IκBα and IκBβ possess injury context-specific functions that uniquely influence hepatic NF-κB induction and inflammation

Journal of Clinical Investigation

Volumn 113, Issue 5, 2004, Pages 746-755

  Fan, Chenguang ^a   Li, Qiang ^a   Zhang, Yulong ^a   Liu, Xiaoming ^a   Luo, Meihui ^a   Abbott, Duane ^a   Zhou, Weihong ^a   Engelhardt, John F ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; ENDOTOXIN; I KAPPA B ALPHA; I KAPPA B BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; TYROSINE; I KAPPA B; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; PROTEIN KINASE P60;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENVIRONMENT; FIBROBLAST; GENE EXPRESSION; HEPATITIS; LIVER CELL; LIVER INJURY; LIVER ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; SURVIVAL; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; HETEROZYGOTE; INFLAMMATION; INJURY; LIVER; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TIME; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DNA, COMPLEMENTARY; ENDOTOXINS; HEPATOCYTES; HETEROZYGOTE; I-KAPPA B PROTEINS; INFLAMMATION; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, TRANSGENIC; MODELS, GENETIC; NF-KAPPA B; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS PP60(C-SRC); TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE;

EID: 85047689695     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI17337     Document Type: Article

References (47)

1. Karin, M., and Lin, A. 2002. NF-κB at the crossroads of life and death. Nat. Immunol. 3:221-227.
2. Ghosh, S., and Karin, M. 2002. Missing pieces in the NF-κB puzzle. Cell. 109 (Suppl):S81-S96.
3. Imbert, V., et al. 1996. Tyrosine phosphorylation of IκBα activates NF-κB without proteolytic degradation of IκBα. Cell. 86:787-798.
4. Livolsi, A., Busuttil, V., Imbert, V., Abraham, R.T., and Peyron, J.F. 2001. Tyrosine phosphorylation-dependent activation of NFκB. Requirement for p56 LCK and ZAP-70 protein tyrosine kinases. Eur. J. Biochem. 268:1508-1515.
5. Liu, R., Aupperle, K., and Terkeltaub, R. 2001. Src family protein tyrosine kinase signaling mediates monosodium urate crystal-induced IL-8 expression by monocytic THP-1 cells. J. Leukoc. Biol. 70:961-968.
6. al-Ramadi, B.K., et al. 2001. The Src-protein tyrosine kinase Lck is required for IL-I-mediated costimulatory signaling in Th2 cells. J. Immunol. 167:6827-6833.
7. Abu-Amer, Y., Dowdy, S.F., Ross, F.P., Clohisy, J.C., and Teitelbaum, S.L. 2001. TAT fusion proteins containing tyrosine 42-deleted IkappaBalpha arrest osteoclastogenesis. J. Biol. Chem. 276:30499-30503.
8. Beraud, C., Henzel, W.J., and Baeuerle, P.A. 1999. Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NFκB activation. Proc. Natl. Acad. Sci. U. S. A. 96:429-434.
9. Thompson, J.E., Phillips, R.J., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. 1995. I kappa B-beta regulates the persistent response in a biphasic activation of NF-kappa B. Cell. 80:573-582.
10. Velasco, M., Diaz-Guerra, M.J., Martin-Sanz, P., Alvarez, A., and Bosca, L. 1997. Rapid Up-regulation of IκBβ and abrogation of NF-κB activity in peritoneal macrophages stimulated with lipopolysaccharide. J. Biol. Chem. 272:23025-23030.
11. Beg, A.A., Sha, W.C., Bronson, R.T., and Baltimore, D. 1995. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev. 9:2736-2746.
12. Cheng, J.D., Ryseck, R.P., Attar, R.M., Dambach, D., and Bravo, R. 1998. Functional redundancy of the nuclear factor κB inhibitors IκBα and IκBβ. J. Exp. Med. 188:1055-1062.
13. Scoazec, J.Y., et al. 1994. Expression of cytokine-dependent adhesion molecules in postreperfusion biopsy specimens of liver allografts. Gastroenterology. 107:1094-1102.
14. Ghezzi, P., et al. 1991. Hypoxia increases production of interleukin-1 and tumor necrosis factor by human mononuclear cells. Cytokine. 3:189-194.
15. Tamatani, M., et al. 2000. A pathway of neuronal apoptosis induced by hypoxia/reoxygenation: roles of nuclear factor-κB and Bcl-2. J. Neurochem. 75:683-693.
16. Iimuro, Y., et al. 1998. NF-κB prevents apoptosis and liver dysfunction during liver regeneration. J. Clin. Invest. 101:802-811.
17. Morgan, E.N., et al. 1999. An essential role for NF-κB in the cardioadaptive response to ischemia. Ann. Thorac. Surg. 68:377-382.
18. Bach, F.H., et al. 1997. Modification of vascular responses in xenotransplantation: inflammation and apoptosis [see comments]. Nat. Med. 3:944-948.
19. Li, Z.W., et al. 1999. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189:1839-1845.
20. Li, Q., Van Antwerp, D., Mercurio, F., Lee, K.F., and Verma, I.M. 1999. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science. 284:321-325.
21. Rudolph, D., et al. 2000. Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14:854-862.
22. Iimuro, Y., et al. 1998. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J. Clin. Invest. 101:802-811.
23. Fan, C., Yang, J., and Engelhardt, J.F. 2002. Temporal pattern of NFκB activation influences apoptotic cell fate in a stimuli dependent fashion. J. Cell Sci. 115:4843-4853.
24. Lawrence, T., Gilroy, D.W., Colville-Nash, P.R., and Willoughby, DA. 2001. Possible new role for NF-κB in the resolution of inflammation. Nat. Med. 7:1291-1297.
25. Zwacka, R.M., Zhang, Y., Zhou, W., Halldorson, J., and Engelhardt, J.F. 1998. Ischemia/reperfusion injury in the liver of BALB/c mice activates AP-1 and nuclear factor κB independently of IκB degradation. Hepatology. 28:1022-1030.
26. Schierwagen, C., Bylund-Fellenius, A.C., and Lundberg, C. 1990. Improved method for quantification of tissue PMN accumulation measured by myeloperoxidase activity. J. Pharmacol. Methods. 23:179-186.
27. Dalet, C., Fehlmann, M., and Debey, P. 1982. Use of Percoll density gradient centrifugation for preparing isolated rat hepatocytes having long-term viability. Anal. Biochem. 122:119-123.
28. Page, D.T., and Garvey, J.S. 1979. Isolation and characterization of hepatocytes and Kupffer cells. J. Immunol. Methods. 27:159-173.
29. Sanlioglu, S., et al. 2001. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-α secretion through IKK regulation of NFκB. J. Biol. Chem. 276:30188-30198.
30. Fan, C., Li, Q., Ross, D., and Engelhardt, J.F. 2003. Tyrosine phosphorylation of IκBα activates NFκB through a redox-regulated and c-Src-dependent mechanism following hypoxia/reoxygenation. J. Biol. Chem. 278:2072-2080.
31. Colletti, L.M., et al. 1990. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J. Clin. Invest. 85:1936-1943.
32. Ben-Ari, Z., et al. 2002. Role of anti-tumor necrosis factor-alpha in ischemia/reperfusion injury in isolated rat liver in a blood-free environment. Transplantation. 73:1875-1880.
33. Sugita, S., et al. 2002. Induction of macrophage-inflammatory protein-3α gene expression by TNF-dependent NF-κB activation. J. Immunol. 168:5621-5628.
34. Oberholzer, A., Oberholzer, C., Bahjat, F.R., Edwards, C.K., III, and Moldawer, L.L. 2001. Genetic determinants of lipopolysaccharide and D-galactosamine-mediated hepatocellular apoptosis and lethality. J. Endotoxin Res. 7:375-380.
35. Abu-Amer, Y., et al. 1998. Tumor necrosis factor-α activation of nuclear transcription factor-κB in marrow macrophages is mediated by c-Src tyrosine phosphorylation of Ikappa Balpha. J. Biol. Chem. 273:29417-29423.
36. Rothwarf, D.M., and Karin, M. 1999. The NF-kappa B activation pathway: a paradigm in information transfer from membrane to nucleus. Sci. STKE. 1999(5):RE1.
37. Klement, J.F., et al. 1996. IkappaBalpha deficiency results in a sustained NF-kappaB response and severe widespread dermatitis in mice. Mol. Cell. Biol. 16:2341-2349.
38. Tam, W.F., Lee, L.H., Davis, L., and Sen, R. 2000. Cytoplasmic sequestration of rel proteins by IkappaBalpha requires CRM1-dependent nuclear export. Mol. Cell. Biol. 20:2269-2284.
39. Memet, S., et al. 1999. IκBε-deficient mice: reduction of one T cell precursor subspecies and enhanced Ig isotype switching and cytokine synthesis. J. Immunol. 163:5994-6005.
40. Zingarelli, B., et al. 2002. Absence of inducible nitric oxide synthase modulates early reperfusion-induced NF-κB and AP-1 activation and enhances myocardial damage. FASEB J. 16:327-342.
41. Chen, L.W., et al. 2003. The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med. 9:575-581.
42. Ozaki, M., et al. 2000. Inhibition of the Rac1 GTPase protects against nonlethal ischemia/reperfusion-induced necrosis and apoptosis in vivo. FASEB J. 14:418-429.
43. Colletti, L.M., et al. 1996. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology. 23:506-514.
44. Suzaki, Y., et al. 2002. Hydrogen peroxide stimulates c-Src-mediated big mitogen-activated protein kinase 1 (BMK1) and the MEF2C signaling pathway in PC12 cells: potential role in cell survival following oxidative insults. J. Biol. Chem. 277:9614-9621.
45. Takada, Y., et al. 2003. Hydrogen peroxide activates NF-κB through tyrosine phosphorylation of IκBα and serine phosphorylation of P65: evidence for the involvement of IκBα kinase and Syk protein tyrosine kinase. J. Biol. Chem. 278:24233-24241.
46. Chaisson, M.L., Brooling,J.T., Ladiges, W., Tsai, S., and Fausto, N. 2002. Hepatocyte-specific inhibition of NFκB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J. Clin. Invest. 110:193-202. doi:10.1172/JCI200215295.
47. Zwacka, R.M., et al. 1998. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-κB activation. Nat. Med. 4:698-704.