Smurf2-mediated ubiquitination and degradation of Id1 regulates p16 expression during senescence

Aging Cell

Volumn 10, Issue 6, 2011, Pages 1038-1046

  Kong, Yahui ^a   Cui, Hang ^a   Zhang, Hong ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

E3 ligase; Id1; P16; Senescence; Smurf2; Ubiquitination

Indexed keywords

INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; PROTEIN P16; PROTEIN SMURF2; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; COMPLEX FORMATION; DOWN REGULATION; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENESCENCE; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

CELL AGING; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; FIBROBLASTS; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; LENTIVIRUS; NEOPLASM PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 81155151472     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00746.x     Document Type: Article

References (45)

1. Alani RM, Young AZ, Shifflett CB (2001) Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc. Natl Acad. Sci. U S A 98, 7812-7816.
2. Barone MV, Pepperkok R, Peverali FA, Philipson L (1994) Id proteins control growth induction in mammalian cells. Proc. Natl Acad. Sci. U S A 91, 4985-4988.
3. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H (1990) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59.
4. Bond J, Jones C, Haughton M, DeMicco C, Kipling D, Wynford-Thomas D (2004) Direct evidence from siRNA-directed "knock down" that p16(INK4a) is required for human fibroblast senescence and for limiting ras-induced epithelial cell proliferation. Exp. Cell Res. 292, 151-156.
5. Bounpheng MA, Dimas JJ, Dodds SG, Christy BA (1999) Degradation of Id proteins by the ubiquitin-proteasome pathway. FASEB J. 13, 2257-2264.
6. Brookes S, Rowe J, Gutierrez Del Arroyo A, Bond J, Peters G (2004) Contribution of p16(INK4a) to replicative senescence of human fibroblasts. Exp. Cell Res. 298, 549-559.
7. Christy BA, Sanders LK, Lau LF, Copeland NG, Jenkins NA, Nathans D (1991) An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. Proc. Natl Acad. Sci. U S A 88, 1815-1819.
8. Collins CJ, Sedivy JM (2003) Involvement of the INK4a/Arf gene locus in senescence. Aging Cell 2, 145-150.
9. Cummings SD, Ryu B, Samuels MA, Yu X, Meeker AK, Healey MA, Alani RM (2008) Id1 delays senescence of primary human melanocytes. Mol. Carcinog. 47, 653-659.
10. Fajerman I, Schwartz AL, Ciechanover A (2004) Degradation of the Id2 developmental regulator: targeting via N-terminal ubiquitination. Biochem. Biophys. Res. Commun. 314, 505-512.
11. Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat. Rev. Mol. Cell Biol. 7, 667-677.
12. Hara E, Yamaguchi T, Nojima H, Ide T, Campisi J, Okayama H, Oda K (1994) Id-related genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269, 2139-2145.
13. Hara E, Uzman JA, Dimri GP, Nehlin JO, Testori A, Campisi J (1996) The helix-loop-helix protein Id-1 and a retinoblastoma protein binding mutant of SV40 T antigen synergize to reactivate DNA synthesis in senescent human fibroblasts. Dev. Genet. 18, 161-172.
14. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A (1999) Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J. Biol. Chem. 274, 19838-19845.
15. Iavarone A, Garg P, Lasorella A, Hsu J, Israel MA (1994) The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8, 1270-1284.
16. Ide T, Tsuji Y, Ishibashi S, Mitsui Y (1983) Reinitiation of host DNA synthesis in senescent human diploid cells by infection with Simian virus 40. Exp. Cell Res. 143, 343-349.
17. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE, Scadden DT (2006) Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 443, 421-426.
18. Kang Y, Chen CR, Massague J (2003) A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11, 915-926.
19. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL (2000) Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 6, 1365-1375.
20. Kim WY, Sharpless NE (2006) The regulation of INK4/ARF in cancer and aging. Cell 127, 265-275.
21. Kreider BL, Benezra R, Rovera G, Kadesch T (1992) Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255, 1700-1702.
22. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, Su L, Sharpless NE (2004) Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114, 1299-1307.
23. Krishnamurthy J, Ramsey MR, Ligon KL, Torrice C, Koh A, Bonner-Weir S, Sharpless NE (2006) p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 443, 453-457.
24. Lasorella A, Stegmuller J, Guardavaccaro D, Liu G, Carro MS, Rothschild G, de la Torre-Ubieta L, Pagano M, Bonni A, Iavarone A (2006) Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442, 471-474.
25. Lin X, Liang M, Feng XH (2000) Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 275, 36818-36822.
26. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670-677.
27. McConnell BB, Starborg M, Brookes S, Peters G (1998) Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr. Biol. 8, 351-354.
28. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443, 448-452.
29. Nickoloff BJ, Chaturvedi V, Bacon P, Qin JZ, Denning MF, Diaz MO (2000) Id-1 delays senescence but does not immortalize keratinocytes. J. Biol. Chem. 275, 27501-27504.
30. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E (2001) Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409, 1067-1070.
31. Perk J, Iavarone A, Benezra R (2005) Id family of helix-loop-helix proteins in cancer. Nat. Rev. Cancer 5, 603-614.
32. Qian Y, Chen X (2008) ID1, inhibitor of differentiation/DNA binding, is an effector of the p53-dependent DNA damage response pathway. J. Biol. Chem. 283, 22410-22416.
33. Riechmann V, van Cruchten I, Sablitzky F (1994) The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res. 22, 749-755.
34. Schwarze SR, DePrimo SE, Grabert LM, Fu VX, Brooks JD, Jarrard DF (2002) Novel pathways associated with bypassing cellular senescence in human prostate epithelial cells. J. Biol. Chem. 277, 14877-14883.
35. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88, 593-602.
36. Shay JW, Pereira-Smith OM, Wright WE (1991) A role for both RB and p53 in the regulation of human cellular senescence. Exp. Cell Res. 196, 33-39.
37. Suh HC, Leeanansaksiri W, Ji M, Klarmann KD, Renn K, Gooya J, Smith D, McNiece I, Lugthart S, Valk PJ, Delwel R, Keller JR (2008) Id1 immortalizes hematopoietic progenitors in vitro and promotes a myeloproliferative disease in vivo. Oncogene 27, 5612-5623.
38. Sun XH, Copeland NG, Jenkins NA, Baltimore D (1991) Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11, 5603-5611.
39. Tang J, Gordon GM, Nickoloff BJ, Foreman KE (2002) The helix-loop-helix protein id-1 delays onset of replicative senescence in human endothelial cells. Lab. Invest. 82, 1073-1079.
40. Trausch-Azar JS, Lingbeck J, Ciechanover A, Schwartz AL (2004) Ubiquitin-Proteasome-mediated degradation of Id1 is modulated by MyoD. J. Biol. Chem. 279, 32614-32619.
41. Vogt M, Haggblom C, Yeargin J, Christiansen-Weber T, Haas M (1998) Independent induction of senescence by p16INK4a and p21CIP1 in spontaneously immortalized human fibroblasts. Cell Growth Differ. 9, 139-146.
42. Zhang H, Cohen SN (2004) Smurf2 up-regulation activates telomere-dependent senescence. Genes Dev. 18, 3028-3040.
43. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R (2001) Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl Acad. Sci. U S A 98, 974-979.
44. Zhang H, Teng Y, Kong Y, Kowalski PE, Cohen SN (2008) Suppression of human tumor cell proliferation by Smurf2-induced senescence. J. Cell. Physiol. 215, 613-620.
45. Zheng W, Wang H, Xue L, Zhang Z, Tong T (2004) Regulation of cellular senescence and p16(INK4a) expression by Id1 and E47 proteins in human diploid fibroblast. J. Biol. Chem. 279, 31524-31532.