Differential Ubiquitination of Smad1 Mediated by CHIP: Implications in the Regulation of the Bone Morphogenetic Protein Signaling Pathway

Journal of Molecular Biology

Volumn 374, Issue 3, 2007, Pages 777-790

  Li, Ren Feng ^a   Shang, Yu ^a,b   Liu, Di ^a   Ren, Ze Song ^a   Chang, Zhijie ^a,b   Sui, Sen Fang ^a  

^a TSINGHUA UNIVERSITY   (China)

^b Tsinghua University   (China)

Author keywords

BMP; CHIP; Hsp70; Smad1; ubiquitination

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CARBOXYL GROUP; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; LYSINE; SMAD1 PROTEIN; SMAD5 PROTEIN; UBIQUITIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; UBIQUITINATION;

EID: 35548989214     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.082     Document Type: Article

References (62)

1. Hershko A., and Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67 (1998) 425-479
2. Izzi L., and Attisano L. Regulation of the TGFbeta signalling pathway by ubiquitin-mediated degradation. Oncogene 23 (2004) 2071-2078
3. Shi Y., and Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700
4. Attisano L., and Wrana J.L. Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12 (2000) 235-243
5. Derynck R., Zhang Y., and Feng X.H. Smads: transcriptional activators of TGF-beta responses. Cell 95 (1998) 737-740
6. Heldin C.H., Miyazono K., and ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390 (1997) 465-471
7. Nakao A., Afrakhte M., Moren A., Nakayama T., Christian J.L., Heuchel R., et al. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389 (1997) 631-635
8. Imamura T., Takase M., Nishihara A., Oeda E., Hanai J., Kawabata M., and Miyazono K. Smad6 inhibits signalling by the TGF-beta superfamily. Nature 389 (1997) 622-626
9. Zhu H., Kavsak P., Abdollah S., Wrana J.L., and Thomsen G.H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400 (1999) 687-693
10. Kavsak P., Rasmussen R.K., Causing C.G., Bonni S., Zhu H., Thomsen G.H., and Wrana J.L. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 6 (2000) 1365-1375
11. Lin X., Liang M., and Feng X.H. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 275 (2000) 36818-36822
12. Zhang Y., Chang C., Gehling D.J., Hemmati-Brivanlou A., and Derynck R. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl Acad. Sci. USA 98 (2001) 974-979
13. Moren A., Imamura T., Miyazono K., Heldin C.H., and Moustakas A. Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J. Biol. Chem. 280 (2005) 22115-22123
14. Fukuchi M., Imamura T., Chiba T., Ebisawa T., Kawabata M., Tanaka K., and Miyazono K. Ligand-dependent degradation of Smad3 by a ubiquitin ligase complex of ROC1 and associated proteins. Mol. Biol. Cell 12 (2001) 1431-1443
15. Gruendler C., Lin Y., Farley J., and Wang T. Proteasomal degradation of Smad1 induced by bone morphogenetic proteins. J. Biol. Chem. 276 (2001) 46533-46543
16. 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
17. Connell P., Ballinger C.A., Jiang J., Wu Y., Thompson L.J., Hohfeld J., and Patterson C. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nature Cell Biol. 3 (2001) 93-96
18. 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
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. Nature Cell Biol. 3 (2001) 100-105
20. 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
21. Shigetsugu Hatakeyama M.Y., Matsumoto M., Ishida N., and Nakayama a.K.-I. U Box proteins as a new family of ubiquitin-protein ligases*. J. Biol. Chem. 276 (2001) 33111-33120
22. Alberti S., Demand J., Esser C., Emmerich N., Schild H., and Hohfeld J. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J. Biol. Chem. 277 (2002) 45920-45927
23. Imai Y., Soda M., Hatakeyama S., Akagi T., Hashikawa T., Nakayama K.I., and Takahashi R. CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol. Cell 10 (2002) 55-67
24. Wiederkehr T., Bukau B., and Buchberger A. Protein turnover: a CHIP programmed for proteolysis. Curr. Biol. 12 (2002) R26-R28
25. 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
26. Zhou P., Fernandes N., Dodge I.L., Reddi A.L., Rao N., Safran H., et al. ErbB2 degradation mediated by the co-chaperone protein CHIP. J. Biol. Chem. 278 (2003) 13829-13837
27. Li L., Xin H., Xu X., Huang M., Zhang X., Chen Y., et al. CHIP mediates degradation of Smad proteins and potentially regulates Smad-induced transcription. Mol. Cell. Biol. 24 (2004) 856-864
28. Li R.F., Zhang F., Lu Y.J., and Sui S.F. Specific interaction between Smad1 and CHIP: a surface plasmon resonance study. Colloids Surf. B Biointerfs. 40 (2005) 133-136
29. Xin H., Xu X., Li L., Ning H., Rong Y., Shang Y., et al. CHIP controls the sensitivity of transforming growth factor-beta signaling by modulating the basal level of Smad3 through ubiquitin-mediated degradation. J. Biol. Chem. 280 (2005) 20842-20850
30. Xu Z., Devlin K.I., Ford M.G., Nix J.C., Qin J., and Misra S. Structure and interactions of the helical and U-box domains of CHIP, the C terminus of HSP70 interacting protein. Biochemistry 45 (2006) 4749-4759
31. Zhang M., Windheim M., Roe S.M., Peggie M., Cohen P., Prodromou C., and Pearl L.H. Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 20 (2005) 525-538
32. Lin X., Liang M., Liang Y.Y., Brunicardi F.C., Melchior F., and Feng X.H. Activation of transforming growth factor-beta signaling by SUMO-1 modification of tumor suppressor Smad4/DPC4. J. Biol. Chem. 278 (2003) 18714-18719
33. Chacko B.M., Qin B., Correia J.J., Lam S.S., de Caestecker M.P., and Lin K. The L3 loop and C-terminal phosphorylation jointly define Smad protein trimerization. Nature Struct. Biol. 8 (2001) 248-253
34. Qin B.Y., Chacko B.M., Lam S.S., de Caestecker M.P., Correia J.J., and Lin K. Structural basis of Smad1 activation by receptor kinase phosphorylation. Mol. Cell 8 (2001) 1303-1312
35. Rees I., Lee S., Kim H., and Tsai F.T. The E3 ubiquitin ligase CHIP binds the androgen receptor in a phosphorylation-dependent manner. Biochim. Biophys. Acta 1764 (2006) 1073-1079
36. Wu S.J., Liu F.H., Hu S.M., and Wang C. Different combinations of the heat-shock cognate protein 70 (hsc70) C-terminal functional groups are utilized to interact with distinct tetratricopeptide repeat-containing proteins. Biochem. J. 359 (2001) 419-426
37. Long J., Wang G., He D., and Liu F. Repression of Smad4 transcriptional activity by SUMO modification. Biochem. J. 379 (2004) 23-29
38. Liang M., Melchior F., Feng X.H., and Lin X. Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1. J. Biol. Chem. 279 (2004) 22857-22865
39. Lin X., Liang M., Liang Y.Y., Brunicardi F.C., and Feng X.H. SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J. Biol. Chem. 278 (2003) 31043-31048
40. Lee P.S., Chang C., Liu D., and Derynck R. Sumoylation of Smad4, the common Smad mediator of transforming growth factor-beta family signaling. J. Biol. Chem. 278 (2003) 27853-27863
41. Moren A., Hellman U., Inada Y., Imamura T., Heldin C.H., and Moustakas A. Differential ubiquitination defines the functional status of the tumor suppressor Smad4. J. Biol. Chem. 278 (2003) 33571-33582
42. Simonsson M., Heldin C.H., Ericsson J., and Gronroos E. The balance between acetylation and deacetylation controls Smad7 stability. J. Biol. Chem. 280 (2005) 21797-21803
43. Gronroos E., Hellman U., Heldin C.H., and Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol. Cell 10 (2002) 483-493
44. Shi Y., Wang Y.F., Jayaraman L., Yang H., Massague J., and Pavletich N.P. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-beta signaling. Cell 94 (1998) 585-594
45. Chai J., Wu J.W., Yan N., Massague J., Pavletich N. P., and Shi Y. Features of a Smad3 MH1-DNA complex. Roles of water and zinc in DNA binding. J. Biol. Chem. 278 (2003) 20327-20331
46. Breitschopf K., Bengal E., Ziv T., Admon A., and Ciechanover A. A novel site for ubiquitination: the N-terminal residue, and not internal lysines of MyoD, is essential for conjugation and degradation of the protein. EMBO J. 17 (1998) 5964-5973
47. Aviel S., Winberg G., Massucci M., and Ciechanover A. Degradation of the epstein-barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. Targeting via ubiquitination of the N-terminal residue. J. Biol. Chem. 275 (2000) 23491-23499
48. Reinstein E., Scheffner M., Oren M., Ciechanover A., and Schwartz A. Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Oncogene 19 (2000) 5944-5950
49. Ikeda M., Ikeda A., and Longnecker R. Lysine-independent ubiquitination of Epstein-Barr virus LMP2A. Virology 300 (2002) 153-159
50. Bloom J., Amador V., Bartolini F., DeMartino G., and Pagano M. Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115 (2003) 71-82
51. Ben-Saadon R., Fajerman I., Ziv T., Hellman U., Schwartz A.L., and Ciechanover A. The tumor suppressor protein p16(INK4a) and the human papillomavirus oncoprotein-58 E7 are naturally occurring lysine-less proteins that are degraded by the ubiquitin system. Direct evidence for ubiquitination at the N-terminal residue. J. Biol. Chem. 279 (2004) 41414-41421
52. Ciechanover A., and Ben-Saadon R. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 14 (2004) 103-106
53. Coulombe P., Rodier G., Bonneil E., Thibault P., and Meloche S. N-terminal ubiquitination of extracellular signal-regulated kinase 3 and p21 directs their degradation by the proteasome. Mol. Cell. Biol. 24 (2004) 6140-6150
54. Doolman R., Leichner G.S., Avner R., and Roitelman J. Ubiquitin is conjugated by membrane ubiquitin ligase to three sites, including the N terminus, in transmembrane region of mammalian 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for sterol-regulated enzyme degradation. J. Biol. Chem. 279 (2004) 38184-38193
55. Fajerman I., Schwartz A.L., and Ciechanover A. Degradation of the Id2 developmental regulator: targeting via N-terminal ubiquitination. Biochem. Biophys. Res. Commun. 314 (2004) 505-512
56. Kuo M.L., den Besten W., Bertwistle D., Roussel M. F., and Sherr C.J. N-terminal polyubiquitination and degradation of the Arf tumor suppressor. Genes Dev. 18 (2004) 1862-1874
57. Kirisako T., Kamei K., Murata S., Kato M., Fukumoto H., Kanie M., et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25 (2006) 4877-4887
58. Senga T., Sivaprasad U., Zhu W., Park J.H., Arias E.E., Walter J.C., and Dutta A. PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem. 281 (2006) 6246-6252
59. Seibert V., Prohl C., Schoultz I., Rhee E., Lopez R., Abderazzaq K., et al. Combinatorial diversity of fission yeast SCF ubiquitin ligases by homo- and heterooligomeric assemblies of the F-box proteins Pop1p and Pop2p. BMC Biochem. 3 (2002) 22
60. Gonen H., Bercovich B., Orian A., Carrano A., Takizawa C., Yamanaka K., et al. Identification of the ubiquitin carrier proteins, E2s, involved in signal-induced conjugation and subsequent degradation of IkappaBalpha. J. Biol. Chem. 274 (1999) 14823-14830
61. Ravid T., and Hochstrasser M. Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nature Cell Biol. 9 (2007) 422-427
62. Li W., Tu D., Brunger A.T., and Ye Y. A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446 (2007) 333-337