CHIP facilitates ubiquitination of inducible nitric oxide synthase and promotes its proteasomal degradation

Cellular Immunology

Volumn 258, Issue 1, 2009, Pages 38-43

  Chen, Li ^a   Kong, Xiuqin ^a   Fu, Jin ^a   Xu, Yimiao ^a   Fang, Shuping ^a   Hua, Peng ^a   Luo, Lan ^b   Yin, Zhimin ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

CHIP; Degradation; Inflammation; iNOS; Ubiquitination

Indexed keywords

ARGININE; HEAT SHOCK PROTEIN 70 INTERACTING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE CHIP; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEGRADATION KINETICS; ENZYME DEGRADATION; HALF LIFE TIME; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ANIMALS; CELL LINE; HUMANS; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PLASMIDS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 67349084344     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2009.03.009     Document Type: Article

References (36)

1. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357 (2001) 593-615
2. Xu W., Liu L.Z., Loizidou M., Ahmed M., and Charles I.G. The role of nitric oxide in cancer. Cell Res. 12 (2002) 311-320
3. D'Acquisto F., Sautebin L., Iuvone T., Di Rosa M., and Carnuccio R. Prostaglandins prevent inducible nitric oxide synthase protein expression by inhibiting nuclear factor-kappaB activation in J774 macrophages. FEBS Lett. 440 (1998) 76-80
4. Aktan F. INOS-mediated nitric oxide production and its regulation. Life Sci. 75 (2004) 639-653
5. Crowell J.A., Steele V.E., Sigman C.C., and Fay J.R. Is inducible nitric oxide synthase a target for chemoprevention?. Mol. Cancer Ther. 2 (2003) 815-823
6. Musial A., and Eissa N.T. Inducible nitric-oxide synthase is regulated by the proteasome degradation pathway. J. Biol. Chem. 276 (2001) 24268-24273
7. Lancaster Jr. J.R., and Xie K. Tumors face NO problems?. Cancer. Res. 66 (2006) 6459-6462
8. Shah A.M. Inducible nitric oxide synthase and cardiovascular disease. Cardiovasc. Res. 45 (2000) 148-155
9. Kolodziejski P.J., Musial A., Koo J.S., and Eissa N.T. Ubiquitination of inducible nitric oxide synthase is required for its degradation. Proc. Natl. Acad. Sci. USA 99 (2002) 12315-12320
10. Ying W.Z., and Sanders P.W. Accelerated ubiquitination and proteasome degradation of a genetic variant of inducible nitric oxide synthase. Biochem. J. 376 (2003) 789-794
11. McDonough H., and Patterson C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8 (2003) 303-308
12. Ballinger C.A., Connell P., Wu Y., Hu Z., Thompson L.J., Yin L.Y., and Patterson C. Identification of CHIP, a novel tetratricopeptide repeat containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 19 (1999) 4535-4545
13. Murata S., Minami Y., Minami M., Chiba T., and Tanaka K. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2 (2001) 1133-1138
14. Jiang J., Ballinger C.A., Wu Y., Dai Q., Cyr D.M., Hohfeld J., and Patterson C. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 276 (2001) 42938-42944
15. Peng H.M., Morishima Y., Jenkins G.J., Dunbar A.Y., Lau M., Patterson C., Pratt W.B., and Osawa Y. Ubiquitylation of neuronal nitric-oxide synthase by CHIP, a chaperone-dependent E3 ligase. J. Biol. Chem. 279 (2004) 52970-52977
16. Xin H., Xu X.L., Li L.Y., Ning H.X., Rong Y., Shang Y., Wang Y.Y., Fu X.Y., and Chang Z.J. CHIP controls the sensitivity of transforming growth factor-β signaling by modulating the basal level of Smad3 through ubiquitin-mediated degradation. J. Biol. Chem. 280 (2005) 20842-20850
17. Xu W., Marcu M., Yuan X., Mimnaugh E., Patterson C., and Neckers L. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc. Natl. Acad. Sci. USA 99 (2002) 12847-12852
18. Petrucelli L., Dickson D., Kehoe K., Taylor J., Snyder H., Grover A., De Lucia M., McGowan E., Lewis J., Prihar G., Kim J., Dillmann W.H., Browne S.E., Hall A., Voellmy R., Tsuboi Y., Dawson T.M., Wolozin B., Hardy J., and Hutton M. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum. Mol. Genet. 13 (2004) 703-714
19. Meacham G.C., Patterson C., Zhang W., Younger J.M., and Cyr D.M. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell. Biol. 3 (2001) 100-105
20. Jiang J., Cyr D., Babbitt R.W., Sessa W.C., and Patterson C. Chaperone-dependent regulation of endothelial nitric-oxide synthase intracellular trafficking by the co-chaperone/ubiquitin ligase CHIP. J. Biol. Chem. 278 (2003) 49332-49341
21. Khurana A., Nakayama K., Williams S., Davis R.J., Mustelin T., and Ronai Z. Regulation of the ring finger E3 ligase Siah2 by p38 MAPK. J. Biol. Chem. 281 (2006) 35316-35326
22. Chen H., Wu Y., Zhang Y., Jin L., Luo L., Xue B., Lu C., Zhang X., and Yin Z. Hsp70 inhibits lipopolysaccharide-induced NF-κB activation by interacting with TRAF6 and inhibiting its ubiquitination. FEBS Lett. 580 (2006) 3145-3152
23. Li L., Xin H., Xu X., Huang M., Zhang X., Chen Y., Zhang S., Fu X.Y., and Chang Z. CHIP mediates degradation of Smad proteins and potentially regulates Smad-induced transcription. Mol. Cell. Biol. 24 (2004) 856-864
24. S.F. Kim, D.A. Huri, S.H. Snyder, Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2, Science 310 (1966-1970) 250.
25. 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 singaling by GSTp. EMBO J. 18 (1999) 1321-1334
26. Yoshida M., and Xia Y. Heat shock protein 90 as an endogenous protein enhancer of inducible nitric-oxide synthase. J. Biol. Chem. 278 (2003) 36953-36958
27. Kiang J.G. Inducible heat shock protein 70 kD and inducible nitric oxide synthase in hemorrhage/resuscitation-induced injury. Cell Res. 14 (2004) 450-459
28. Barnes P.J., and Liew F.Y. Nitric oxide and asthmatic inflammation. Immunol. Today 16 (1995) 128-130
29. Vodovotz Y., Lucia M.S., Flanders K.C., Chesler L., Xie Q.W., Smith T.W., Weidner J., Mumford R., Webber R., Nathan C., Roberts A.B., Lippa C.F., and Sporn M.B. Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J. Exp. Med. 184 (1996) 1425-1433
30. Iadecola C., Zhang F., Xu S., Casey R., and Ross M.E. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J. Cereb. Blood Flow Metab. 15 (1995) 378-384
31. Guo F.H., Suzy A., Comhair A., Zheng S., Dweik R.A., Eissa N.T., Thomassen M.J., Calhoun W., and Erzurum S.C. Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J. Immunol. 164 (2000) 5970-5980
32. Vodovotz Y., Bogdan C., Paik J., Xie Q.W., and Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. J. Exp. Med. 178 (1993) 605-613
33. Walker G., Pfeilschifter J., and Kunz D. Mechanisms of suppression of inducible nitric-oxide synthase (iNOS) expression in interferon (IFN)-γ-stimulated RAW 264.7 cells by dexamethasone. J. Biol. Chem. 272 (1996) 16679-16687
34. Bosco E.F., Bender F.C., Gautier F.C., Bron C., and Andrew F.G. Quest, Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc. Natl. Acad. Sci. USA 97 (2000) 14334-14339
35. Gallo M.P., Ghigo D., Bosia A., Alloatti G., Costamagna C., Penna C., and Levi R.C. Modulation of guinea-pig cardiac L-type calcium current by nitric oxide synthase inhibitors. J. Physiol. 506 (1998) 639-651
36. Thomsen L.L., Scott J.M.J., Topley P., Knowles R.G., Keerie A.J., and Frend A.J. Selective inhibition of inducible nitric oxide synthase inhibits tumor growth in vivo: studies with 1400W, a novel inhibitor. Cancer Res. 57 (1997) 3300-3304