Mutant MMP-9 and HGF gene transfer enhance resolution of CCL4-induced liver fibrosis in rats: Role of ASH1 and EZH2 methyltransferases repression

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Atta, Hussein ^a   El Rehany, Mahmoud ^a   Hammam, Olfat ^b   Abdel Ghany, Hend ^a   Ramzy, Maggie ^a   Roderfeld, Martin ^c   Roeb, Elke ^c   Al Hendy, Ayman ^d   Raheim, Salama Abdel ^a   Allam, Hatem ^a   Marey, Heba ^a  

^a Minia University   (Egypt)

^b Imbaba   (Egypt)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSENT SMALL HOMEOTIC DISC 1 PROTEIN; ADENOVIRUS VECTOR; ALANINE AMINOTRANSFERASE; ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; CYCLINE; GELATINASE B; HISTONE METHYLTRANSFERASE; HYDROXYPROLINE; MESSENGER RNA; SCATTER FACTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR EZH2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ACTIN; ASH1L PROTEIN, RAT; CARBON TETRACHLORIDE; COLLAGEN TYPE 1; COLLAGEN TYPE I, ALPHA 1 CHAIN; EZH2 PROTEIN, RAT; HGF PROTEIN, HUMAN; HISTONE LYSINE METHYLTRANSFERASE; METHYLTRANSFERASE; MUTANT PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; FIBROGENESIS; GELATINASE B GENE; GENE EXPRESSION; LIVER FIBROSIS; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SCATTER FACTOR GENE; TRANSFORMING GROWTH FACTOR BETA1 GENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ADENOVIRIDAE; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; HUMAN; LIVER CIRRHOSIS, EXPERIMENTAL; METABOLISM; MUTATION; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE; WISTAR RAT;

RATTUS;

ACTINS; ADENOVIRIDAE; ANIMALS; CARBON TETRACHLORIDE; COLLAGEN TYPE I; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HEPATOCYTE GROWTH FACTOR; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; LIVER CIRRHOSIS, EXPERIMENTAL; MALE; MATRIX METALLOPROTEINASE 9; METHYLTRANSFERASES; MUSCLE, SMOOTH; MUTANT PROTEINS; MUTATION; POLYCOMB REPRESSIVE COMPLEX 2; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84911425320     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112384     Document Type: Article

References (60)

1. Tsochatzis EA, Bosch J, Burroughs AK (2012) New therapeutic paradigm for patients with cirrhosis. Hepatology 56: 1983-1992.
2. Prosser CC, Yen RD, Wu J (2006) Molecular therapy for hepatic injury and fibrosis: where are we? World J Gastroenterol 12: 509-515.
3. Iredale JP, Benyon RC, Arthur MJ, Ferris WF, Alcolado R, et al. (1996) Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology 24: 176-184.
4. Cohen-Naftaly M, Friedman SL (2011) Current status of novel antifibrotic therapies in patients with chronic liver disease. Therap Adv Gastroenterol 4: 391-417.
5. Iredale JP, Benyon RC, Pickering J, McCullen M, Northrop M, et al. (1998) Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 102: 538-549.
6. Roderfeld M, Weiskirchen R, Wagner S, Berres ML, Henkel C, et al. (2006) Inhibition of hepatic fibrogenesis by matrix metalloproteinase-9 mutants in mice. FASEB J 20: 444-454.
7. Murphy FR, Issa R, Zhou X, Ratnarajah S, Nagase H, et al. (2002) Inhibition of apoptosis of activated hepatic stellate cells by tissue inhibitor of metalloprotei-nase-1 is mediated via effects on matrix metalloproteinase inhibition: implications for reversibility of liver fibrosis. J Biol Chem 277: 11069-11076.
8. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, et al. (2002) Tissue inhibitor of metalloproteinases-1 attenuates spontaneous liver fibrosis resolution in the transgenic mouse. Hepatology 36: 850-860.
9. Murphy G, Willenbrock F, Crabbe T, O'Shea M, Ward R, et al. (1994) Regulation of matrix metalloproteinase activity. Ann N Y Acad Sci 732: 31-41.
10. O'Connell JP, Willenbrock F, Docherty AJ, Eaton D, Murphy G (1994) Analysis of the role of the COOH-terminal domain in the activation, proteolytic activity, and tissue inhibitor of metalloproteinase interactions of gelatinase B. J Biol Chem 269: 14967-14973.
11. Roeb E, Behrmann I, Grotzinger J, Breuer B, Matern S (2000) An MMP-9 mutant without gelatinolytic activity as a novel TIMP-1-antagonist. FASEB J 14: 1671-1673.
12. Boros P, Miller CM (1995) Hepatocyte growth factor: a multifunctional cytokine. Lancet 345: 293-295.
13. Atta HM, Al-Hendy A, Salama SA, Shaker OG, Hammam OA (2009) Lowdose simultaneous delivery of adenovirus encoding hepatocyte growth factor and vascular endothelial growth factor in dogs enhances liver proliferation without systemic growth factor elevation. Liver Int 29: 1022-1030.
14. Fujiwara K, Nagoshi S, Ohno A, Hirata K, Ohta Y, et al. (1993) Stimulation of liver growth by exogenous human hepatocyte growth factor in normal and partially hepatectomized rats. Hepatology 18: 1443-1449.
15. Matsuda Y, Matsumoto K, Yamada A, Ichida T, Asakura H, et al. (1997) Preventive and therapeutic effects in rats of hepatocyte growth factor infusion on liver fibrosis/cirrhosis. Hepatology 26: 81-89.
16. Oe H, Kaido T, Furuyama H, Mori A, Imamura M (2004) Simultaneous transfer of vascular endothelial growth factor and hepatocyte growth factor genes effectively promotes liver regeneration after hepatectomy in cirrhotic rats. Hepatogastroenterology 51: 1641-1647.
17. Yasuda H, Imai E, Shiota A, Fujise N, Morinaga T, et al. (1996) Antifibrogenic effect of a deletion variant of hepatocyte growth factor on liver fibrosis in rats. Hepatology 24: 636-642.
18. Ueno M, Uchiyama K, Nakamori M, Ueda K, Iwahashi M, et al. (2007) Adenoviral vector expressing hepatocyte growth factor promotes liver regeneration by preoperative injection: the advantages of performing selective injection to the remnant lobe. Surgery 141: 511-519.
19. Ishiki Y, Ohnishi H, Muto Y, Matsumoto K, Nakamura T (1992) Direct evidence that hepatocyte growth factor is a hepatotrophic factor for liver regeneration and has a potent antihepatitis effect in vivo. Hepatology 16: 1227-1235.
20. Seto S, Kaido T, Yamaoka S, Yoshikawa A, Arii S, et al. (1998) Hepatocyte growth factor prevents lipopolysaccharide-induced hepatic sinusoidal endothelial cell injury and intrasinusoidal fibrin deposition in rats. J Surg Res 80: 194-199.
21. Phaneuf D, Chen SJ, Wilson JM (2000) Intravenous injection of an adenovirus encoding hepatocyte growth factor results in liver growth and has a protective effect against apoptosis. Mol Med 6: 96-103.
22. Nishino M, Iimuro Y, Ueki T, Hirano T, Fujimoto J (2008) Hepatocyte growth factor improves survival after partial hepatectomy in cirrhotic rats suppressing apoptosis of hepatocytes. Surgery 144: 374-384.
23. Nomi T, Shiota G, Isono M, Sato K, Kawasaki H (2000) Adenovirus-mediated hepatocyte growth factor gene transfer prevents lethal liver failure in rats. Biochem Biophys Res Commun 278: 338-343.
24. Ueki T, Kaneda Y, Tsutsui H, Nakanishi K, Sawa Y, et al. (1999) Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat Med 5: 226-230.
25. Liu Y, Rajur K, Tolbert E, Dworkin LD (2000) Endogenous hepatocyte growth factor ameliorates chronic renal injury by activating matrix degradation pathways. Kidney Int 58: 2028-2043.
26. Gregory GD, Vakoc CR, Rozovskaia T, Zheng X, Patel S, et al. (2007) Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Mol Cell Biol 27: 8466-8479.
27. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, et al. (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411.
28. Perugorria MJ, Wilson CL, Zeybel M, Walsh M, Amin S, et al. (2012) Histone methyltransferase ASH1 orchestrates fibrogenic gene transcription during myofibroblast transdifferentiation. Hepatology 56: 1129-1139.
29. Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14: 155-164.
30. Yu YL, Su KJ, Hsieh YH, Lee HL, Chen TY, et al. (2013) Effects of EZH2 polymorphisms on susceptibility to and pathological development of hepatocellular carcinoma. PLoS One 8: e74870.
31. Xie G, Diehl AM (2013) Evidence for and against epithelial-to-mesenchymal transition in the liver. Am J Physiol Gastrointest Liver Physiol 305: G881-890.
32. Mann J, Chu DC, Maxwell A, Oakley F, Zhu NL, et al. (2010) MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterology 138: 705-714.
33. Zeybel M, Mann DA, Mann J (2013) Epigenetic modifications as new targets for liver disease therapies. J Hepatol 59: 1349-1353.
34. Al-Hendy A, Magliocco AM, Al-Tweigeri T, Braileanu G, Crellin N, et al. (2000) Ovarian cancer gene therapy: repeated treatment with thymidine kinase in an adenovirus vector and ganciclovir improves survival in a novel immunocompetent murine model. Am J Obstet Gynecol 182: 553-559.
35. Iredale JP (2007) Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest 117: 539-548.
36. Popov Y, Schuppan D (2009) Targeting liver fibrosis: strategies for development and validation of antifibrotic therapies. Hepatology 50: 1294-1306.
37. Ozawa S, Uchiyama K, Nakamori M, Ueda K, Iwahashi M, et al. (2006) Combination gene therapy of HGF and truncated type II TGF-beta receptor for rat liver cirrhosis after partial hepatectomy. Surgery 139: 563-573.
38. Peterson GL (1983) Determination of total protein. Methods Enzymol 91: 95-119.
39. Batts KP, Ludwig J (1995) Chronic hepatitis. An update on terminology and reporting. Am J Surg Pathol 19: 1409-1417.
40. Li L, Hu Z, Li W, Hu M, Ran J, et al. (2012) Establishment of a standardized liver fibrosis model with different pathological stages in rats. Gastroenterol Res Pract 2012: 560345.
41. Takahara T, Furui K, Funaki J, Nakayama Y, Itoh H, et al. (1995) Increased expression of matrix metalloproteinase-II in experimental liver fibrosis in rats. Hepatology 21: 787-795.
42. Lee HS, Huang GT, Miau LH, Chiou LL, Chen CH, et al. (2001) Expression of matrix metalloproteinases in spontaneous regression of liver fibrosis. Hepatogastroenterology 48: 1114-1117.
43. Liu J, Cheng X, Guo Z, Wang Z, Li D, et al. (2013) Truncated active human matrix metalloproteinase-8 delivered by a chimeric adenovirus-hepatitis B virus vector ameliorates rat liver cirrhosis. PLoS One 8: e53392.
44. Liu WB, Yang CQ, Jiang W, Wang YQ, Guo JS, et al. (2003) Inhibition on the production of collagen type I, III of activated hepatic stellate cells by antisense TIMP-1 recombinant plasmid. World J Gastroenterol 9: 316-319.
45. Parsons CJ, Bradford BU, Pan CQ, Cheung E, Schauer M, et al. (2004) Antifibrotic effects of a tissue inhibitor of metalloproteinase-1 antibody on established liver fibrosis in rats. Hepatology 40: 1106-1115.
46. Inagaki Y, Higashi K, Kushida M, Hong YY, Nakao S, et al. (2008) Hepatocyte growth factor suppresses profibrogenic signal transduction via nuclear export of Smad3 with galectin-7. Gastroenterology 134: 1180-1190.
47. Kim WH, Matsumoto K, Bessho K, Nakamura T (2005) Growth inhibition and apoptosis in liver myofibroblasts promoted by hepatocyte growth factor leads to resolution from liver cirrhosis. Am J Pathol 166: 1017-1028.
48. Inoue H, Yokoyama F, Kita Y, Yoshiji H, Tsujimoto T, et al. (2006)Relationship between the proliferative capability of hepatocytes and the intrahepatic expression of hepatocyte growth factor and c-Met in the course of cirrhosis development in rats. Int J Mol Med 17: 857-864.
49. D'Errico A, Fiorentino M, Ponzetto A, Daikuhara Y, Tsubouchi H, et al. (1996)Liver hepatocyte growth factor does not always correlate with hepatocellular proliferation in human liver lesions: its specific receptor c-met does. Hepatology 24: 60-64.
50. Liu Y, Centracchio JN, Lin L, Sun AM, Dworkin LD (1998) Constitutive expression of HGF modulates renal epithelial cell phenotype and induces c-met and fibronectin expression. Exp Cell Res 242: 174-185.
51. Rampino T, Cancarini G, Gregorini M, Guallini P, Maggio M, et al. (2001)Hepatocyte growth factor/scatter factor released during peritonitis is active on mesothelial cells. Am J Pathol 159: 1275-1285.
52. He CJ, Striker LJ, Tsokos M, Yang CW, Peten EP, et al. (1995) Relationships between mesangial cell proliferation and types I and IV collagen mRNA levels in vitro. Am J Physiol 269: C554-562.
53. Flaumenhaft R, Rifkin DB (1992) The extracellular regulation of growth factor action. Mol Biol Cell 3: 1057-1065.
54. Esposito C, Parrilla B, Cornacchia F, Grosjean F, Mangione F, et al. (2009) The antifibrogenic effect of hepatocyte growth factor (HGF) on renal tubular (HK-2)cells is dependent on cell growth. Growth Factors 27: 173-180.
55. Kusumoto K, Ido A, Moriuchi A, Katsura T, Kim I, et al. (2006) Repeated intravenous injection of recombinant human hepatocyte growth factor ameliorates liver cirrhosis but causes albuminuria in rats. Int J Mol Med 17: 503-509.
56. Mizuno S, Ikebuchi F, Fukuta K, Kato T, Matsumoto K, et al. (2011) Recombinant human HGF, but not rat HGF, elicits glomerular injury and albuminuria in normal rats via an immune complex-dependent mechanism. Clin Exp Pharmacol Physiol 38: 192-201.
57. Tashiro K, Hagiya M, Nishizawa T, Seki T, Shimonishi M, et al. (1990) Deduced primary structure of rat hepatocyte growth factor and expression of the mRNA in rat tissues. Proc Natl Acad Sci U S A 87: 3200-3204.
58. Volkel P, Angrand PO (2007) The control of histone lysine methylation in epigenetic regulation. Biochimie 89: 1-20.
59. Hazra S, Xiong S, Wang J, Rippe RA, Krishna V, et al. (2004) Peroxisome proliferator-activated receptor gamma induces a phenotypic switch from activated to quiescent hepatic stellate cells. J Biol Chem 279: 11392-11401.
60. Yang MD, Chiang YM, Higashiyama R, Asahina K, Mann DA, et al. (2012) Rosmarinic acid and baicalin epigenetically derepress peroxisomal proliferatoractivated receptor gamma in hepatic stellate cells for their antifibrotic effect. Hepatology 55: 1271-1281.