Principles of cotranslational ubiquitination and quality control at the ribosome

Molecular Cell

Volumn 50, Issue 3, 2013, Pages 379-393

  Duttler, Stefanie ^a   Pechmann, Sebastian ^a   Frydman, Judith ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MESSENGER RNA; UBIQUITIN PROTEIN LIGASE E3; PEPTIDE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; COTRANSLATIONAL UBIQUITINATION; DISSOCIATION; HOMEOSTASIS; IMMUNOBLOTTING; IN VIVO STUDY; NONHUMAN; POLYSOME; PREMATURITY; PROTEOMICS; QUALITY CONTROL; RIBOSOME; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; GENETICS; METABOLISM; PROTEIN FOLDING; PROTEIN SYNTHESIS;

EUKARYOTA;

MOLECULAR CHAPERONES; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; QUALITY CONTROL; RIBOSOMES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84883210213     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.03.010     Document Type: Article

References (58)

1. Albanèse V., Yam A.Y., Baughman J., Parnot C., Frydman J. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 2006, 124:75-88.
2. Balch W.E., Morimoto R.I., Dillin A., Kelly J.W. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
3. Belle A., Tanay A., Bitincka L., Shamir R., O'Shea E.K. Quantification of protein half-lives in the budding yeast proteome. Proc. Natl. Acad. Sci. USA 2006, 103:13004-13009.
4. Bengtson M.H., Joazeiro C.A.P. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 2010, 467:470-473.
5. Brandman O., Stewart-Ornstein J., Wong D., Larson A., Williams C.C., Li G.W., Zhou S., King D., Shen P.S., Weibezahn J., et al. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 2012, 151:1042-1054.
6. Chen P., Johnson P., Sommer T., Jentsch S., Hochstrasser M. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MAT alpha 2 repressor. Cell 1993, 74:357-369.
7. Chu J., Hong N.A., Masuda C.A., Jenkins B.V., Nelms K.A., Goodnow C.C., Glynne R.J., Wu H., Masliah E., Joazeiro C.A., Kay S.A. A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc. Natl. Acad. Sci. USA 2009, 106:2097-2103.
8. Collart M.A., Panasenko O.O. The Ccr4-not complex. Gene 2012, 492:42-53.
9. del Alamo M., Hogan D.J., Pechmann S., Albanese V., Brown P.O., Frydman J. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 2011, 9:e1001100.
10. Dimitrova L.N., Kuroha K., Tatematsu T., Inada T. Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J. Biol. Chem. 2009, 284:10343-10352.
11. Doma M.K., Parker R. RNA quality control in eukaryotes. Cell 2007, 131:660-668.
12. Fang N.N., Ng A.H., Measday V., Mayor T. Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat. Cell Biol. 2011, 13:1344-1352.
13. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
14. Fleischer T.C., Weaver C.M., McAfee K.J., Jennings J.L., Link A.J. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 2006, 20:1294-1307.
15. Frydman J., Hartl F.U. Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms. Science 1996, 272:1497-1502.
16. Frydman J., Nimmesgern E., Ohtsuka K., Hartl F.U. Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 1994, 370:111-117.
17. Funakoshi M., Sasaki T., Nishimoto T., Kobayashi H. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc. Natl. Acad. Sci. USA 2002, 99:745-750.
18. George R., Beddoe T., Landl K., Lithgow T. The yeast nascent polypeptide-associated complex initiates protein targeting to mitochondria in vivo. Proc. Natl. Acad. Sci. USA 1998, 95:2296-2301.
19. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
20. Hagai T., Azia A., Tóth-Petróczy å., Levy Y. Intrinsic disorder in ubiquitination substrates. J. Mol. Biol. 2011, 412:319-324.
21. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
22. Henderson A., Erales J., Hoyt M.A., Coffino P. Dependence of proteasome processing rate on substrate unfolding. J. Biol. Chem. 2011, 286:17495-17502.
23. Ito-Harashima S., Kuroha K., Tatematsu T., Inada T. Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev. 2007, 21:519-524.
24. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
25. Kramer G., Boehringer D., Ban N., Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16:589-597.
26. Lelouard H., Ferrand V., Marguet D., Bania J., Camosseto V., David A., Gatti E., Pierre P. Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J. Cell Biol. 2004, 164:667-675.
27. Mayor T., Deshaies R.J. Two-step affinity purification of multiubiquitylated proteins from Saccharomyces cerevisiae. Methods Enzymol. 2005, 399:385-392.
28. Nakatogawa H., Ito K. Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol. Cell 2001, 7:185-192.
29. Netzer W.J., Hartl F.U. Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms. Trends Biochem. Sci. 1998, 23:68-73.
30. O'Brien E.P., Vendruscolo M., Dobson C.M. Prediction of variable translation rate effects on cotranslational protein folding. Nat. Commun. 2012, 3:868.
31. Olzscha H., Schermann S.M., Woerner A.C., Pinkert S., Hecht M.H., Tartaglia G.G., Vendruscolo M., Hayer-Hartl M., Hartl F.U., Vabulas R.M. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 2011, 144:67-78.
32. Oromendia A.B., Dodgson S.E., Amon A. Aneuploidy causes proteotoxic stress in yeast. Genes Dev. 2012, 26:2696-2708.
33. Ouyang Z., Liang J. Predicting protein folding rates from geometric contact and amino acid sequence. Protein Sci. 2008, 17:1256-1263.
34. Pechmann S., Frydman J. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 2013, 20:237-243.
35. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
36. Preissler S., Deuerling E. Ribosome-associated chaperones as key players in proteostasis. Trends Biochem. Sci. 2012, 37:274-283.
37. Radivojac P., Vacic V., Haynes C., Cocklin R.R., Mohan A., Heyen J.W., Goebl M.G., Iakoucheva L.M. Identification, analysis, and prediction of protein ubiquitination sites. Proteins 2010, 78:365-380.
38. Rechsteiner M., Rogers S.W. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 1996, 21:267-271.
39. Reits E.A.J., Vos J.C., Grommé M., Neefjes J. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 2000, 404:774-778.
40. Russell S.J., Steger K.A., Johnston S.A. Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J. Biol. Chem. 1999, 274:21943-21952.
41. Sato S., Ward C.L., Kopito R.R. Cotranslational ubiquitination of cystic fibrosis transmembrane conductance regulator in vitro. J. Biol. Chem. 1998, 273:7189-7192.
42. Schubert U., Antón L.C., Gibbs J., Norbury C.C., Yewdell J.W., Bennink J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
43. Seufert W., Jentsch S. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 1990, 9:543-550.
44. Sha Z., Brill L.M., Cabrera R., Kleifeld O., Scheliga J.S., Glickman M.H., Chang E.C., Wolf D.A. The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. Mol. Cell 2009, 36:141-152.
45. Siwiak M., Zielenkiewicz P. A comprehensive, quantitative, and genome-wide model of translation. PLoS Comput. Biol. 2010, 6:e1000865.
46. Taylor R.C., Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 2011, 3:3.
47. Theodoraki M.A., Nillegoda N.B., Saini J., Caplan A.J. A network of ubiquitin ligases is important for the dynamics of misfolded protein aggregates in yeast. J. Biol. Chem. 2012, 287:23911-23922.
48. Thulasiraman V., Yang C.F., Frydman J. In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 1999, 18:85-95.
49. Trotter E.W., Kao C.M.-F., Berenfeld L., Botstein D., Petsko G.A., Gray J.V. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J. Biol. Chem. 2002, 277:44817-44825.
50. Turner G.C., Varshavsky A. Detecting and measuring cotranslational protein degradation in vivo. Science 2000, 289:2117-2120.
51. Turner G.C., Du F., Varshavsky A. Peptides accelerate their uptake by activating a ubiquitin-dependent proteolytic pathway. Nature 2000, 405:579-583.
52. Vabulas R.M., Hartl F.U. Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 2005, 310:1960-1963.
53. Verma R., Oania R., Fang R., Smith G.T., Deshaies R.J. Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol. Cell 2011, 41:82-92.
54. von der Haar T. A quantitative estimation of the global translational activity in logarithmically growing yeast cells. BMC Syst. Biol. 2008, 2:87.
55. Willmund F., del Alamo M., Pechmann S., Chen T., Albanèse V., Dammer E.B., Peng J., Frydman J. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 2013, 152:196-209.
56. Yam A.Y., Albanèse V., Lin H.T., Frydman J. Hsp110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J. Biol. Chem. 2005, 280:41252-41261.
57. Yewdell J.W., Nicchitta C.V. The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol. 2006, 27:368-373.
58. Zhou M., Fisher E.A., Ginsberg H.N. Regulated Co-translational ubiquitination of apolipoprotein B100. A new paradigm for proteasomal degradation of a secretory protein. J. Biol. Chem. 1998, 273:24649-24653.