Hsp70 inhibits lipopolysaccharide-induced NF-κB activation by interacting with TRAF6 and inhibiting its ubiquitination

FEBS Letters

Volumn 580, Issue 13, 2006, Pages 3145-3152

  Chen, Huaqun ^a   Wu, Yifan ^a   Zhang, Yiqing ^a   Jin, Lina ^a   Luo, Lan ^b   Xue, Bin ^b   Lu, Chen ^a   Zhang, Xiran ^a   Yin, Zhimin ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

Heat shock protein 70; Lipopolysaccharide; NF B; Tumor necrosis factor receptor associated factor 6; Ubiquitination

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ANIMALS; CYCLOOXYGENASE 2; DOWN-REGULATION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; TNF RECEPTOR-ASSOCIATED FACTOR 6; UBIQUITIN;

BACTERIA (MICROORGANISMS);

EID: 33646580045     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.04.066     Document Type: Article

References (45)

1. Ulevitch R.J., and Tobias P.S. Recognition of Gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11 (1999) 19-22
2. Guha M., and Mackman N. LPS induction of gene expression in human monocytes. Cell. Signal. 13 (2001) 85-94
3. Hsu H., and Wen M. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J. Biol. Chem. 277 (2002) 22131-22139
4. Wheeler M.A., Smith S.D., García-Cardena G., Nathan C.F., Weiss R.M., and Sessa W.C. Bacterial infection induces nitric oxide synthase in human neutrophils. J. Clin. Invest. 99 (1997) 110-116
5. Lee J.C., Laydon J.T., McDonnell P.C., Gallagher T.F., Kumar S., Green D., McNulty D., Blumenthal M.J., Heys J.R., and Landvatter S.W. A protein kinase involved in the regulation of the inflammatory cytokine biosynthesis. Nature 372 (1994) 739-746
6. Hambleton J., Weinstein S.L., Lem L., and DeFranco A.L. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA 93 (1996) 2774-2778
7. 2 production in lipopolysaccharide-stimulated monocytes. J. Immunol. 161 (1998) 5681-5686
8. Krappmann D., Wegener E., Sunami Y., Esen M., Thiel A., Mordmuller B., and Scheidereit C. The IκB kinase complex and NF-κB act as master regulators of lipopolysaccharide-induced gene expression and control subordinate activation of AP-1. Mol. Cell. Biol. 24 (2004) 6488-6500
9. Aggarwal B.B. Nuclear factor-κB: The enemy within. Cancer Cell 6 (2004) 203-208
10. Hayden M.S., and Ghosh S. Signaling to NF-κB. Genes Dev. 18 (2004) 2195-2224
11. Karin M., and Greten F.R. NF-κB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5 (2005) 749-759
12. Chen Z., Hagler J., Palombella V.J., Melandri F., Scherer D., Ballard D., and Maniatis T. Signal-induced site specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9 (1995) 1586-1597
13. Qian Y., Commane M., Ninomiya-Tsuji J., Matsumto K., and Li X. IRAK-mediated translocation of TRAF6 and TAB2 in the interleukin-1-induced activation of NF-κB. J. Biol. Chem. 276 (2001) 41661-41667
14. Janssens S., and Beyaert R. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11 (2003) 293-302
15. Kopp E., and Medzhidov R. Recognition of microbial infection by Toll-like receptors. Curr. Opin. Immunol. 15 (2003) 396-401
16. Feder M.E., and Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61 (1999) 243-282
17. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2 (2002) 185-194
18. Amici C., Rossi A., and Satoro M.G. Selective inhibition of virus protein synthesis by prostaglandin A: a translational block associated with Hsp70 synthesis. J. Virol. 68 (1994) 6890-6899
19. Mestril R., Chi S.H., Sayen M.R., O'Reilly K., and Dillmann W.H. Expression of inducible stress protein 70 in rat heart myogenic cells confers protection against stimulated ischemia-induced injury. J. Clin. Invest. 93 (1994) 759-767
20. Polla B.S., Bachelet M., and Santoro M.G. Stress proteins in inflammation. Ann. N.Y. Acsd. Sci. 85 (1998) 75-85
21. Jiang B., Xiao W., Shi Y., Liu M., and Xiao X. Heat shock pretreatment inhibited the release of Smac/DIABLO from mitochondria and apoptosis induced by hydrogen peroxide in cardiomyocytes and C2C12 myogenic cells. Cell Stress Chaperones 10 (2005) 252-262
22. Koller M., Hensler T., Konig B., Prevost G., Alouf J., and Konig W. Induction of heat-shock proteins by bacterial toxins, lipid mediators and cytokines in human leukocytes. Zentralbl Bakteriol. 278 (1993) 365-376
23. Hauser G.J., Dayao E.K., Wasserloos K., Pitt B.R., and Wong H.R. HSP induction inhibits iNOS mRNA expression and attenuates hypotension in endotoxin-challenged rats. Am. J. Physiol. 271 (1996) H2529-H2535
24. Ding X.Z., Fernandez-Prada C.M., Bhattacharjee A.K., and Hoover D.L. Over-expression of Hsp-70 inhibits bacterial lipopolysaccharide-induced production of cytokines in human monocyte-derived macrophages. Cytokine 16 (2001) 210-219
25. Feinstein D.L., Galea E., and Reis D.J. Suppression of glial nitric oxide synthase induction by heat shock: effects on proteolytic degradation of IκB-α. Nitric Oxide 2 (1997) 167-176
26. Margulis B.A., Sandler S., Eizirik D.L., Welsh N., and Welsh M. Liposomal delivery of purified heat shock protein hsp70 into rat pancreatic islets as protection against interleukin 1 beta-induced impaired β-cell function. Diabetes 40 (1991) 1418-1422
27. Meng X., Shames B.D., Ao L., Meldrum D.R., Chan D., Banerjee A., and Harken A.H. Heat shock protein 72 suppresses macrophage TNFα production by inhibition of NF-κB intranuclear translocation. Shock 11 (1999) S40
28. Adler V., Yin Z., Fuchs S.Y., Benezra M., Rosario L., Tew K.D., Pincus M.R., Sardana M., Henderson C.J., Wolf C.R., Davis R.J., and Ronai Z. Regulation of JNK signaling by GSTp. EMBO J. 18 (1999) 1321-1334
29. Lomaga M.A., Yeh W.C., Sarosi I., Duncan G.S., Furlonger C., Ho A., Morony S., Capparelli C., Van G., Kaufman S., van der Heiden A., Itie A., Wakeham A., Khoo W., Sasaki T., Cao Z., Penninger J.M., Paige C.J., Lancey D.L., Dunstan C.R., Boyle W.J., Goeddel D.V., and Mak T.W. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 15 (1999) 1015-1024
30. Kobayashi N., Kadono Y., Naito A., Matsumoto K., Yamamoto T., Tanaka S., and Inoue J. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J. 20 (2001) 1271-1280
31. Ran R., Lu A., Zhang L., Tang Y., Zhu H., Xu H., Feng Y., Han C., Zhou G., Rigby A.C., and Sharp F.R. Hsp70 promotes TNF-mediated apoptosis by binding IKKγ and impairing NF-κB survival signaling. Genes Dev. 18 (2004) 1466-1481
32. Park K.J., Gaynor R.B., and Kwak Y.T. Heat shock protein 27 association with the IκB kinase complex regulates tumor necrosis factor α-induced NF-κB activation. J. Biol. Chem. 278 (2003) 35272-35278
33. Craig E.A. Chaperones: helpers along the pathways to protein folding. Science 260 (1993) 1902-1903
34. Rhee S.H., and Hwang D. Murine Toll-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J. Biol. Chem. 275 (2000) 34035-34040
35. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., and Chen Z.J. Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103 (2000) 351-361
36. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., and Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412 (2001) 346-351
37. Baud V., Liu Z., Bennett B., Suzuki N., Xia Y., and Karin M. Signaling by proinflammatory cytokines: oligomerization of TRAF2 and TRAF6 is sufficient for JNK and IKK activation and target gene induction via an amino-terminal effector domain. Genes Dev. 13 (1999) 1297-1308
38. Chung J.Y., Park Y.C., Ye H., and Wu H. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J. Cell Sci. 115 (2002) 679-688
39. Song H.Y., Regnier C.H., Kirschning C.J., Goeddel D.V., and Rothe M. Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc. Natl. Acad. Sci. USA 94 (1997) 9792-9796
40. Cao Z., Xiong J., Takeuchi M., Kurama T., and Goeddel D.V. TRAF6 is a signal transducer for interleukin-1. Nature 383 (1996) 443-446
41. Curry H.A., Clemens R.A., Shah S.C., Bradbury M., Botero A., Goswami P., and Gius D. Heat shock inhibits radiation-induced activation of NF-κB via inhibition of IκB kinase. J. Biol. Chem. 274 (1999) 23061-23067
42. Yoo C., Lee G.S., Lee C.T., Kim Y.W., Han S.K., and Shim Y.S. Anti-inflammatory effect of heat shock protein induction is related to stabilization of IκBα through preventing IκB kinase activation in respiratory epithelial cells. J. Immunol. 164 (2000) 5416-5423
43. Shanley T.P., Ryan M.A., Eaves-Pyles T., and Wong H.R. Heat shock inhibits phosphorylation of I-kappaBalpha. Shock 14 (2000) 447-450
44. Lee K.H., Lee C.T., Kim Y.W., Han S.K., Shim Y.S., and Yoo C.G. Heat shock protein 70 negatively regulates heat-shock-induced suppression of the IκB/NFκB cascade by facilitating IκB kinase renaturation and blocking its further denaturation. Exp. Cell Res. 307 (2005) 276-284
45. Malhotra V., Eaves-Pyles T., Odoms K., Quaid G., Shanley T.P., and Wong H.R. Heat shock inhibits activation of NF-κB in the absence of heat shock factor-1. Biochem. Biophys. Res. Commun. 291 (2002) 453-457