswas P., Centracchio J.N., Dworkin L.D. Hepatocyte growth factor ameliorates renal interstitial inflammation in rat remnant kidney by modulating tubular expression of macrophage chemoattractant protein-1 and RANTES. J. Am. Soc. Nephrol. 2004, 15:2868-2881.
51. Berres M.L., Trautwein C., Schmeding M., Eurich D., Tacke F., Bahra M., Neuhaus P., Neumann U.P., Wasmuth H.E. Serum chemokine CXC ligand 10 (CXCL10) predicts fibrosis progression after liver transplantation for hepatitis C infection. Hepatology 2011, 53:596-603.
52. Harvey C.E., Post J.J., Palladinetti P., Freeman A.J., Ffrench R.A., Kumar R.K., Marinos G., Lloyd A.R. Expression of the chemokine IP-10 (CXCL10) by hepatocytes in chronic hepatitis C virus infection correlates with histological severity and lobular inflammation. J. Leukoc. Biol. 2003, 74:360-369.
53. Hintermann E., Bayer M., Pfeilschifter J.M., Luster A.D., Christen U. CXCL10 promotes liver fibrosis by prevention of NK cell mediated hepatic stellate cell inactivation. J. Autoimmun. 2010, 35:424-435.
54. Hui A.Y., Friedman S.L. Molecular basis of hepatic fibrosis. Expert Rev. Mol. Med. 2003, 5:1-23.
55. Ghiassi-Nejad Z., Friedman S.L. Advances in antifibrotic therapy. Expert Rev. Gastroenterol. Hepatol. 2008, 2:803-816.