Matrix metalloproteinases in liver injury, repair and fibrosis

Matrix Biology

Volumn 44-46, Issue , 2015, Pages 147-156

  Duarte, Sergio ^a   Baber, John ^a   Fujii, Takehiro ^a   Coito, Ana J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acute liver injury; Chronic liver injury; Extracellular matrix; Liver; Liver injury; Liver ischemia and reperfusion injury; Matrix metalloproteinases

Indexed keywords

GELATINASE B; MATRIX METALLOPROTEINASE; PROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

CHRONIC INFLAMMATION; CHRONIC LIVER DISEASE; DISEASE COURSE; EXTRACELLULAR MATRIX; HUMAN; LIVER FIBROSIS; LIVER INJURY; LIVER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ENZYMOLOGY; LIVER; LIVER DISEASE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; WOUND HEALING;

EXTRACELLULAR MATRIX; HUMANS; LIVER; LIVER DISEASES; MATRIX METALLOPROTEINASES; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASES; WOUND HEALING;

EID: 84930753614     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.01.004     Document Type: Review

References (112)

1. Protzer U., Maini M.K., Knolle P.A. Living in the liver: hepatic infections. Nat Rev Immunol 2012, 12:201-213.
2. Hernandez-Gea V., Friedman S.L. Pathogenesis of liver fibrosis. Annu Rev Pathol 2011, 6:425-456.
3. Si-Tayeb K., Lemaigre F.P., Duncan S.A. Organogenesis and development of the liver. Dev Cell 2010, 18:175-189.
4. Malhi H., Guicciardi M.E., Gores G.J. Hepatocyte death: a clear and present danger. Physiol Rev 2010, 90:1165-1194.
5. Fausto N. Liver regeneration. J Hepatol 2000, 32:19-31.
6. Diehl A.M., Chute J. Underlying potential: cellular and molecular determinants of adult liver repair. J Clin Invest 2013, 123:1858-1860.
7. Cox T.R., Erler J.T. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 2011, 4:165-178.
8. Friedman S.L., Maher J.J., Bissell D.M. Mechanisms and therapy of hepatic fibrosis: report of the AASLD Single Topic Basic Research Conference. Hepatology 2000, 32:1403-1408.
9. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
10. Gross J., Lapiere C.M. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci U S A 1962, 48:1014-1022.
11. Bourboulia D., Stetler-Stevenson W.G. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 2010, 20:161-168.
12. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004, 4:617-629.
13. Nissinen L., Kahari V.M. Matrix metalloproteinases in inflammation. Biochim Biophys Acta 1840, 2014:2571-2580.
14. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001, 17:463-516.
15. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003, 92:827-839.
16. Chirco R., Liu X.W., Jung K.K., Kim H.R. Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev 2006, 25:99-113.
17. Martin M.D., Matrisian L.M. The other side of MMPs: protective roles in tumor progression. Cancer Metastasis Rev 2007, 26:717-724.
18. Bjorklund M., Koivunen E. Gelatinase-mediated migration and invasion of cancer cells. Biochim Biophys Acta 2005, 1755:37-69.
19. Schwarzbauer J.E., Sechler J.L. Fibronectin fibrillogenesis: a paradigm for extracellular matrix assembly. Curr Opin Cell Biol 1999, 11:622-627.
20. Bedossa P., Paradis V. Liver extracellular matrix in health and disease. J Pathol 2003, 200:504-515.
21. Martinez-Hernandez A. The hepatic extracellular matrix. I. Electron immunohistochemical studies in normal rat liver. Lab Invest 1984, 51:57-74.
22. Martinez-Hernandez A., Amenta P.S. The extracellular matrix in hepatic regeneration. FASEB J 1995, 9:1401-1410.
23. Benyon R.C., Arthur M.J. Extracellular matrix degradation and the role of hepatic stellate cells. Semin Liver Dis 2001, 21:373-384.
24. Moore C., Shen X.D., Gao F., Busuttil R.W., Coito A.J. Fibronectin-alpha4beta1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am J Pathol 2007, 170:567-577.
25. Lichtinghagen R., Helmbrecht T., Arndt B., Boker K.H. Expression pattern of matrix metalloproteinases in human liver. Eur J Clin Chem Clin Biochem 1995, 33:65-71.
26. Milani S., Herbst H., Schuppan D., Grappone C., Pellegrini G., Pinzani M., et al. Differential expression of matrix-metalloproteinase-1 and -2 genes in normal and fibrotic human liver. Am J Pathol 1994, 144:528-537.
27. Hamada T., Fondevila C., Busuttil R.W., Coito A.J. Metalloproteinase-9 deficiency protects against hepatic ischemia/reperfusion injury. Hepatology 2008, 47:186-198.
28. Vu T.H., Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000, 14:2123-2133.
29. McQuibban G.A., Gong J.H., Wong J.P., Wallace J.L., Clark-Lewis I., Overall C.M. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 2002, 100:1160-1167.
30. Duarte S., Hamada T., Kuriyama N., Busuttil R.W., Coito A.J. TIMP-1 deficiency leads to lethal partial hepatic ischemia and reperfusion injury. Hepatology 2012, 56:1074-1085.
31. Murphy F.R., Issa R., Zhou X., Ratnarajah S., Nagase H., Arthur M.J., et al. 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.
32. Boulday G., Fitau J., Coupel S., Soulillou J.P., Charreau B. Exogenous tissue inhibitor of metalloproteinase-1 promotes endothelial cell survival through activation of the phosphatidylinositol 3-kinase/Akt pathway. Ann N Y Acad Sci 2004, 1030:28-36.
33. Murthy A., Shao Y.W., Defamie V., Wedeles C., Smookler D., Khokha R. Stromal TIMP3 regulates liver lymphocyte populations and provides protection against Th1 T cell-driven autoimmune hepatitis. J Immunol 2012, 188:2876-2883.
34. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury: present concepts. J Gastroenterol Hepatol 2011, 26(Suppl. 1):173-179.
35. Amersi F., Shen X.D., Moore C., Melinek J., Busuttil R.W., Kupiec-Weglinski J.W., et al. Fibronectin-alpha 4 beta 1 integrin-mediated blockade protects genetically fat Zucker rat livers from ischemia/reperfusion injury. Am J Pathol 2003, 162:1229-1239.
36. Kuriyama N., Duarte S., Hamada T., Busuttil R.W., Coito A.J. Tenascin-C: a novel mediator of hepatic ischemia and reperfusion injury. Hepatology 2011, 54:2125-2136.
37. Jarnagin W.R., Rockey D.C., Koteliansky V.E., Wang S.S., Bissell D.M. Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol 1994, 127:2037-2048.
38. Riordan S.M., Williams R. Mechanisms of hepatocyte injury, multiorgan failure, and prognostic criteria in acute liver failure. Semin Liver Dis 2003, 23:203-215.
39. Bernal W., Auzinger G., Dhawan A., Wendon J. Acute liver failure. Lancet 2010, 376:190-201.
40. Henderson J.M. Liver transplantation and rejection: an overview. Hepatogastroenterology 1999, 46(Suppl. 2):1482-1484.
41. Coito A.J. Leukocyte transmigration across endothelial and extracellular matrix protein barriers in liver ischemia/reperfusion injury. Curr Opin Organ Transplant 2011, 16:34-40.
42. Fondevila C., Shen X.D., Duarte S., Busuttil R.W., Coito A.J. Cytoprotective effects of a cyclic RGD peptide in steatotic liver cold ischemia and reperfusion injury. Am J Transplant 2009, 9:2240-2250.
43. Midwood K., Sacre S., Piccinini A.M., Inglis J., Trebaul A., Chan E., et al. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 2009, 15:774-780.
44. Ram M., Sherer Y., Shoenfeld Y. Matrix metalloproteinase-9 and autoimmune diseases. J Clin Immunol 2006, 26:299-307.
45. Kato H., Kuriyama N., Duarte S., Clavien P.A., Busuttil R.W., Coito A.J. MMP-9 deficiency shelters endothelial PECAM-1 expression and enhances regeneration of steatotic livers after ischemia and reperfusion injury. J Hepatol 2014, 60:1032-1039.
46. Kuyvenhoven J.P., Verspaget H.W., Gao Q., Ringers J., Smit V.T., Lamers C.B., et al. Assessment of serum matrix metalloproteinases MMP-2 and MMP-9 after human liver transplantation: increased serum MMP-9 level in acute rejection. Transplantation 2004, 77:1646-1652.
47. Kuyvenhoven J.P., Ringers J., Verspaget H.W., Lamers C.B., van Hoek B. Serum matrix metalloproteinase MMP-2 and MMP-9 in the late phase of ischemia and reperfusion injury in human orthotopic liver transplantation. Transplant Proc 2003, 35:2967-2969.
48. Cursio R., Mari B., Louis K., Rostagno P., Saint-Paul M.C., Giudicelli J., et al. Rat liver injury after normothermic ischemia is prevented by a phosphinic matrix metalloproteinase inhibitor. FASEB J 2002, 16:93-95.
49. Ma Z.Y., Qian J.M., Rui X.H., Wang F.R., Wang Q.W., Cui Y.Y., et al. Inhibition of matrix metalloproteinase-9 attenuates acute small-for-size liver graft injury in rats. Am J Transplant 2010, 10:784-795.
50. Gu Z., Kaul M., Yan B., Kridel S.J., Cui J., Strongin A., et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 2002, 297:1186-1190.
51. Hamada T., Duarte S., Tsuchihashi S., Busuttil R.W., Coito A.J. Inducible nitric oxide synthase deficiency impairs matrix metalloproteinase-9 activity and disrupts leukocyte migration in hepatic ischemia/reperfusion injury. Am J Pathol 2009, 174:2265-2277.
52. Duarte S., Shen X.D., Fondevila C., Busuttil R.W., Coito A.J. Fibronectin-alpha4beta1 interactions in hepatic cold ischemia and reperfusion injury: regulation of MMP-9 and MT1-MMP via the p38 MAPK pathway. Am J Transplant 2012, 12:2689-2699.
53. Frisch S.M., Screaton R.A. Anoikis mechanisms. Curr Opin Cell Biol 2001, 13:555-562.
54. Lee W.M. Acute liver failure. Semin Respir Crit Care Med 2012, 33:36-45.
55. Ito Y., Abril E.R., Bethea N.W., McCuskey R.S. Inhibition of matrix metalloproteinases minimizes hepatic microvascular injury in response to acetaminophen in mice. Toxicol Sci 2005, 83:190-196.
56. Hanumegowda U.M., Copple B.L., Shibuya M., Malle E., Ganey P.E., Roth R.A. Basement membrane and matrix metalloproteinases in monocrotaline-induced liver injury. Toxicol Sci 2003, 76:237-246.
57. Periasamy S., Hsu D.Z., Chen S.Y., Yang S.S., Chandrasekaran V.R., Liu M.Y. Therapeutic sesamol attenuates monocrotaline-induced sinusoidal obstruction syndrome in rats by inhibiting matrix metalloproteinase-9. Cell Biochem Biophys 2011, 61:327-336.
58. Nakamura K., Hatano E., Narita M., Miyagawa-Hayashino A., Koyama Y., Nagata H., et al. Sorafenib attenuates monocrotaline-induced sinusoidal obstruction syndrome in rats through suppression of JNK and MMP-9. J Hepatol 2012, 57:1037-1043.
59. Wielockx B., Lannoy K., Shapiro S.D., Itoh T., Itohara S., Vandekerckhove J., et al. Inhibition of matrix metalloproteinases blocks lethal hepatitis and apoptosis induced by tumor necrosis factor and allows safe antitumor therapy. Nat Med 2001, 7:1202-1208.
60. Van Lint P., Wielockx B., Puimege L., Noel A., Lopez-Otin C., Libert C. Resistance of collagenase-2 (matrix metalloproteinase-8)-deficient mice to TNF-induced lethal hepatitis. J Immunol 2005, 175:7642-7649.
61. Riehle K.J., Dan Y.Y., Campbell J.S., Fausto N. New concepts in liver regeneration. J Gastroenterol Hepatol 2011, 26(Suppl. 1):203-212.
62. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 2004, 5:836-847.
63. Michalopoulos G.K. Principles of liver regeneration and growth homeostasis. Compr Physiol 2013, 3:485-513.
64. Fausto N., Campbell J.S., Riehle K.J. Liver regeneration. Hepatology 2006, 43:S45-S53.
65. Olle E.W., Ren X., McClintock S.D., Warner R.L., Deogracias M.P., Johnson K.J., et al. Matrix metalloproteinase-9 is an important factor in hepatic regeneration after partial hepatectomy in mice. Hepatology 2006, 44:540-549.
66. Mohammed F.F., Pennington C.J., Kassiri Z., Rubin J.S., Soloway P.D., Ruther U., et al. Metalloproteinase inhibitor TIMP-1 affects hepatocyte cell cycle via HGF activation in murine liver regeneration. Hepatology 2005, 41:857-867.
67. Ding B.S., Nolan D.J., Butler J.M., James D., Babazadeh A.O., Rosenwaks Z., et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 2010, 468:310-315.
68. Wustefeld T., Rakemann T., Kubicka S., Manns M.P., Trautwein C. Hyperstimulation with interleukin 6 inhibits cell cycle progression after hepatectomy in mice. Hepatology 2000, 32:514-522.
69. Mohammed F.F., Smookler D.S., Taylor S.E., Fingleton B., Kassiri Z., Sanchez O.H., et al. Abnormal TNF activity in Timp3-/- mice leads to chronic hepatic inflammation and failure of liver regeneration. Nat Genet 2004, 36:969-977.
70. Han Y.P. Matrix metalloproteinases, the pros and cons, in liver fibrosis. J Gastroenterol Hepatol 2006, 21(Suppl. 3):S88-S91.
71. Giannandrea M., Parks W.C. Diverse functions of matrix metalloproteinases during fibrosis. Dis Model Mech 2014, 7:193-203.
72. 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.
73. Iredale J.P., Thompson A., Henderson N.C. Extracellular matrix degradation in liver fibrosis: biochemistry and regulation. Biochim Biophys Acta 1832, 2013:876-883.
74. Calabro S.R., Maczurek A.E., Morgan A.J., Tu T., Wen V.W., Yee C., et al. Hepatocyte produced matrix metalloproteinases are regulated by CD147 in liver fibrogenesis. PLoS One 2014, 9:e90571.
75. Harty M.W., Huddleston H.M., Papa E.F., Puthawala T., Tracy A.P., Ramm G.A., et al. Repair after cholestatic liver injury correlates with neutrophil infiltration and matrix metalloproteinase 8 activity. Surgery 2005, 138:313-320.
76. Iimuro Y., Nishio T., Morimoto T., Nitta T., Stefanovic B., Choi S.K., et al. Delivery of matrix metalloproteinase-1 attenuates established liver fibrosis in the rat. Gastroenterology 2003, 124:445-458.
77. Endo H., Niioka M., Sugioka Y., Itoh J., Kameyama K., Okazaki I., et al. Matrix metalloproteinase-13 promotes recovery from experimental liver cirrhosis in rats. Pathobiology 2011, 78:239-252.
78. Fallowfield J.A., Mizuno M., Kendall T.J., Constandinou C.M., Benyon R.C., Duffield J.S., et al. Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis. J Immunol 2007, 178:5288-5295.
79. Uchinami H., Seki E., Brenner D.A., D'Armiento J. Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis. Hepatology 2006, 44:420-429.
80. Ramachandran P., Pellicoro A., Vernon M.A., Boulter L., Aucott R.L., Ali A., et al. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc Natl Acad Sci U S A 2012, 109:E3186-E3195.
81. Knittel T., Mehde M., Grundmann A., Saile B., Scharf J.G., Ramadori G. Expression of matrix metalloproteinases and their inhibitors during hepatic tissue repair in the rat. Histochem Cell Biol 2000, 113:443-453.
82. Ramachandran P., Iredale J.P. Liver fibrosis: a bidirectional model of fibrogenesis and resolution. QJM 2012, 105:813-817.
83. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 2000, 14:163-176.
84. Radbill B.D., Gupta R., Ramirez M.C., DiFeo A., Martignetti J.A., Alvarez C.E., et al. Loss of matrix metalloproteinase-2 amplifies murine toxin-induced liver fibrosis by upregulating collagen I expression. Dig Dis Sci 2011, 56:406-416.
85. Onozuka I., Kakinuma S., Kamiya A., Miyoshi M., Sakamoto N., Kiyohashi K., et al. Cholestatic liver fibrosis and toxin-induced fibrosis are exacerbated in matrix metalloproteinase-2 deficient mice. Biochem Biophys Res Commun 2011, 406:134-140.
86. Hartland S.N., Murphy F., Aucott R.L., Abergel A., Zhou X., Waung J., et al. Active matrix metalloproteinase-2 promotes apoptosis of hepatic stellate cells via the cleavage of cellular N-cadherin. Liver Int 2009, 29:966-978.
87. Jirouskova M., Zbodakova O., Gregor M., Chalupsky K., Sarnova L., Hajduch M., et al. Hepatoprotective effect of MMP-19 deficiency in a mouse model of chronic liver fibrosis. PLoS One 2012, 7:e46271.
88. Roeb E., Purucker E., Breuer B., Nguyen H., Heinrich P.C., Rose-John S., et al. TIMP expression in toxic and cholestatic liver injury in rat. J Hepatol 1997, 27:535-544.
89. Yoshiji H., Kuriyama S., Yoshii J., Ikenaka Y., Noguchi R., Nakatani T., et al. Tissue inhibitor of metalloproteinases-1 attenuates spontaneous liver fibrosis resolution in the transgenic mouse. Hepatology 2002, 36:850-860.
90. Yoshiji H., Kuriyama S., Miyamoto Y., Thorgeirsson U.P., Gomez D.E., Kawata M., et al. Tissue inhibitor of metalloproteinases-1 promotes liver fibrosis development in a transgenic mouse model. Hepatology 2000, 32:1248-1254.
91. Hu Y.B., Li D.G., Lu H.M. Modified synthetic siRNA targeting tissue inhibitor of metalloproteinase-2 inhibits hepatic fibrogenesis in rats. J Gene Med 2007, 9:217-229.
92. Takahara T., Furui K., Yata Y., Jin B., Zhang L.P., Nambu S., et al. Dual expression of matrix metalloproteinase-2 and membrane-type 1-matrix metalloproteinase in fibrotic human livers. Hepatology 1997, 26:1521-1529.
93. Bodey B., Bodey B., Siegel S.E., Kaiser H.E. Immunocytochemical detection of MMP-3 and -10 expressions in hepatocellular carcinomas. Anticancer Res 2000, 20:4585-4590.
94. Huang C.C., Chuang J.H., Chou M.H., Wu C.L., Chen C.M., Wang C.C., et al. Matrilysin (MMP-7) is a major matrix metalloproteinase upregulated in biliary atresia-associated liver fibrosis. Mod Pathol 2005, 18:941-950.
95. Zeng Z.S., Shu W.P., Cohen A.M., Guillem J.G. Matrix metalloproteinase-7 expression in colorectal cancer liver metastases: evidence for involvement of MMP-7 activation in human cancer metastases. Clin Cancer Res 2002, 8:144-148.
96. Siller-Lopez F., Sandoval A., Salgado S., Salazar A., Bueno M., Garcia J., et al. Treatment with human metalloproteinase-8 gene delivery ameliorates experimental rat liver cirrhosis. Gastroenterology 2004, 126:1122-1133. [discussion 949].
97. Kato H., Kuriyama N., Duarte S., Clavien P.A., Busuttil R.W., Coito A.J. MMP-9 deficiency shelters endothelial PECAM-1 expression and enhances regeneration of steatotic livers after ischemia and reperfusion injury. J Hepatol 2014, 60:1032-1039.
98. Nguyen J.H., Yamamoto S., Steers J., Sevlever D., Lin W., Shimojima N., et al. Matrix metalloproteinase-9 contributes to brain extravasation and edema in fulminant hepatic failure mice. J Hepatol 2006, 44:1105-1114.
99. Hori T., Uemoto S., Walden L.B., Chen F., Baine A.M., Hata T., et al. Matrix metalloproteinase-9 as a therapeutic target for the progression of fulminant liver failure with hepatic encephalopathy: a pilot study in mice. Hepatol Res 2014, 44:651-662.
100. Zhou X., Murphy F.R., Gehdu N., Zhang J., Iredale J.P., Benyon R.C. Engagement of alphavbeta3 integrin regulates proliferation and apoptosis of hepatic stellate cells. J Biol Chem 2004, 279:23996-24006.
101. Arii S., Mise M., Harada T., Furutani M., Ishigami S., Niwano M., et al. Overexpression of matrix metalloproteinase 9 gene in hepatocellular carcinoma with invasive potential. Hepatology 1996, 24:316-322.
102. Sakamoto Y., Mafune K., Mori M., Shiraishi T., Imamura H., Mori M., et al. Overexpression of MMP-9 correlates with growth of small hepatocellular carcinoma. Int J Oncol 2000, 17:237-243.
103. Sun M.H., Han X.C., Jia M.K., Jiang W.D., Wang M., Zhang H., et al. Expressions of inducible nitric oxide synthase and matrix metalloproteinase-9 and their effects on angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 2005, 11:5931-5937.
104. Nart D., Yaman B., Yilmaz F., Zeytunlu M., Karasu Z., Kilic M. Expression of matrix metalloproteinase-9 in predicting prognosis of hepatocellular carcinoma after liver transplantation. Liver Transpl 2010, 16:621-630.
105. Garcia-Irigoyen O., Carotti S., Latasa M.U., Uriarte I., Fernandez-Barrena M.G., Elizalde M., et al. Matrix metalloproteinase-10 expression is induced during hepatic injury and plays a fundamental role in liver tissue repair. Liver Int 2014, 34:e257-e270.
106. Pellicoro A., Aucott R.L., Ramachandran P., Robson A.J., Fallowfield J.A., Snowdon V.K., et al. Elastin accumulation is regulated at the level of degradation by macrophage metalloelastase (MMP-12) during experimental liver fibrosis. Hepatology 2012, 55:1965-1975.
107. Madala S.K., Pesce J.T., Ramalingam T.R., Wilson M.S., Minnicozzi S., Cheever A.W., et al. Matrix metalloproteinase 12-deficiency augments extracellular matrix degrading metalloproteinases and attenuates IL-13-dependent fibrosis. J Immunol 2010, 184:3955-3963.
108. Yata Y., Takahara T., Furui K., Zhang L.P., Watanabe A. Expression of matrix metalloproteinase-13 and tissue inhibitor of metalloproteinase-1 in acute liver injury. J Hepatol 1999, 30:419-424.
109. Hironaka K., Sakaida I., Matsumura Y., Kaino S., Miyamoto K., Okita K. Enhanced interstitial collagenase (matrix metalloproteinase-13) production of Kupffer cell by gadolinium chloride prevents pig serum-induced rat liver fibrosis. Biochem Biophys Res Commun 2000, 267:290-295.
110. Harada T., Arii S., Mise M., Imamura T., Higashitsuji H., Furutani M., et al. Membrane-type matrix metalloproteinase-1(MT1-MTP) gene is overexpressed in highly invasive hepatocellular carcinomas. J Hepatol 1998, 28:231-239.
111. Zhou X., Hovell C.J., Pawley S., Hutchings M.I., Arthur M.J., Iredale J.P., et al. Expression of matrix metalloproteinase-2 and -14 persists during early resolution of experimental liver fibrosis and might contribute to fibrolysis. Liver Int 2004, 24:492-501.
112. Arai I., Nagano H., Kondo M., Yamamoto H., Hiraoka N., Sugita Y., et al. Overexpression of MT3-MMP in hepatocellular carcinoma correlates with capsular invasion. Hepatogastroenterology 2007, 54:167-171.