Matrix metalloproteinase-9 as a therapeutic target for the progression of fulminant liver failure with hepatic encephalopathy: A pilot study in mice

Hepatology Research

Volumn 44, Issue 6, 2014, Pages 651-662

  Hori, Tomohide ^a,b   Uemoto, Shinji ^b   Walden, Lindsay B ^a   Chen, Feng ^a   Baine, Ann Marie T ^a   Hata, Toshiyuki ^b   Kogure, Takayuki ^c   Nguyen, Justin H ^a  

^a MAYO CLINIC   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Comatose; Hepatic encephalopathy; Liver transplantation; Matrix metalloproteinase; Tissue inhibitor of metalloproteinases

Indexed keywords

AZOXYMETHANE; COMPLEMENTARY DNA; GELATINASE B; ILOMASTAT; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DISEASE COURSE; DISEASE DURATION; DISEASE MODEL; ENZYME INHIBITION; FULMINANT HEPATIC FAILURE; GENETIC TRANSFECTION; HEPATIC COMA; HEPATIC ENCEPHALOPATHY; HISTOPATHOLOGY; INFANT; MALE; MOUSE; MURINE MODEL; NONHUMAN; PILOT STUDY; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SURVIVAL RATE; WESTERN BLOTTING; ZYMOGRAPHY;

EID: 84901932044     PISSN: 13866346     EISSN: 1872034X     Source Type: Journal    
DOI: 10.1111/hepr.12161     Document Type: Article

References (57)

1. Mochida S, Takikawa Y, Nakayama N etal. Diagnostic criteria of acute liver failure: a report by the Intractable Hepato-Biliary Diseases Study Group of Japan. Hepatol Res 2011; 41: 805-812.
2. Sugawara K, Nakayama N, Mochida S. Acute liver failure in Japan: definition, classification, and prediction of the outcome. J Gastroenterol 2012; 47: 849-861.
3. Lee WM. Acute liver failure. Semin Respir Crit Care Med 2012; 33: 36-45.
4. Mpabanzi L, Jalan R. Neurological complications of acute liver failure: pathophysiological basis of current management and emerging therapies. Neurochem Int 2012; 60: 736-742.
5. Williams R, Wendon J. Indications for orthotopic liver transplantation in fulminant liver failure. Hepatology 1994; 20: S5-10S.
6. Bismuth H, Samuel D, Castaing D etal. Orthotopic liver transplantation in fulminant and subfulminant hepatitis. The Paul Brousse experience. Ann Surg 1995; 222: 109-119.
7. Boudjema K, Cherqui D, Jaeck D etal. Auxiliary liver transplantation for fulminant and subfulminant hepatic failure. Transplantation 1995; 59: 218-223.
8. Tan WF, Steadman RH, Farmer DG etal. Pretransplant neurological presentation and severe posttransplant brain injury in patients with acute liver failure. Transplantation 2012; 94: 768-774.
9. Goss JA, Shackleton CR, Maggard M etal. Liver transplantation for fulminant hepatic failure in the pediatric patient. Arch Surg 1998; 133: 839-846.
10. Defamie V, Laurens M, Patrono D etal. Matrix metalloproteinase inhibition protects rat livers from prolonged cold ischemia-warm reperfusion injury. Hepatology 2008; 47: 177-185.
11. Ma ZY, Qian JM, Rui XH etal. Inhibition of matrix metalloproteinase-9 attenuates acute small-for-size liver graft injury in rats. Am J Transplant 2010; 10: 784-795.
12. Hua H, Li M, Luo T, Yin Y, Jiang Y. Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol Life Sci 2011; 68: 3853-3868.
13. Friedl P, Wolf K. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res 2008; 68: 7247-7249.
14. Kireva T, Erhardt A, Tiegs G etal. Transcription factor Fra-1 induces cholangitis and liver fibrosis. Hepatology 2011; 53: 1259-1269.
15. Shi GM, Ke AW, Zhou J etal. CD151 modulates expression of matrix metalloproteinase 9 and promotes neoangiogenesis and progression of hepatocellular carcinoma. Hepatology 2010; 52: 183-196.
16. Mei Y, Thevananther S. Endothelial nitric oxide synthase is a key mediator of hepatocyte proliferation in response to partial hepatectomy in mice. Hepatology 2011; 54: 1777-1789.
17. Olle EW, Ren X, McClintock SD etal. Matrix metalloproteinase-9 is an important factor in hepatic regeneration after partial hepatectomy in mice. Hepatology 2006; 44: 540-549.
18. Overall CM, Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2002; 2: 657-672.
19. Wielockx B, Lannoy K, Shapiro SD etal. 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.
20. Yan C, Zhou L, Han YP. Contribution of hepatic stellate cells and matrix metalloproteinase 9 in acute liver failure. Liver Int 2008; 28: 959-971.
21. Hanumegowda UM, Copple BL, Shibuya M, Malle E, Ganey PE, Roth RA. Basement membrane and matrix metalloproteinases in monocrotaline-induced liver injury. Toxicol Sci 2003; 76: 237-246.
22. Ito Y, Abril ER, Bethea NW etal. Mechanisms and pathophysiological implications of sinusoidal endothelial cell gap formation following treatment with galactosamine/endotoxin in mice. Am J Physiol Gastrointest Liver Physiol 2006; 291: G211-218.
23. Fujimoto M, Takagi Y, Aoki T etal. Tissue inhibitor of metalloproteinases protect blood-brain barrier disruption in focal cerebral ischemia. J Cereb Blood Flow Metab 2008; 28: 1674-1685.
24. Tejima E, Guo S, Murata Y etal. Neuroprotective effects of overexpressing tissue inhibitor of metalloproteinase TIMP-1. J Neurotrauma 2009; 26: 1935-1941.
25. Hori T, Chen F, Baine A, Gardner L, Nguyen J. Fulminant liver failure model with hepatic encephalopathy in the mouse. Ann Gastroenterol 2011; 24: 294-306.
26. Matkowskyj KA, Marrero JA, Carroll RE, Danilkovich AV, Green RM, Benya RV. Azoxymethane-induced fulminant hepatic failure in C57BL/6J mice: characterization of a new animal model. Am J Physiol 1999; 277: G455-462.
27. Belanger M, Cote J, Butterworth RF. Neurobiological characterization of an azoxymethane mouse model of acute liver failure. Neurochem Int 2006; 48: 434-440.
28. Nguyen JH, Yamamoto S, Steers J etal. Matrix metalloproteinase-9 contributes to brain extravasation and edema in fulminant hepatic failure mice. J Hepatol 2006; 44: 1105-1114.
29. Ohashi N, Hori T, Chen F etal. Matrix metalloproteinase-9 contributes to parenchymal hemorrhage and necrosis in the remnant liver after extended hepatectomy in mice. World J Gastroenterol 2012; 18: 2320-2333.
30. Chen F, Ohashi N, Li W, Eckman C, Nguyen JH. Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology 2009; 50: 1914-1923.
31. Chen F, Hori T, Ohashi N, Baine AM, Eckman CB, Nguyen JH. Occludin is regulated by epidermal growth factor receptor activation in brain endothelial cells and brains of mice with acute liver failure. Hepatology 2011; 53: 1294-1305.
32. Hori T, Uemoto S, Zhao X etal. Surgical guide including innovative techniques for orthotopic liver transplantation in the rat: key techniques and pitfalls in whole and split liver grafts. Ann Gastroenterol 2010; 23: 270-295.
33. Sawara K, Desjardins P, Chatauret N, Kato A, Suzuki K, Butterworth RF. Alterations in expression of genes coding for proteins of the neurovascular unit in ischemic liver failure. Neurochem Int 2009; 55: 119-123.
34. Yamamoto S, Steers JL, Wharen RE, Jr, Eckman CB, Nguyen JH. Cerebrospinal fluid drainage and cranial decompression prolong survival in rats with fulminant hepatic failure. Transpl Int 2006; 19: 675-682.
35. Yamamoto S, Nguyen JH. TIMP-1/MMP-9 imbalance in brain edema in rats with fulminant hepatic failure. J Surg Res 2006; 134: 307-314.
36. Knittel T, Mehde M, Grundmann A, Saile B, Scharf JG, Ramadori G. Expression of matrix metalloproteinases and their inhibitors during hepatic tissue repair in the rat. Histochem Cell Biol 2000; 113: 443-453.
37. Padrissa-Altes S, Zaouali MA, Franco-Gou R etal. Matrix metalloproteinase 2 in reduced-size liver transplantation: beyond the matrix. Am J Transplant 2010; 10: 1167-1177.
38. Hori T, Uemoto S, Chen F etal. Effect of cold ischemia/reperfusion injury and/or shear stress with portal hypertension on the expression of matrix metalloproteinase-9. Ann Gastroenterol 2012; 25: 345-351.
39. Vaquero J, Chung C, Blei AT. Brain edema in acute liver failure. A window to the pathogenesis of hepatic encephalopathy. Ann Hepatol 2003; 2: 12-22.
40. Horowitz ME, Schafer DF, Molnar P etal. Increased blood-brain transfer in a rabbit model of acute liver failure. Gastroenterology 1983; 84: 1003-1011.
41. Nguyen JH. Blood-brain barrier in acute liver failure. Neurochem Int 2012; 60: 676-683.
42. Nguyen JH. Subtle BBB alterations in brain edema associated with acute liver failure. Neurochem Int 2010; 56: 203-204.
43. Shimojima N, Eckman CB, McKinney M etal. Altered expression of zonula occludens-2 precedes increased blood-brain barrier permeability in a murine model of fulminant hepatic failure. J Invest Surg 2008; 21: 101-108.
44. Chen F, Radisky ES, Das P etal. TIMP-1 attenuates blood-brain barrier permeability in mice with acute liver failure. J Cereb Blood Flow Metab 2013. doi: 10.1038/jcbfm.2013.45
45. Potvin M, Finlayson MH, Hinchey EJ, Lough JO, Goresky CA. Cerebral abnormalities in hepatectomized rats with acute hepatic coma. Lab Invest 1984; 50: 560-564.
46. Traber PG, Dal Canto M, Ganger DR, Blei AT. Electron microscopic evaluation of brain edema in rabbits with galactosamine-induced fulminant hepatic failure: ultrastructure and integrity of the blood-brain barrier. Hepatology 1987; 7: 1272-1277.
47. Kato M, Hughes RD, Keays RT, Williams R. Electron microscopic study of brain capillaries in cerebral edema from fulminant hepatic failure. Hepatology 1992; 15: 1060-1066.
48. Gove CD, Hughes RD, Ede RJ, Williams R. Regional cerebral edema and chloride space in galactosamine-induced liver failure in rats. Hepatology 1997; 25: 295-301.
49. Wong V, Gumbiner BM. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 1997; 136: 399-409.
50. Tavelin S, Hashimoto K, Malkinson J, Lazorova L, Toth I, Artursson P. A new principle for tight junction modulation based on occludin peptides. Mol Pharmacol 2003; 64: 1530-1540.
51. Nusrat A, Parkos CA, Verkade P etal. Tight junctions are membrane microdomains. J Cell Sci 2000; 113: 1771-1781.
52. Nitta T, Hata M, Gotoh S etal. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 2003; 161: 653-660.
53. Luedde T, Trautwein C. Intracellular survival pathways in the liver. Liver Int 2006; 26: 1163-1174.
54. Rutherford A, Chung RT. Acute liver failure: mechanisms of hepatocyte injury and regeneration. Semin Liver Dis 2008; 28: 167-174.
55. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology 2006; 43: S45-53.
56. Tanaka Y, Sohda T, Matsuo K etal. Vascular endothelial growth factor reduces Fas-mediated acute liver injury in mice. J Gastroenterol Hepatol 2008; 23: e207-211.
57. Dechêne A, Sowa JP, Gieseler RK etal. Acute liver failure is associated with elevated liver stiffness and hepatic stellate cell activation. Hepatology 2010; 52: 1008-1016.