The transcription factor interferon regulatory factor-1 mediates liver damage during ischemia-reperfusion injury

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 290, Issue 6, 2006, Pages

  Tsung, Allan ^a   Stang, Michael T ^a   Ikeda, Atsushi ^a   Critchlow, Nathan D ^a   Izuishi, Kunihiko ^a   Nakao, Atsunori ^a   Chan, Meagan H ^a   Jeyabalan, Geetha ^a   Yim, John H ^a   Geller, David A ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

c Jun NH2 terminal kinase; Cytokines; Hepatic ischemia; Inducible nitric oxide synthase; Liver injury

Indexed keywords

ADENOVIRUS VECTOR; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; GENE EXPRESSION; GENE TARGETING; KNOCKOUT MOUSE; LIVER CELL CULTURE; LIVER INJURY; LIVER ISCHEMIA; LIVER TRANSPLANTATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; TRANSCRIPTION FACTORS;

EID: 33646886598     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00460.2005     Document Type: Article

References (42)

1. Bendinelli P, Piccoletti R, Maroni P, and Bernelli-Zazzera A. The MAP kinase cascades are activated during post-ischemic liver reperfusion. FEBS Lett 398: 193-197, 1996.
2. Bradham CA, Stachlewitz RF, Gao W, Qian T, Jayadev S, Jenkins G, Hannun Y, Lemasters JJ, Thurman RG, and Brenner DA. Reperfusion after liver transplantation in rats differentially activates the mitogen-activated protein kinases. Hepatology 25: 1128-1135, 1997.
3. Chia SH, Geller DA, Kibbe M, Watkins SC, Fung JJ, Starzl TE, and Murase N. Adenovirus-mediated gene transfer to liver grafts: an important method to maximize infectivity. Transplantation 66: 1545-1551, 1998.
4. Chomczynski P and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
5. Clavien PA, Rudiger HA, and Selzner M. Mechanism of hepatocyte death after ischemia: apoptosis versus necrosis. Hepatology 33: 1555-1557, 2001.
6. Colletti LM, Kunkel SL, Walz A, Burdick MD, Kunkel RG, Wilke CA, and Strieter RM. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology 23: 506-514, 1996.
7. Crenesse D, Schmid-Alliana A, Laurens M, Cursio R, and Gugenheim J. JNK(1)/SAPK(1) involvement in hypoxia-reoxygenation-induced apoptosis in rat hepatocytes. Transplant Proc 33: 260-261, 2001.
8. Fan C, Zwacka RM, and Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J Mol Med 77: 577-592, 1999.
9. Fondevila C, Busuttil RW, and Kupiec-Weglinski JW. Hepatic ischemia/reperfusion injury: a fresh look. Exp Mol Pathol 74: 86-93, 2003.
10. Geller DA, Nguyen D, Shapiro RA, Nussler A, Di Silvio M, Freeswick P, Wang SC, Tweardy DJ, Simmons RL, and Billiar TR. Cytokine induction of interferon regulatory factor-1 in hepatocytes. Surgery 114: 235-242, 1993.
11. Geller DA, Nussler AK, DiSilvio M, Lowenstein CJ, Shapiro RA, Wang SC, Simmons RL, and Billiar TR. Cyokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. Proc Natl Acad Sci USA 90: 522-526, 1993.
12. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284: G15-G26, 2003.
13. Jaeschke H and Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125: 1246-1257, 2003.
14. Kamada N and Calne RY. A surgical experience with five hundred thirty liver transplants in the rat. Surgery 93: 64-69, 1983.
15. Kamijo R, Harada H, Matsuyama T, Boslard M, Gerecitano D, Shapiro J, Le S, Koh SI, Kimura T, and Green J. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263: 1612-1615, 1994.
16. Ke B, Shen XD, Gao F, Busuttil RW, and Kupiec-Weglinski JW Interleukin 13 gene transfer in liver ischemia and reperfusion injury: role of Stat 6 and TLR4 in cytoprotection. Hum Gene Ther 15: 691-698, 2004.
17. Kim PK, Armstrong M, Liu Y, Yan P, Bucher B, Zuckerbraun BS, Gambotto A, Billiar TR, and Yim JH. IRF-1 expression induces apoptosis and inhibits tumor growth in mouse mammary cancer cells in vitro and in vivo. Oncogene 23: 1125-1135, 2004.
18. Kohli V, Selzner M, Madden JF, Bentley RC, and Clavien PA. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation 67: 1099-1105, 1999.
19. Kroger A, Koster M, Schroeder K, Hauser H, and Mueller PP. Activities of IRF-1. J Interferon Cytokine Res 22: 5-14, 2002.
20. Lechleitner S, Gille J, Johnson DR, and Petzelbauer P. Interferon enhances tumor necrosis factor-induced vascular cell adhesion molecule 1 (CD106) expression in human endothelial cells by an interferon-related factor 1-dependent pathway. J Exp Med 187: 2023-2030, 1998.
21. Lee VG, Johnson ML, Baust J, Laubach VE, Watkins SC, and Billiar TR. The roles of iNOS in liver ischemia-reperfusion injury. Shock 16: 355-360, 2001.
22. Lowenstein CJ, Alley EW, Raval P, Snowman AM, Snyder SH, Russell SW, and Murphy WJ. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA 90: 9730-9734, 1993.
23. Martin E, Nathan C, and Xie QW. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J Exp Med 180: 977-984, 1994.
24. Mavier P, Preaux AM, Guigui B, Lescs MC, Zafrani ES, and Dhumeaux D. In vitro toxicity of polymorphonuclear neutrophils to rat hepatocytes: evidence for a proteinase-mediated mechanism. Hepatology 8: 254-258, 1988.
25. McCloskey CA, Kameneva MV, Uryash A, Gallo DJ, and Billiar TR. Tissue hypoxia activates JNK in the liver during hemorrhagic shock. Shock 22: 380-386, 2004.
26. Miyamoto M, Fujita T, Kimura Y, Maruyama M, Harada H, Sudo Y, Miyata T, and Taniguchi T. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell 54: 903-913, 1988.
27. Moore BA, Otterbein LE, Turler A, Choi AM, and Bauer AJ. Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology 124: 377-391, 2003.
28. Morris SM Jr, Kepka-Lenhart D, and Chen LC. Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol Endocrinol Metab 275: E740-E747, 1998.
29. Olthoff KM. Molecular pathways of regeneration and repair after liver transplantation. World J Surg 26: 831-837, 2002.
30. Overbergh L, Valckx D, Waer M, and Mathieu C. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 11: 305-312, 1999.
31. Reis LF, Harad H, Wolchok JD, Taniguchi T, and Vilcek J. Critical role of a common transcription factor, IRF-1, in the regulation of IFN-beta and IFN-inducible genes. EMBO J 185-193, 1991.
32. Selzner N, Rudiger H, Graf R, and Clavien PA. Protective strategies against ischemic injury of the liver. Gastroenterology 125: 917-936, 2003.
33. Takahashi Y, Ganster RW, Gambotto A, Shao L, Kaizu T, Wu T, Yagnik GP, Nakao A, Tsoulfas G, Ishikawa T, Okuda T, Geller DA, and Murase N. Role of NF-κB on liver cold ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 283: G1175-G1184, 2002.
34. Takahashi Y, Geller DA, Gambotto A, Watkins SC, Fung JJ, and Murase N. Adenovirus-mediated gene therapy to liver grafts: Donor pre-treatment vs. back-table clamp technique. Surgery 128: 345-352, 2000.
35. Taniguchi T, Ogasawara K, Takaoka A, and Tanaka N. IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19: 623-655, 2001.
36. Tsung A, Kaizu T, Nakao A, Shao L, Bucher B, Fink MP, Murase N, and Geller DA. Ethyl pyruvate ameliorates liver ischemia-reperfusion injury by decreasing hepatic necrosis and apoptosis. Transplantation 79: 196-204, 2005.
37. Uehara T, Bennett B, Sakata ST, Satoh Y, Bilter GK, Westwick JK, and Brenner DA. JNK mediates hepatic ischemia reperfusion injury. J Hepatol 42: 850-859, 2005.
38. Uehara T, Xi Peng X, Bennett B, Satoh Y, Friedman G, Currin R, Brenner DA, and Lemasters J. c-Jun N-terminal kinase mediates hepatic injury after rat liver transplantation. Transplantation 78: 324-332, 2004.
39. Wanner GA, Muller PE, Ertel W, Bauer M, Menger MD, and Messmer K. Differential effect of anti-TNF-alpha antibody on proinflammatory cytokine release by Kupffer cells following liver ischemia and reperfusion. Shock 11: 391-395, 1999.
40. Watanabe Y, Suzuki O, Haruyama T, and Akaike T. Interferon-gamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis. J Cell Biochem 89: 244-253, 2003.
41. Whitmarsch AJ and Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74: 589-607, 1996.
42. Yu-Lee LY, Hrachovy JA, Stevens AM, and Schwarz LA. Interferon-regulatory factor 1 is an immediate-early gene under transcriptional regulation by prolactin in Nb2 T cells. Mol Cell Biol 10: 3087-3094, 1990.