Intrinsically disordered segments affect protein half-life in the cell and during evolution

Cell Reports

Volumn 8, Issue 6, 2014, Pages 1832-1844

  van der Lee, Robin ^a,b   Lang, Benjamin ^a   Kruse, Kai ^a   Gsponer, Jörg ^c   de Groot, Natalia Sánchezde ^a   Huynen, Martijn A ^b   Matouschek, Andreas ^d   Fuxreiter, Monika ^e   Babu, M Madan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^e UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; PROTEASOME; PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME STRUCTURE; EVOLUTION; GENE DUPLICATION; HALF LIFE TIME; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PARALOGY; PROTEIN METABOLISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; YEAST; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; METABOLISM; MOLECULAR EVOLUTION; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

ANIMALS; EVOLUTION, MOLECULAR; HALF-LIFE; HUMANS; MICE; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SOFTWARE;

EID: 84907406045     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.055     Document Type: Article

References (74)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J.Mol. Biol. 1990, 215:403-410.
2. Alvarez-Castelao B., Losada F., Ahicart P., Castaño J.G. The N-terminal region of Nurr1 (a.a 1-31) is essential for its efficient degradation by the ubiquitin proteasome pathway. PLoS ONE 2013, 8:e55999.
3. Babon J.J., McManus E.J., Yao S., DeSouza D.P., Mielke L.A., Sprigg N.S., Willson T.A., Hilton D.J., Nicola N.A., Baca M., et al. The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol. Cell 2006, 22:205-216.
4. Babu M.M., van der Lee R., de Groot N.S., Gsponer J. Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 2011, 21:432-440.
5. Babu M.M., Kriwacki R.W., Pappu R.V. Structural biology. Versatility from protein disorder. Science 2012, 337:1460-1461.
6. Barthelme D., Sauer R.T. Identification of the Cdc48•20S proteasome as an ancient AAA+ proteolytic machine. Science 2012, 337:843-846.
7. 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.
8. Berko D., Tabachnick-Cherny S., Shental-Bechor D., Cascio P., Mioletti S., Levy Y., Admon A., Ziv T., Tirosh B., Goldberg A.L., Navon A. The direction of protein entry into the proteasome determines the variety of products and depends on the force needed to unfold its two termini. Mol. Cell 2012, 48:601-611.
9. Beskow A., Grimberg K.B., Bott L.C., Salomons F.A., Dantuma N.P., Young P. A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation. J.Mol. Biol. 2009, 394:732-746.
10. Buljan M., Chalancon G., Dunker A.K., Bateman A., Balaji S., Fuxreiter M., Babu M.M. Alternative splicing of intrinsically disordered regions and rewiring of protein interactions. Curr. Opin. Struct. Biol. 2013, 23:443-450.
11. Carninci P., Sandelin A., Lenhard B., Katayama S., Shimokawa K., Ponjavic J., Semple C.A., Taylor M.S., Engström P.G., Frith M.C., et al. Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 2006, 38:626-635.
12. Cascio P., Hilton C., Kisselev A.F., Rock K.L., Goldberg A.L. 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J. 2001, 20:2357-2366.
13. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Biochim. Biophys. Acta 2012, 1824:3-13.
14. da Fonseca P.C., He J., Morris E.P. Molecular model of the human 26S proteasome. Mol. Cell 2012, 46:54-66.
15. Di Talia S., Skotheim J.M., Bean J.M., Siggia E.D., Cross F.R. The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 2007, 448:947-951.
16. Dosztányi Z., Csizmók V., Tompa P., Simon I. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J.Mol. Biol. 2005, 347:827-839.
17. Drury L.S., Perkins G., Diffley J.F. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 1997, 16:5966-5976.
18. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
19. Fishbain S., Prakash S., Herrig A., Elsasser S., Matouschek A. Rad23 escapes degradation because it lacks a proteasome initiation region. Nat. Commun. 2011, 2:192.
20. Fishbain S., Inobe T., Israeli E., Zokarkar A., Chavali S., Babu M.M., Matouschek A. The sequence composition of disordered regions affects protein half-life by controlling the initiation step of proteasomal degradation. Nat. Struct. Mol. Biol. 2014.
21. Gödderz D., Schäfer E., Palanimurugan R., Dohmen R.J. The N-terminal unstructured domain of yeast ODC functions as a transplantable and replaceable ubiquitin-independent degron. J.Mol. Biol. 2011, 407:354-367.
22. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
23. Groettrup M., Kirk C.J., Basler M. Proteasomes in immune cells: more than peptide producers?. Nat. Rev. Immunol. 2010, 10:73-78.
24. Gsponer J., Futschik M.E., Teichmann S.A., Babu M.M. Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 2008, 322:1365-1368.
25. Guttmann-Raviv N., Martin S., Kassir Y. Ime2, a meiosis-specific kinase in yeast, is required for destabilization of its transcriptional activator, Ime1. Mol. Cell. Biol. 2002, 22:2047-2056.
26. Hagai T., Azia A., Tóth-Petróczy Á., Levy Y. Intrinsic disorder in ubiquitination substrates. J.Mol. Biol. 2011, 412:319-324.
27. Henderson A., Erales J., Hoyt M.A., Coffino P. Dependence of proteasome processing rate on substrate unfolding. J.Biol. Chem. 2011, 286:17495-17502.
28. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
29. Hirata H., Bessho Y., Kokubu H., Masamizu Y., Yamada S., Lewis J., Kageyama R. Instability of Hes7 protein is crucial for the somite segmentation clock. Nat. Genet. 2004, 36:750-754.
30. Hutchins A.P., Liu S., Diez D., Miranda-Saavedra D. The repertoires of ubiquitinating and deubiquitinating enzymes in eukaryotic genomes. Mol. Biol. Evol. 2013, 30:1172-1187.
31. Inobe T., Fishbain S., Prakash S., Matouschek A. Defining the geometry of the two-component proteasome degron. Nat. Chem. Biol. 2011, 7:161-167.
32. Irimia M., Denuc A., Ferran J.L., Pernaute B., Puelles L., Roy S.W., Garcia-Fernàndez J., Marfany G. Evolutionarily conserved A-to-I editing increases protein stability of the alternative splicing factor Nova1. RNA Biol. 2012, 9:12-21.
33. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
34. Komander D., Clague M.J., Urbé S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10:550-563.
35. Kristensen A.R., Gsponer J., Foster L.J. Protein synthesis rate is the predominant regulator of protein expression during differentiation. Mol. Syst. Biol. 2013, 9:689.
36. Lakin N.D., Jackson S.P. Regulation of p53 in response to DNA damage. Oncogene 1999, 18:7644-7655.
37. Lander G.C., Estrin E., Matyskiela M.E., Bashore C., Nogales E., Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
38. Lange P.F., Overall C.M. Protein TAILS: when termini tell tales of proteolysis and function. Curr. Opin. Chem. Biol. 2013, 17:73-82.
39. Lasker K., Förster F., Bohn S., Walzthoeni T., Villa E., Unverdorben P., Beck F., Aebersold R., Sali A., Baumeister W. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. USA 2012, 109:1380-1387.
40. Legewie S., Herzel H., Westerhoff H.V., Blüthgen N. Recurrent design patterns in the feedback regulation of the mammalian signalling network. Mol. Syst. Biol. 2008, 4:190.
41. Levinson G., Gutman G.A. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 1987, 4:203-221.
42. Light S., Sagit R., Ekman D., Elofsson A. Long indels are disordered: a study of disorder and indels in homologous eukaryotic proteins. Biochim. Biophys. Acta 2013, 1834:890-897.
43. Liu C.W., Corboy M.J., DeMartino G.N., Thomas P.J. Endoproteolytic activity of the proteasome. Science 2003, 299:408-411.
44. Mao A.H., Lyle N., Pappu R.V. Describing sequence-ensemble relationships for intrinsically disordered proteins. Biochem. J. 2013, 449:307-318.
45. Obradovic Z., Peng K., Vucetic S., Radivojac P., Dunker A.K. Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 2005, 61(Suppl 7):176-182.
46. Pagano M., Tam S.W., Theodoras A.M., Beer-Romero P., Del Sal G., Chau V., Yew P.R., Draetta G.F., Rolfe M. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 1995, 269:682-685.
47. Peña M.M., Melo S.P., Xing Y.Y., White K., Barbour K.W., Berger F.G. The intrinsically disordered N-terminal domain of thymidylate synthase targets the enzyme to the ubiquitin-independent proteasomal degradation pathway. J.Biol. Chem. 2009, 284:31597-31607.
48. Peth A., Nathan J.A., Goldberg A.L. The ATP costs and time required to degrade ubiquitinated proteins by the 26S proteasome. J.Biol. Chem. 2013, 288:29215-29222.
49. Piwko W., Jentsch S. Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site. Nat. Struct. Mol. Biol. 2006, 13:691-697.
50. Prakash S., Tian L., Ratliff K.S., Lehotzky R.E., Matouschek A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 2004, 11:830-837.
51. Purvis J.E., Lahav G. Encoding and decoding cellular information through signaling dynamics. Cell 2013, 152:945-956.
52. Ramakrishna S., Suresh B., Lim K.H., Cha B.H., Lee S.H., Kim K.S., Baek K.H. PEST motif sequence regulating human NANOG for proteasomal degradation. Stem Cells Dev. 2011, 20:1511-1519.
53. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 2008, 9:679-690.
54. Rutkowski D.T., Arnold S.M., Miller C.N., Wu J., Li J., Gunnison K.M., Mori K., Sadighi Akha A.A., Raden D., Kaufman R.J. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006, 4:e374.
55. Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
56. Sharipo A., Imreh M., Leonchiks A., Imreh S., Masucci M.G. A minimal glycine-alanine repeat prevents the interaction of ubiquitinated I kappaB alpha with the proteasome: a new mechanism for selective inhibition of proteolysis. Nat. Med. 1998, 4:939-944.
57. Simister P.C., Schaper F., O'Reilly N., McGowan S., Feller S.M. Self-organization and regulation of intrinsically disordered proteins with folded N-termini. PLoS Biol. 2011, 9:e1000591.
58. Stadtmueller B.M., Hill C.P. Proteasome activators. Mol. Cell 2011, 41:8-19.
59. Takeuchi J., Chen H., Coffino P. Proteasome substrate degradation requires association plus extended peptide. EMBO J. 2007, 26:123-131.
60. Tian L., Holmgren R.A., Matouschek A. A conserved processing mechanism regulates the activity of transcription factors Cubitus interruptus and NF-kappaB. Nat. Struct. Mol. Biol. 2005, 12:1045-1053.
61. Tompa P. Intrinsically unstructured proteins evolve by repeat expansion. BioEssays 2003, 25:847-855.
62. Tompa P., Prilusky J., Silman I., Sussman J.L. Structural disorder serves as a weak signal for intracellular protein degradation. Proteins 2008, 71:903-909.
63. Tsvetkov P., Asher G., Paz A., Reuven N., Sussman J.L., Silman I., Shaul Y. Operational definition of intrinsically unstructured protein sequences based on susceptibility to the 20S proteasome. Proteins 2008, 70:1357-1366.
64. Tsvetkov P., Reuven N., Shaul Y. The nanny model for IDPs. Nat. Chem. Biol. 2009, 5:778-781.
65. van der Lee R., Buljan M., Lang B., Weatheritt R.J., Daughdrill G.W., Dunker A.K., Fuxreiter M., Gough J., Gsponer J., Jones D.T., et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 2014, 114:6589-6631.
66. van Ooijen G., Dixon L.E., Troein C., Millar A.J. Proteasome function is required for biological timing throughout the twenty-four hour cycle. Curr. Biol. 2011, 21:869-875.
67. Varshavsky A. The ubiquitin system, an immense realm. Annu. Rev. Biochem. 2012, 81:167-176.
68. Verhoef L.G., Heinen C., Selivanova A., Halff E.F., Salomons F.A., Dantuma N.P. Minimal length requirement for proteasomal degradation of ubiquitin-dependent substrates. FASEB J. 2009, 23:123-133.
69. Ward J.J., Sodhi J.S., McGuffin L.J., Buxton B.F., Jones D.T. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J.Mol. Biol. 2004, 337:635-645.
70. Wolfe K.H., Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713.
71. Yang C., Matro J.C., Huntoon K.M., Ye D.Y., Huynh T.T., Fliedner S.M., Breza J., Zhuang Z., Pacak K. Missense mutations in the human SDHB gene increase protein degradation without altering intrinsic enzymatic function. FASEB J. 2012, 26:4506-4516.
72. Yen H.C., Xu Q., Chou D.M., Zhao Z., Elledge S.J. Global protein stability profiling in mammalian cells. Science 2008, 322:918-923.
73. Zhang M., Coffino P. Repeat sequence of Epstein-Barr virus-encoded nuclear antigen 1 protein interrupts proteasome substrate processing. J.Biol. Chem. 2004, 279:8635-8641.
74. Zhao M., Zhang N.Y., Zurawel A., Hansen K.C., Liu C.W. Degradation of some polyubiquitinated proteins requires an intrinsic proteasomal binding element in the substrates. J.Biol. Chem. 2010, 285:4771-4780.