Alternative Ubiquitin Activation/Conjugation Cascades Interact with N-End Rule Ubiquitin Ligases to Control Degradation of RGS Proteins

Molecular Cell

Volumn 43, Issue 3, 2011, Pages 392-405

  Lee, Peter C W ^a   Sowa, Mathew E ^a   Gygi, Steven P ^a   Harper, J Wade ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; PROTEIN UBA6; PROTEIN USE1; RGS PROTEIN; RGS4 PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME SUBSTRATE; HUMAN; IN VITRO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN METABOLISM; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CONSENSUS SEQUENCE; HEK293 CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PROTEIN STRUCTURE, TERTIARY; RGS PROTEINS; SEQUENCE ALIGNMENT; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

VERTEBRATA;

EID: 79960693484     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.05.034     Document Type: Article

References (43)

1. Aichem A., Pelzer C., Lukasiak S., Kalveram B., Sheppard P.W., Rani N., Schmidtke G., Groettrup M. USE1 is a bispecific conjugating enzyme for ubiquitin and FAT10, which FAT10ylates itself in cis. Nat. Commun. 2010, 1:13. 10.1038/ncomms1012.
2. An J.Y., Seo J.W., Tasaki T., Lee M.J., Varshavsky A., Kwon Y.T. Impaired neurogenesis and cardiovascular development in mice lacking the E3 ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 2006, 103:6212-6217.
3. Bartel B., Wünning I., Varshavsky A. The recognition component of the N-end rule pathway. EMBO J. 1990, 9:3179-3189.
4. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
5. Canaan A., Yu X., Booth C.J., Lian J., Lazar I., Gamfi S.L., Castille K., Kohya N., Nakayama Y., Liu Y.C., et al. FAT10/diubiquitin-like protein-deficient mice exhibit minimal phenotypic differences. Mol. Cell. Biol. 2006, 26:5180-5189.
6. Chiu Y.H., Sun Q., Chen Z.J. E1-L2 activates both ubiquitin and FAT10. Mol. Cell 2007, 27:1014-1023.
7. Ciechanover A., Finley D., Varshavsky A. Ubiquitin dependence of selective protein degradation demonstrated in the mammalian cell cycle mutant ts85. Cell 1984, 37:57-66.
8. Dantuma N.P., Lindsten K., Glas R., Jellne M., Masucci M.G. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 2000, 18:538-543.
9. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
10. Dohmen R.J., Madura K., Bartel B., Varshavsky A. The N-end rule is mediated by the UBC2(RAD6) ubiquitin-conjugating enzyme. Proc. Natl. Acad. Sci. USA 1991, 88:7351-7355.
11. Du F., Navarro-Garcia F., Xia Z., Tasaki T., Varshavsky A. Pairs of dipeptides synergistically activate the binding of substrate by ubiquitin ligase through dissociation of its autoinhibitory domain. Proc. Natl. Acad. Sci. USA 2002, 99:14110-14115.
12. Finley D., Ciechanover A., Varshavsky A. Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85. Cell 1984, 37:43-55.
13. Hershko A., Heller H., Elias S., Ciechanover A. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 1983, 258:8206-8214.
14. Hu R.G., Sheng J., Qi X., Xu Z., Takahashi T.T., Varshavsky A. The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 2005, 437:981-986.
15. Jin J., Li X., Gygi S.P., Harper J.W. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 2007, 447:1135-1138.
16. Kwon Y.T., Lévy F., Varshavsky A. Bivalent inhibitor of the N-end rule pathway. J. Biol. Chem. 1999, 274:18135-18139.
17. Kwon Y.T., Xia Z., Davydov I.V., Lecker S.H., Varshavsky A. Construction and analysis of mouse strains lacking the ubiquitin ligase UBR1 (E3alpha) of the N-end rule pathway. Mol. Cell. Biol. 2001, 21:8007-8021.
18. Kwon Y.T., Kashina A.S., Davydov I.V., Hu R.G., An J.Y., Seo J.W., Du F., Varshavsky A. An essential role of N-terminal arginylation in cardiovascular development. Science 2002, 297:96-99.
19. Kwon Y.T., Xia Z., An J.Y., Tasaki T., Davydov I.V., Seo J.W., Sheng J., Xie Y., Varshavsky A. Female lethality and apoptosis of spermatocytes in mice lacking the UBR2 ubiquitin ligase of the N-end rule pathway. Mol. Cell. Biol. 2003, 23:8255-8271.
20. Lee M.J., Tasaki T., Moroi K., An J.Y., Kimura S., Davydov I.V., Kwon Y.T. RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 2005, 102:15030-15035.
21. Lee M.J., Pal K., Tasaki T., Roy S., Jiang Y., An J.Y., Banerjee R., Kwon Y.T. Synthetic heterovalent inhibitors targeting recognition E3 components of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 2008, 105:100-105.
22. Lee S.Y., Lee H.Y., Kim S.D., Jo S.H., Shim J.W., Lee H.J., Yun J., Bae Y.S. Lysophosphatidylserine stimulates chemotactic migration in U87 human glioma cells. Biochem. Biophys. Res. Commun. 2008, 374:147-151.
23. Madura K., Dohmen R.J., Varshavsky A. N-recognin/Ubc2 interactions in the N-end rule pathway. J. Biol. Chem. 1993, 268:12046-12054.
24. Markson G., Kiel C., Hyde R., Brown S., Charalabous P., Bremm A., Semple J., Woodsmith J., Duley S., Salehi-Ashtiani K., et al. Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res. 2009, 19:1905-1911.
25. Matta-Camacho E., Kozlov G., Li F.F., Gehring K. Structural basis of substrate recognition and specificity in the N-end rule pathway. Nat. Struct. Mol. Biol. 2010, 17:1182-1187.
26. Nalepa G., Rolfe M., Harper J.W. Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discov. 2006, 5:596-613.
27. Pelzer C., Kassner I., Matentzoglu K., Singh R.K., Wollscheid H.P., Scheffner M., Schmidtke G., Groettrup M. UBE1L2, a novel E1 enzyme specific for ubiquitin. J. Biol. Chem. 2007, 282:23010-23014.
28. Petroski M.D., Deshaies R.J. Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 2005, 123:1107-1120.
29. Pickart C.M. Back to the future with ubiquitin. Cell 2004, 116:181-190.
30. Schulman B.A., Harper J.W. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 2009, 10:319-331.
31. Sowa M.E., Bennett E.J., Gygi S.P., Harper J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138:389-403.
32. Sriram S.M., Kwon Y.T. The molecular principles of N-end rule recognition. Nat. Struct. Mol. Biol. 2010, 17:1164-1165.
33. Tasaki T., Kwon Y.T. The mammalian N-end rule pathway: new insights into its components and physiological roles. Trends Biochem. Sci. 2007, 32:520-528.
34. Tasaki T., Mulder L.C., Iwamatsu A., Lee M.J., Davydov I.V., Varshavsky A., Muesing M., Kwon Y.T. A family of mammalian E3 ubiquitin ligases that contain the UBR box motif and recognize N-degrons. Mol. Cell. Biol. 2005, 25:7120-7136.
35. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
36. van Wijk S.J., de Vries S.J., Kemmeren P., Huang A., Boelens R., Bonvin A.M., Timmers H.T. A comprehensive framework of E2-RING E3 interactions of the human ubiquitin-proteasome system. Mol. Syst. Biol. 2009, 5:295.
37. Varshavsky A. The N-end rule: functions, mysteries, uses. Proc. Natl. Acad. Sci. USA 1996, 93:12142-12149.
38. Wójcik C., Rowicka M., Kudlicki A., Nowis D., McConnell E., Kujawa M., DeMartino G.N. Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol. Biol. Cell 2006, 17:4606-4618.
39. Xia Z., Webster A., Du F., Piatkov K., Ghislain M., Varshavsky A. Substrate-binding sites of UBR1, the ubiquitin ligase of the N-end rule pathway. J. Biol. Chem. 2008, 283:24011-24028.
40. Xie Y., Varshavsky A. The E2-E3 interaction in the N-end rule pathway: the RING-H2 finger of E3 is required for the synthesis of multiubiquitin chain. EMBO J. 1999, 18:6832-6844.
41. Ye Y., Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10:755-764.
42. Zenker M., Mayerle J., Lerch M.M., Tagariello A., Zerres K., Durie P.R., Beier M., Hülskamp G., Guzman C., Rehder H., et al. Deficiency of UBR1, a ubiquitin ligase of the N-end rule pathway, causes pancreatic dysfunction, malformations and mental retardation (Johanson-Blizzard syndrome). Nat. Genet. 2005, 37:1345-1350.
43. Zheng N., Wang P., Jeffrey P.D., Pavletich N.P. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 2000, 102:533-539.