Insulin-like growth factor 1 enhances bile-duct proliferation and fibrosis in Abcb4-/- mice

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 6, 2013, Pages 697-704

  Sokolović, Aleksandar ^a   Rodriguez Ortigosa, Carlos M ^b   Bloemendaal, Lysbeth ten ^a   Oude Elferink, Ronald P J ^a   Prieto, Jesús ^b   Bosma, Piter J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Abcb4 mice; Cholangiocytes proliferation; IGF1; Liver fibrosis; Primary sclerosing cholangitis

Indexed keywords

SOMATOMEDIN C; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT; BILE DUCT DISEASE; BILE DUCT LIGATION; BILIARY TRACT FIBROSIS; CELL PROLIFERATION; CHOLESTASIS; CONTROLLED STUDY; DISEASE COURSE; FIBROGENESIS; GENE OVEREXPRESSION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LIVER FIBROSIS; LIVER FUNCTION; MACROPHAGE; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL LINE; CELL PROLIFERATION; CHOLESTASIS; CHRONIC DISEASE; COLLAGEN; EPITHELIUM; FIBROSIS; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, KNOCKOUT; P-GLYCOPROTEINS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE PLASMINOGEN ACTIVATOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 84875077491     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.02.005     Document Type: Article

References (47)

1. Selmi C., Zuin M., Gershwin M.E. The unfinished business of primary biliary cirrhosis. J. Hepatol. 2008, 49:451-460.
2. Weismuller T.J., Wedemeyer J., Kubicka S., Strassburg C.P., Manns M.P. The challenges in primary sclerosing cholangitis-aetiopathogenesis, autoimmunity, management and malignancy. J. Hepatol. 2008, 48(Suppl. 1):S38-S57.
3. Cohick W.S., Clemmons D.R. The insulin-like growth factors. Annu. Rev. Physiol. 1993, 55:131-153.
4. Sjogren K., Liu J.L., Blad K., Skrtic S., Vidal O., Wallenius V., LeRoith D., Tornell J., Isaksson O.G., Jansson J.O., Ohlsson C. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7088-7092.
5. Mohan S., Baylink D.J. IGF-binding proteins are multifunctional and act via IGF-dependent and -independent mechanisms. J. Endocrinol. 2002, 175:19-31.
6. Riedemann J., Macaulay V.M. IGF1R signalling and its inhibition. Endocr. Relat. Cancer 2006, 13(Suppl. 1):S33-S43.
7. Assy N., Pruzansky Y., Gaitini D., Shen O.Z., Hochberg Z., Baruch Y. Growth hormone-stimulated IGF-1 generation in cirrhosis reflects hepatocellular dysfunction. J. Hepatol. 2008, 49:34-42.
8. Caregaro L., Alberino F., Angeli P., Gatta A. Insulin-like growth factor 1 (IGF-1) in liver cirrhosis: a marker of hepatocellular dysfunction?. J. Hepatol. 1998, 29:342.
9. Castilla-Cortazar I., Garcia M., Muguerza B., Quiroga J., Perez R., Santidrian S., Prieto J. Hepatoprotective effects of insulin-like growth factor I in rats with carbon tetrachloride-induced cirrhosis. Gastroenterology 1997, 113:1682-1691.
10. Sobrevals L., Rodriguez C., Romero-Trevejo J.L., 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 2010, 51:912-921.
11. Conchillo M., de Knegt R.J., Payeras M., Quiroga J., Sangro B., Herrero J.I., Castilla-Cortazar I., Frystyk J., Flyvbjerg A., Yoshizawa C., Jansen P.L., Scharschmidt B., Prieto J. Insulin-like growth factor I (IGF-I) replacement therapy increases albumin concentration in liver cirrhosis: results of a pilot randomized controlled clinical trial. J. Hepatol. 2005, 43:630-636.
12. Alvaro D., Metalli V.D., Alpini G., Onori P., Franchitto A., Barbaro B., Glaser S.S., Francis H., Cantafora A., Blotta I., Attili A.F., Gaudio E. The intrahepatic biliary epithelium is a target of the growth hormone/insulin-like growth factor 1 axis. J. Hepatol. 2005, 43:875-883.
13. Gatto M., Drudi-Metalli V., Torrice A., Alpini G., Cantafora A., Blotta I., Alvaro D. Insulin-like growth factor-1 isoforms in rat hepatocytes and cholangiocytes and their involvement in protection against cholestatic injury. Lab. Invest. 2008, 88:986-994.
14. Oude Elferink R.P., Paulusma C.C. Function and pathophysiological importance of ABCB4 (MDR3 P-glycoprotein). Pflugers Arch. 2007, 453:601-610.
15. van Nieuwerk C.M., Groen A.K., Ottenhoff R., van W.M., van den Bergh, Weerman M.A., Tytgat G.N., Offerhaus J.J., Oude Elferink R.P. The role of bile salt composition in liver pathology of mdr2 (-/-) mice: differences between males and females. J. Hepatol. 1997, 26:138-145.
16. Fickert P., Fuchsbichler A., Wagner M., Zollner G., Kaser A., Tilg H., Krause R., Lammert F., Langner C., Zatloukal K., Marschall H.U., Denk H., Trauner M. Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 2004, 127:261-274.
17. Wang J., Niu W., Nikiforov Y., Naito S., Chernausek S., Witte D., LeRoith D., Strauch A., Fagin J.A. Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J. Clin. Invest. 1997, 100:1425-1439.
18. Mauad T.H., van Nieuwkerk C.M., Dingemans K.P., Smit J.J., Schinkel A.H., Notenboom R.G., van den Bergh Weerman M.A., Verkruisen R.P., Groen A.K., Oude Elferink R.P. Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am. J. Pathol. 1994, 145:1237-1245.
19. van W.R., de Waart D.R., Akman S., Krediet R.T. Assessment of peritoneal fibrosis by conventional light microscopy and hydroxyproline measurements. Perit. Dial. Int. 2004, 24:290-292.
20. Sokolovic A., Sokolovic M., Boers W., Elferink R.P., Bosma P.J. Insulin-like growth factor binding protein 5 enhances survival of LX2 human hepatic stellate cells. Fibrogenesis Tissue Repair 2010, 3:3.
21. Lekanne Deprez R.H., Fijnvandraat A.C., Ruijter J.M., Moorman A.F. Sensitivity and accuracy of quantitative real-time polymerase chain reaction using SYBR green I depends on cDNA synthesis conditions. Anal. Biochem. 2002, 307:63-69.
22. Ramakers C., Ruijter J.M., Deprez R.H.L., Moorman A.F.M. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 2003, 339:62-66.
23. Ruijter J.M., Ramakers C., Hoogaars W.M., Karlen Y., Bakker O., van den Hoff M.J., Moorman A.F. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009, 37:e45.
24. Sokolovic A., Montenegro-Miranda P.S., de Waart D.R., Cappai R.M., Duijst S., Sokolovic M., Bosma P.J. Overexpression of insulin like growth factor binding protein 5 reduces liver fibrosis in chronic cholangiopathy. Biochim. Biophys. Acta 2012, 1822:996-1003.
25. Latasa M.U., Gil-Puig C., Fernandez-Barrena M.G., Rodriguez-Ortigosa C.M., Banales J.M., Urtasun R., Goni S., Mendez M., Arcelus S., Juanarena N., Recio J.A., Lotersztajn S., Prieto J., Berasain C., Corrales F.J., Lecanda J., Avila M.A. Oral methylthioadenosine administration attenuates fibrosis and chronic liver disease progression in Mdr2-/- mice. PLoS One 2010, 5:e15690.
26. Sokolovic M., Wehkamp D., Sokolovic A., Vermeulen J., Gilhuijs-Pederson L.A., van Haaften R.I., Nikolsky Y., Evelo C.T., van Kampen A.H., Hakvoort T.B., Lamers W.H. Fasting induces a biphasic adaptive metabolic response in murine small intestine. BMC Genomics 2007, 8:361.
27. Sanz S., Pucilowska J.B., Liu S., Rodriguez-Ortigosa C.M., Lund P.K., Brenner D.A., Fuller C.R., Simmons J.G., Pardo A., Martinez-Chantar M.L., Fagin J.A., Prieto J. Expression of insulin-like growth factor I by activated hepatic stellate cells reduces fibrogenesis and enhances regeneration after liver injury. Gut 2005, 54:134-141.
28. Skrtic S., Wallenius V., Ekberg S., Brenzel A., Gressner A.M., Jansson J.O. Hepatocyte-stimulated expression of hepatocyte growth factor (HGF) in cultured rat hepatic stellate cells. J. Hepatol. 1999, 30:115-124.
29. Dimai H.P., Linkhart T.A., Linkhart S.G., Donahue L.R., Beamer W.G., Rosen C.J., Farley J.R., Baylink D.J. Alkaline phosphatase levels and osteoprogenitor cell numbers suggest bone formation may contribute to peak bone density differences between two inbred strains of mice. Bone 1998, 22:211-216.
30. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
31. Iredale J.P., Benyon R.C., Arthur M.J., Ferris W.F., Alcolado R., Winwood P.J., Clark N., Murphy G. Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology 1996, 24:176-184.
32. Murphy F.R., Issa R., Zhou X., Ratnarajah S., Nagase H., Arthur M.J., Benyon C., Iredale J.P. Inhibition of apoptosis of activated hepatic stellate cells by tissue inhibitor of metalloproteinase-1 is mediated via effects on matrix metalloproteinase inhibition: implications for reversibility of liver fibrosis. J. Biol. Chem. 2002, 277:11069-11076.
33. Hsiao Y., Zou T., Ling C.C., Hu H., Tao X.M., Song H.Y. Disruption of tissue-type plasminogen activator gene in mice aggravated liver fibrosis. J. Gastroenterol. Hepatol. 2008, 23:e258-e264.
34. Popov Y., Patsenker E., Fickert P., Trauner M., Schuppan D. Mdr2 (Abcb4)-/- mice spontaneously develop severe biliary fibrosis via massive dysregulation of pro- and antifibrogenic genes. J. Hepatol. 2005, 43:1045-1054.
35. Hemmann S., Graf J., Roderfeld M., Roeb E. Expression of MMPs and TIMPs in liver fibrosis - a systematic review with special emphasis on anti-fibrotic strategies. J. Hepatol. 2007, 46:955-975.
36. Li Y.Y., McTiernan C.F., Feldman A.M. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc. Res. 2000, 46:214-224.
37. Nagase H., Woessner J.F. Matrix metalloproteinases. J. Biol. Chem. 1999, 274:21491-21494.
38. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
39. Onori P., Alvaro D., Floreani A.R., Mancino M.G., Franchitto A., Guido M., Carpino G., De S.A., Angelico M., Attili A.F., Gaudio E. Activation of the IGF1 system characterizes cholangiocyte survival during progression of primary biliary cirrhosis. J. Histochem. Cytochem. 2007, 55:327-334.
40. Cadoret A., Rey C., Wendum D., Elriz K., Tronche F., Holzenberger M., Housset C. IGF-1R contributes to stress-induced hepatocellular damage in experimental cholestasis. Am. J. Pathol. 2009, 175:627-635.
41. 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.
42. Fabris L., Strazzabosco M. Epithelial-mesenchymal interactions in biliary diseases. Semin. Liver Dis. 2011, 31:11-32.
43. Kalluri R., Neilson E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 2003, 112:1776-1784.
44. Spirli C., Okolicsanyi S., Fiorotto R., Fabris L., Cadamuro M., Lecchi S., Tian X., Somlo S., Strazzabosco M. Mammalian target of rapamycin regulates vascular endothelial growth factor-dependent liver cyst growth in polycystin-2-defective mice. Hepatology 2010, 51:1778-1788.
45. Hulzebos C.V., Voshol P.J., Wolters H., Kruit J.K., Ottenhof R., Groen A.K., Stellaard F., Verkade H.J., Kuipers F. Bile duct proliferation associated with bile salt-induced hypercholeresis in Mdr2 P-glycoprotein-deficient mice. Liver Int. 2005, 25:604-612.
46. Boers W., Aarrass S., Linthorst C., Pinzani M., Elferink R.O., Bosma P. Transcriptional profiling reveals novel markers of liver fibrogenesis: gremlin and insulin-like growth factor-binding proteins. J. Biol. Chem. 2006, 281:16289-16295.
47. Trauner M., Fickert P., Wagner M. MDR3 (ABCB4) defects: a paradigm for the genetics of adult cholestatic syndromes. Semin. Liver Dis. 2007, 27:77-98.