Loss of Gab1 adaptor protein in hepatocytes aggravates experimental liver fibrosis in mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 308, Issue 7, 2015, Pages G613-G624

  Kizu, Takashi ^a   Yoshida, Yuichi ^a   Furuta, Kunimaro ^a   Ogura, Satoshi ^a   Egawa, Mayumi ^a   Chatani, Norihiro ^a   Hamano, Mina ^a   Takemura, Takayo ^a   Ezaki, Hisao ^a   Kamada, Yoshihiro ^a   Nishida, Keigo ^b   Nakaoka, Yoshikazu ^a   Kiso, Shinichi ^a   Takehara, Tetsuo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

Bile duct ligation; Chemokine (C C motif) ligand 5; Cholestasis; Grb2 associated binder 1

Indexed keywords

ADAPTOR PROTEIN; CARBON TETRACHLORIDE; CHEMOKINE; COMPLEMENTARY DNA; GAB1 PROTEIN; LIPOPOLYSACCHARIDE; LIVER PROTEIN; UNCLASSIFIED DRUG; AUTACOID; CCL5 PROTEIN, MOUSE; GAB1 PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHOPROTEIN; RANTES;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; FIBROGENESIS; HEPATITIS; IN VITRO STUDY; LIVER CELL; LIVER FIBROSIS; MICROARRAY ANALYSIS; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; DEFICIENCY; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; GENETICS; KNOCKOUT MOUSE; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARBON TETRACHLORIDE; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CCL5; DRUG-INDUCED LIVER INJURY; HEPATOCYTES; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84929625896     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00289.2014     Document Type: Article

References (45)

1. Appay V, Rowland-Jones SL. RANTES: A versatile and controversial chemokine. Trends Immunol 22: 83–87, 2001.
2. Bard-Chapeau EA, Yuan J, Droin N, Long S, Zhang EE, Nguyen TV, Feng GS. Concerted functions of Gab1 and Shp2 in liver regeneration and hepatoprotection. Mol Cell Biol 26: 4664–4674, 2006.
3. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 115: 209–218, 2005.
4. Berres ML, Koenen RR, Rueland A, Zaldivar MM, Heinrichs D, Sahin H, Schmitz P, Streetz KL, Berg T, Gassler N, Weiskirchen R, Proudfoot A, Weber C, Trautwein C, Wasmuth HE. Antagonism of the chemokine Ccl5 ameliorates experimental liver fibrosis in mice. J Clin Invest 120: 4129–4140, 2010.
5. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376: 768–771, 1995.
6. Butcher BA, Greene RI, Henry SC, Annecharico KL, Weinberg JB, Denkers EY, Sher A, Taylor GA. P47 GTPases regulate Toxoplasma gondii survival in activated macrophages. Infect Immun 73: 3278–3286, 2005.
7. Clayton E, Forbes SJ. The isolation and in vitro expansion of hepatic Sca-1 progenitor cells. Biochem Biophys Res Commun 381: 549–553, 2009.
8. Ebihara T, Azuma M, Oshiumi H, Kasamatsu J, Iwabuchi K, Matsumoto K, Saito H, Taniguchi T, Matsumoto M, Seya T. Identification of a polyI:C-inducible membrane protein that participates in dendritic cellmediated natural killer cell activation. J Exp Med 207: 2675–2687, 2010.
9. Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology 134: 1655–1669, 2008.
10. Georgiev P, Jochum W, Heinrich S, Jang JH, Nocito A, Dahm F, Clavien PA. Characterization of time-related changes after experimental bile duct ligation. Br J Surg 95: 646–656, 2008.
11. Godoy P, Cadenas C, Hellwig B, Marchan R, Stewart J, Reif R, Lohr M, Gehrmann M, Rahnenfuhrer J, Schmidt M, Hengstler JG. Interferon- inducible guanylate binding protein (GBP2) is associated with better prognosis in breast cancer and indicates an efficient T cell response. Breast Cancer 21: 491–499, 2014.
12. Holgado-Madruga M, Emlet DR, Moscatello DK, Godwin AK, Wong AJ. A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature 379: 560–564, 1996.
13. Holmes C, Stanford WL. Concise review: stem cell antigen-1: Expression, function, and enigma. Stem cells 25: 1339–1347, 2007.
14. Huang G, Besner GE, Brigstock DR. Heparin-binding epidermal growth factor-like growth factor suppresses experimental liver fibrosis in mice. Lab Invest 92: 703–712, 2012.
15. Itoh M, Yoshida Y, Nishida K, Narimatsu M, Hibi M, Hirano T. Role of Gab1 in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol Cell Biol 20: 3695–3704, 2000.
16. Jia L, Vianna CR, Fukuda M, Berglund ED, Liu C, Tao C, Sun K, Liu T, Harper MJ, Lee CE, Lee S, Scherer PE, Elmquist JK. Hepatocyte Toll-like receptor 4 regulates obesity-induced inflammation and insulin resistance (Abstract). Nat Commun 5: 3878, 2014.
17. Julia A, Domenech E, Chaparro M, Garcia-Sanchez V, Gomollon F, Panes J, Manosa M, Barreiro-De Acosta M, Gutierrez A, Garcia- Planella E, Aguas M, Munoz F, Esteve M, Mendoza JL, Vera M, Marquez L, Tortosa R, Lopez-Lasanta M, Alonso A, Gelpi JL, Garcia- Montero AC, Bertranpetit J, Absher D, Myers RM, Gisbert JP, Marsal S. A genome-wide association study identifies a novel locus at 6q22.1 associated with ulcerative colitis. Hum Mol Genet 23: 6927–6934, 2014.
18. Katsounas A, Trippler M, Wang B, Polis M, Lempicki RA, Kottilil S, Gerken G, Schlaak JF. CCL5 mRNA is a marker for early fibrosis in chronic hepatitis C and is regulated by interferon-alpha therapy and toll-like receptor 3 signalling. J Viral Hep 19: 128–137, 2012.
19. Kobayashi S, Nagano H, Marubashi S, Hama N, Eguchi TA, Takeda Y, Tanemura M, Doki Y, Mori M. Guanylate-binding protein 2 mRNA in peripheral blood leukocytes of liver transplant recipients as a marker for acute cellular rejection. Transpl Int 23: 390–396, 2010.
20. Kodama T, Takehara T, Hikita H, Shimizu S, Shigekawa M, Tsunematsu H, Li W, Miyagi T, Hosui A, Tatsumi T, Ishida H, Kanto T, Hiramatsu N, Kubota S, Takigawa M, Tomimaru Y, Tomokuni A, Nagano H, Doki Y, Mori M, Hayashi N. Increases in p53 expression induce CTGF synthesis by mouse and human hepatocytes and result in liver fibrosis in mice. J Clin Invest 121: 3343–3356, 2011.
21. Luetteke NC, Qiu TH, Peiffer RL, Oliver P, Smithies O, Lee DC. TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 73: 263–278, 1993.
22. Mann GB, Fowler KJ, Gabriel A, Nice EC, Williams RL, Dunn AR. Mice with a null mutation of the TGF alpha gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 73: 249–261, 1993.
23. Marquardt JU, Seo D, Gomez-Quiroz LE, Uchida K, Gillen MC, Kitade M, Kaposi-Novak P, Conner EA, Factor VM, Thorgeirsson SS. Loss of c-Met accelerates development of liver fibrosis in response to CCl(4) exposure through deregulation of multiple molecular pathways. Biochim Biophys Acta 1822: 942–951, 2012.
24. Nakaoka Y, Komuro I. Gab docking proteins in cardiovascular disease, cancer, and inflammation (Abstract). Int J Inflam 2013: 141068, 2013.
25. Nakaoka Y, Nishida K, Narimatsu M, Kamiya A, Minami T, Sawa H, Okawa K, Fujio Y, Koyama T, Maeda M, Sone M, Yamasaki S, Arai Y, Koh GY, Kodama T, Hirota H, Otsu K, Hirano T, Mochizuki N. Gab family proteins are essential for postnatal maintenance of cardiac function via neuregulin-1/ErbB signaling. J Clin Invest 117: 1771–1781, 2007.
26. Nelson PJ, Kim HT, Manning WC, Goralski TJ, Krensky AM. Genomic organization and transcriptional regulation of the RANTES chemokine gene. J Immunol 151: 2601–2612, 1993.
27. Nishida K, Hirano T. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci 94: 1029–1033, 2003.
28. Perugorria MJ, Latasa MU, Nicou A, Cartagena-Lirola H, Castillo J, Goni S, Vespasiani Gentilucci U, Zagami MG, Lotersztajn S, Prieto J, Berasain C, Avila MA. The epidermal growth factor receptor ligand amphiregulin participates in the development of mouse liver fibrosis. Hepatology 48: 1251–1261, 2008.
29. Proudfoot AE, Power CA, Hoogewerf AJ, Montjovent MO, Borlat F, Offord RE, Wells TN. Extension of recombinant human RANTES by the retention of the initiating methionine produces a potent antagonist. J Biol Chem 271: 2599–2603, 1996.
30. Raabe T, Riesgo-Escovar J, Liu X, Bausenwein BS, Deak P, Maroy P, Hafen E. DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell 85: 911–920, 1996.
31. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M, Gherardi E, Birchmeier C. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373: 699–702, 1995.
32. Schuppan D, Afdhal NH. Liver cirrhosis. Lancet 371: 838–851, 2008.
33. Scott MJ, Chen C, Sun Q, Billiar TR. Hepatocytes express functional NOD1 and NOD2 receptors: A role for NOD1 in hepatocyte CC and CXC chemokine production. J Hepatol 53: 693–701, 2010.
34. Seki E, De Minicis S, Gwak GY, Kluwe J, Inokuchi S, Bursill CA, Llovet JM, Brenner DA, Schwabe RF. CCR1 and CCR5 promote hepatic fibrosis in mice. J Clin Invest 119: 1858–1870, 2009.
35. Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, Schwabe RF. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 13: 1324–1332, 2007.
36. Shlomai A, Halfon P, Goldiner I, Zelber-Sagi S, Halpern Z, Oren R, Bruck R. Serum bile acid levels as a predictor for the severity of liver fibrosis in patients with chronic hepatitis C. J Viral Hep 20: 95–102, 2013.
37. Sobrevals L, Rodriguez C, Romero-Trevejo JL, Gondi G, Monreal I, Paneda A, Juanarena N, Arcelus S, Razquin N, Guembe L, Gonzalez- Aseguinolaza G, Prieto J, Fortes P. Insulin-like growth factor I gene transfer to cirrhotic liver induces fibrolysis and reduces fibrogenesis leading to cirrhosis reversion in rats. Hepatology 51: 912–921, 2010.
38. Sunami Y, Leithauser F, Gul S, Fiedler K, Guldiken N, Espenlaub S, Holzmann KH, Hipp N, Sindrilaru A, Luedde T, Baumann B, Wissel S, Kreppel F, Schneider M, Scharffetter-Kochanek K, Kochanek S, Strnad P, Wirth T. Hepatic activation of IKK/NFkappaB signaling induces liver fibrosis via macrophage-mediated chronic inflammation. Hepatology 56: 1117–1128, 2012.
39. Takahashi-Tezuka M, Yoshida Y, Fukada T, Ohtani T, Yamanaka Y, Nishida K, Nakajima K, Hibi M, Hirano T. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol Cell Biol 18: 4109–4117, 1998.
40. Takemura T, Yoshida Y, Kiso S, Kizu T, Furuta K, Ezaki H, Hamano M, Egawa M, Chatani N, Kamada Y, Imai Y, Higashiyama S, Iwamoto R, Mekada E, Takehara T. Conditional loss of heparin-binding EGF-like growth factor results in enhanced liver fibrosis after bile duct ligation in mice. Biochem Biophys Res Commun 437: 185–191, 2013.
41. Taylor GA, Collazo CM, Yap GS, Nguyen K, Gregorio TA, Taylor LS, Eagleson B, Secrest L, Southon EA, Reid SW, Tessarollo L, Bray M, McVicar DW, Komschlies KL, Young HA, Biron CA, Sher A, Vande Woude GF. Pathogen-specific loss of host resistance in mice lacking the IFNgamma- inducible gene IGTP. Proc Natl Acad Sci USA 97: 751–755, 2000.
42. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC. Targeted disruption of mouse EGF receptor: Effect of genetic background on mutant phenotype. Science 269: 230–234, 1995.
43. 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 5: 226–230, 1999.
44. Xia JL, Dai C, Michalopoulos GK, Liu Y. Hepatocyte growth factor attenuates liver fibrosis induced by bile duct ligation. Am J Pathol 168: 1500–1512, 2006.
45. Yamasaki S, Nishida K, Yoshida Y, Itoh M, Hibi M, Hirano T. Gab1 is required for EGF receptor signaling and the transformation by activated ErbB2. Oncogene 22: 1546–1556, 2003.