Induction of heme oxygenase 1 prevents progression of liver fibrosis in Mdr2 knockout mice

Hepatology

Volumn 55, Issue 2, 2012, Pages 553-562

  Barikbin, Roja ^a   Neureiter, Daniel ^b   Wirth, Jan ^a   Erhardt, Annette ^a   Schwinge, Dorothee ^a   Kluwe, Johannes ^a   Schramm, Christoph ^a   Tiegs, Gisa ^a   Sass, Gabriele ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

HEME OXYGENASE 1; PROTOPORPHYRIN COBALT; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL INFILTRATION; CELL PROLIFERATION; CHRONIC HEPATITIS; CONTROLLED STUDY; DISEASE COURSE; DYSPLASIA; ENZYME INDUCTION; FEMALE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; LIFESPAN; LIVER CELL CARCINOMA; LIVER FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STELLATE CELL;

ANIMALS; CELL PROLIFERATION; DISEASE PROGRESSION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HEME OXYGENASE-1; LIVER CIRRHOSIS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; P-GLYCOPROTEINS; PHOSPHORYLATION; PROTOPORPHYRINS; RECEPTORS, TUMOR NECROSIS FACTOR;

EID: 84855505630     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24711     Document Type: Article

References (47)

1. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986; 261: 411-419.
2. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988; 2: 2557-2568.
3. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. [Review]. Biochem Pharmacol 2010; 80: 1895-1903.
4. Devey L, Mohr E, Bellamy C, Simpson K, Henderson N, Harrison EM, et al. c-Jun terminal kinase-2 gene deleted mice overexpress hemeoxygenase-1 and are protected from hepatic ischemia reperfusion injury. Transplantation 2009; 88: 308-316.
5. Woo J, Iyer S, Cornejo MC, Mori N, Gao L, Sipos I, et al. Stress protein-induced immunosuppression: inhibition of cellular immune effector functions following overexpression of haem oxygenase (HSP 32). Transpl Immunol 1998; 6: 84-93.
6. Devey L, Ferenbach D, Mohr E, Sangster K, Bellamy CO, Hughes J, et al. Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol Ther 2009; 17: 65-72.
7. Sass G, Seyfried S, Parreira Soares M, Yamashita K, Kaczmarek E, Neuhuber WL, et al. Cooperative effect of biliverdin and carbon monoxide on survival of mice in immune-mediated liver injury. HEPATOLOGY 2004; 40: 1128-1135.
8. Sass G, Soares MC, Yamashita K, Seyfried S, Zimmermann WH, Eschenhagen T, et al. Heme oxygenase-1 and its reaction product, carbon monoxide, prevent inflammation-related apoptotic liver damage in mice. HEPATOLOGY 2003; 38: 909-918.
9. Edmondson HA, Peters RL. Tumors of the liver: pathologic features. Semin Roentgenol 1983; 18: 75-83.
10. Sagmeister S, Eisenbauer M, Pirker C, Mohr T, Holzmann K, Zwickl H, et al. New cellular tools reveal complex epithelial-mesenchymal interactions in hepatocarcinogenesis. Br J Cancer 2008; 99: 151-159.
11. Mauad TH, van Nieuwkerk CM, Dingemans KP, Smit JJ, Schinkel AH, Notenboom RG, et al. 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.
12. Smit JJ, Schinkel AH, Oude Elferink RP, Groen AK, Wagenaar E, van Deemter L, et al. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 1993; 75: 451-462.
13. Katzenellenbogen M, Pappo O, Barash H, Klopstock N, Mizrahi L, Olam D, et al. Multiple adaptive mechanisms to chronic liver disease revealed at early stages of liver carcinogenesis in the Mdr2-knockout mice. Cancer Res 2006; 66: 4001-4010.
14. Friedman SL. Liver fibrosis-from bench to bedside. J Hepatol 2003; 38( Suppl 1): S38-S53.
15. Katzenellenbogen M, Mizrahi L, Pappo O, Klopstock N, Olam D, Barash H, et al. Molecular mechanisms of the chemopreventive effect on hepatocellular carcinoma development in Mdr2 knockout mice. Mol Cancer Ther 2007; 6: 1283-1291.
16. van Nieuwerk CM, Groen AK, Ottenhoff R, van Wijland M, van den Bergh Weerman MA, Tytgat GN, et al. The role of bile salt composition in liver pathology of mdr2 (-/-) mice: differences between males and females. J Hepatol 1997; 26: 138-145.
17. Bergmeyer HU. Methods of Enzymatic Analysis, 3rd ed. Weinheim, Germany: Verlag Chemie; 1984: 416-456.
18. Erhardt A, Wegscheid C, Claass B, Carambia A, Herkel J, Mittrücker HW, et al. CXCR3 deficiency exacerbates liver disease and abrogates tolerance in a mouse model of immune-mediated hepatitis. J Immunol 2011; 186: 5284-5293.
19. Kluwe J, Pradere JP, Gwak GY, Mencin A, De Minicis S, Osterreicher CH, et al. Modulation of hepatic fibrosis by c-Jun-N-terminal kinase inhibition. Gastroenterology 2010; 138: 347-359.
20. Lehmann E, El-Tantawy WH, Ocker M, Bartenschlager R, Lohmann V, Hashemolhosseini S, et al. The heme oxygenase 1 product biliverdin interferes with hepatitis C virus replication by increasing antiviral interferon response. HEPATOLOGY 2010; 51: 398-404.
21. Sass G, Shembade ND, Haimerl F, Lamoureux N, Hashemolhosseini S, Tannapfel A, et al. TNF pretreatment interferes with mitochondrial apoptosis in the mouse liver by A20-mediated down-regulation of Bax. J Immunol 2007; 179: 7042-7049.
22. Uchinami H, Seki E, Brenner DA, D'Armiento J. Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis. HEPATOLOGY 2006; 44: 420-429.
23. Libbrecht L, Desmet V, Roskams T. Preneoplastic lesions in human hepatocarcinogenesis. Liver Int 2005; 25: 16-27.
24. Churg J, Prado A. A rapid Mallory trichrome stain (chromotrope-aniline blue). AMA Arch Pathol 1956; 62: 505-506.
25. Beckstead JH, Halverson PS, Ries CA, Bainton DF. Enzyme histochemistry and immunohistochemistry on biopsy specimens of pathologic human bone marrow. Blood 1981; 57: 1088-1098.
26. Ramaiah SK, Rittling S. Pathophysiological role of osteopontin in hepatic inflammation, toxicity, and cancer. Toxicol Sci 2008; 103: 4-13.
27. Arthur MJ. Fibrogenesis II. Metalloproteinases and their inhibitors in liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2000; 279: G245-G249.
28. Martinez-Hernandez A, Amenta PS. The extracellular matrix in hepatic regeneration. FASEB J 1995; 9: 1401-1410.
29. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, at al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007; 317: 121-124.
30. Lee IT, Luo SF, Lee CW, Wang SW, Lin CC, Chang CC, et al. Overexpression of HO-1 protects against TNF-alpha-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress. Am J Pathol 2009; 175: 519-532.
31. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer 2003; 3: 276-285.
32. Beutler B, Cerami A. Cachectin/tumor necrosis factor: an endogenous mediator of shock and inflammation. Immunol Res 1986; 5: 281-293.
33. MacDonald TT, Hutchings P, Choy MY, Murch S, Cooke A. Tumour necrosis factor-alpha and interferon-gamma production measured at the single cell level in normal and inflamed human intestine. Clin Exp Immunol 1990; 81: 301-305.
34. González-Amaro R, García-Monzón C, García-Buey L, Moreno-Otero R, Alonso JL, Yagüe E, et al. Induction of tumor necrosis factor alpha production by human hepatocytes in chronic viral hepatitis. J Exp Med 1994; 179: 841-848.
35. Aderka D, Englemann H, Hornik V, Skornick Y, Levo Y, Wallach D, et al. Increased serum levels of soluble receptors for tumor necrosis factor in cancer patients. Cancer Res 1991; 51: 5602-5607.
36. Fickert P, Thueringer A, Moustafa T, Silbert D, Gumhold J, Tsybrovskyy O, et al. The role of osteopontin and tumor necrosis factor alpha receptor-1 in xenobiotic-induced cholangitis and biliary fibrosis in mice. Lab Invest 2010; 90: 844-852.
37. Théret N, Lehti K, Musso O, Clément B. MMP2 activation by collagen I and concanavalin A in cultured human hepatic stellate cells. HEPATOLOGY 1999; 30: 462-468.
38. Tsui TY, Lau CK, Ma J, Wu X, Wang YQ, Farkas S, et al. rAAV-mediated stable expression of heme oxygenase-1 in stellate cells: a new approach to attenuate liver fibrosis in rats. HEPATOLOGY 2005; 42: 335-342.
39. Iredale JP. Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest 2007; 117: 539-548.
40. Bansal R, Prakash J, Post E, Beljaars L, Schuppan D, Poelstra K. Novel engineered targeted interferon-gamma blocks hepatic fibrogenesis in mice. HEPATOLOGY 2011; 54: 586-596.
41. Schuppan D, Afdhal NH. Liver cirrhosis. Lancet 2008; 371: 838-851.
42. Brenner DA. Molecular pathogenesis of liver fibrosis. Trans Am Clin Climatol Assoc 2009; 120: 361-368.
43. Margadant C, Sonnenberg A. Integrin-TGF-beta crosstalk in fibrosis, cancer, and wound healing. EMBO Rep 2010; 11: 97-105.
44. Milani S, Herbst H, Schuppan D, Stein H, Surrenti C. Transforming growth factors beta 1 and beta 2 are differentially expressed in fibrotic liver disease. Am J Pathol 1991; 139: 1221-1229.
45. Hunter T, Pines J. Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age. Cell 1994; 79: 573-582.
46. Naryzhny SN. Proliferating cell nuclear antigen: a proteomics view. Cell Mol Life Sci 2008; 65: 3789-3808.
47. Sass G, Leukel P, Schmitz V, Raskopf E, Ocker M, Neureiter D, et al. Inhibition of heme oxygenase 1 expression by small interfering RNA decreases orthotopic tumor growth in livers of mice. Int J Cancer 2008; 123: 1269-1277.