HUWE1 ubiquitinates MyoD and targets it for proteasomal degradation

Biochemical and Biophysical Research Communications

Volumn 418, Issue 2, 2012, Pages 408-413

  Noy, Tahel ^a   Suad, Oded ^a   Taglicht, Daniel ^b   Ciechanover, Aaron ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b Proteologics Ltd   (Israel)

Author keywords

HUWE1; MyoD; N terminal ubiquitination; Proteasome; Protein degradation; Ubiquitin

Indexed keywords

MYOD PROTEIN; PEPTIDES AND PROTEINS; PROTEIN HUWE1; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION;

GENE DELETION; HEK293 CELLS; HUMANS; MYOD PROTEIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84856662204     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.01.045     Document Type: Article

References (30)

1. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
2. Smith M.H., Ploegh H.L., Weissman J.S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 2011, 334:1086-1090.
3. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 2008, 9:679-690.
4. Berkes C.A., Tapscott S.J. MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol. 2005, 16:585-595.
5. Kay P.H., Pereira E., Marlow S.A., Turbett G., Mitchell C.A., Jacobsen P.F., Holliday R., Papadimitriou J.M. Evidence for adenine methylation within the mouse myogenic gene Myo-D1. Gene 1994, 151:89-95.
6. Sartorelli V., Puri P.L., Hamamori Y., Ogryzko V., Chung G., Nakatani Y., Wang J.Y., Kedes L. Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol. Cell 1999, 4:725-734.
7. Kitzmann M., Vandromme M., Schaeffer V., Carnac G., Labbe J.C., Lamb N., Fernandez A. Cdk1- and cdk2-mediated phosphorylation of MyoD Ser200 in growing C2 myoblasts: role in modulating MyoD half-life and myogenic activity. Mol. Cell Biol. 1999, 19:3167-3176.
8. Tintignac L.A., Sirri V., Leibovitch M.P., Lecluse Y., Castedo M., Metivier D., Kroemer G., Leibovitch S.A. Mutant MyoD lacking Cdc2 phosphorylation sites delays M-phase entry. Mol. Cell. Biol. 2004, 24:1809-1821.
9. Song A., Wang Q., Goebl M.G., Harrington M.A. Phosphorylation of nuclear MyoD is required for its rapid degradation. Mol. Cell. Biol. 1998, 18:4994-4999.
10. Jo C., Cho S.J., Jo S.A. Mitogen-activated protein kinase kinase 1 (MEK1) stabilizes MyoD through direct phosphorylation at tyrosine 156 during myogenic differentiation. J. Biol. Chem. 2011, 286:18903-18913.
11. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990, 61:49-59.
12. Abu Hatoum O., Gross-Mesilaty S., Breitschopf K., Hoffman A., Gonen H., Ciechanover A., Bengal E. Degradation of myogenic transcription factor MyoD by the ubiquitin pathway in vivo and in vitro: regulation by specific DNA binding. Mol. Cell. Biol. 1998, 18:5670-5677.
13. Breitschopf K., Bengal E., Ziv T., Admon A., 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. 1998, 17:5964-5973.
14. Lingbeck J.M., Trausch-Azar J.S., Ciechanover A., Schwartz A.L. Determinants of nuclear and cytoplasmic ubiquitin-mediated degradation of MyoD. J. Biol. Chem. 2003, 278:1817-1823.
15. Tintignac L.A., Lagirand J., Batonnet S., Sirri V., Leibovitch M.P., Leibovitch S.A. Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 2005, 280:2847-2856.
16. Zhong Q., Gao W., Du F., Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005, 121:1085-1095.
17. Chen D., Kon N., Li M., Zhang W., Qin J., Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005, 121:1071-1083.
18. Sadeh R., Breitschopf K., Bercovich B., Zoabi M., Kravtsova-Ivantsiv Y., Kornitzer D., Schwartz A., Ciechanover A. The N-terminal domain of MyoD is necessary and sufficient for its nuclear localization-dependent degradation by the ubiquitin system. Proc. Natl. Acad. Sci. USA 2008, 105:15690-15695.
19. Hershko A., Heller H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem. Biophys. Res. Commun. 1985, 128:1079-1086.
20. Hall J.R., Kow E., Nevis K.R., Lu C.K., Luce K.S., Zhong Q., Cook J.G. Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol. Biol. Cell 2007, 18:3340-3350.
21. Zaaroor-Regev D., de Bie P., Scheffner M., Noy T., Shemer R., Heled M., Stein I., Pikarsky E., Ciechanover A. Regulation of the polycomb protein Ring1B by self-ubiquitination or by E6-AP may have implications to the pathogenesis of Angelman syndrome. Proc. Natl Acad. Sci USA 2010, 107:6788-6793.
22. Salvat C., Wang G., Dastur A., Lyon N., Huibregtse J.M. The -4 phenylalanine is required for substrate ubiquitination catalyzed by HECT ubiquitin ligases. J. Biol. Chem. 2004, 279:18935-18943.
23. Singh R.K., Kabbaj M.H., Paik J., Gunjan A. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 2009, 11:925-933.
24. Adhikary S., Marinoni F., Hock A., Hulleman E., Popov N., Beier R., Bernard S., Quarto M., Capra M., Goettig S., Kogel U., Scheffner M., Helin K., Eilers M. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 2005, 123:409-421.
25. Zhao X., Heng J.I., Guardavaccaro D., Jiang R., Pagano M., Guillemot F., Iavarone A., Lasorella A. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat. Cell Biol. 2008, 10:643-653.
26. Herold S., Hock A., Herkert B., Berns K., Mullenders J., Beijersbergen R., Bernards R., Eilers M. Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1. EMBO J. 2008, 27:2851-2861.
27. Yang Y., Do H., Tian X., Zhang C., Liu X., Dada L.A., Sznajder J.I., Liu J. E3 ubiquitin ligase Mule ubiquitinates Miz1 and is required for TNFalpha-induced JNK activation. Proc. Natl. Acad. Sci. USA 2010, 107:13444-13449.
28. Parsons J.L., Tait P.S., Finch D., Dianova, Edelmann M.J., Khoronenkova S.V., Kessler B.M., Sharma R.A., McKenna W.G., Dianov G.L. Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J. 2009, 28:3207-3215.
29. Yin L., Joshi S., Wu N., Tong X., Lazar M.A. E3 ligases Arf-bp1 and Pam mediate lithium-stimulated degradation of the circadian heme receptor Rev-erb alpha. Proc. Natl. Acad. Sci. USA 2006, 107:11614-11619.
30. Liu Z., Oughtred R., Wing S.S. Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol. Cell Biol. 2005, 25:2819-2831.