Numerous proteins with unique characteristics are degraded by the 26S proteasome following monoubiquitination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 32, 2016, Pages E4639-E4647

  Braten, Ori ^a   Livneh, Ido ^a   Ziv, Tamar ^a   Admon, Arie ^a   Kehat, Izhak ^a   Caspi, Lilac H ^a   Gonen, Hedva ^a   Bercovich, Beatrice ^a   Godzik, Adam ^b   Jahandideh, Samad ^b   Jaroszewski, Lukasz ^b   Sommer, Thomas ^c   Kwon, Yong Tae ^d   Guharoy, Mainak ^e   Tompa, Peter ^e,f   Ciechanover, Aaron ^a,d  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b BURNHAM INSTITUTE   (United States)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d Seoul National University   (South Korea)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^f INSTITUTE OF ENZYMOLOGY   (Hungary)

Author keywords

26S proteasome; Monoubiquitination; Protein degradation; Ubiquitin replacement

Indexed keywords

26S PROTEASOME; PROTEASOME; UBIQUITIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE; PROTEIN;

CONFERENCE PAPER; CONTROLLED STUDY; HUMAN; HUMAN CELL; MONOUBIQUITINATION; NONHUMAN; POLYMERIZATION; POLYUBIQUITINATION; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; SCREENING; UBIQUITINATION; WILD TYPE; YEAST; CHEMISTRY; MCF-7 CELL LINE; METABOLISM; PHYSIOLOGY; PROTEOMICS;

HUMANS; MCF-7 CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; PROTEOMICS; UBIQUITINATION;

EID: 84982921570     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1608644113     Document Type: Article

References (63)

1. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol Rev 82(2):373-428.
2. Komander D (2009) The emerging complexity of protein ubiquitination. Biochem Soc Trans 37(Pt 5):937-953.
3. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19(1):94-102.
4. Hicke L, Schubert HL, Hill CP (2005) Ubiquitin-binding domains. Nat Rev Mol Cell Biol 6(8):610-621.
5. Hoeller D, et al. (2006) Regulation of ubiquitin-binding proteins by monoubiquitination. Nat Cell Biol 8(2):163-169.
6. Goh LK, Sorkin A (2013) Endocytosis of receptor tyrosine kinases. Cold Spring Harb Perspect Biol 5(5):a017459.
7. Ahearn IM, Haigis K, Bar-Sagi D, Philips MR (2011) Regulating the regulator: Posttranslational modification of RAS. Nat Rev Mol Cell Biol 13(1):39-51.
8. Jura N, Scotto-Lavino E, Sobczyk A, Bar-Sagi D (2006) Differential modification of Ras proteins by ubiquitination. Mol Cell 21(5):679-687.
9. Chandrasekharan MB, Huang F, Sun ZW (2009) Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci USA 106(39):16686-16691.
10. Rott R, et al. (2011) α-Synuclein fate is determined by USP9X-regulated monoubiquitination. Proc Natl Acad Sci USA 108(46):18666-18671.
11. Dimova NV, et al. (2012) APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat Cell Biol 14(2):168-176.
12. Carvallo L, et al. (2010) Non-canonical Wnt signaling induces ubiquitination and degradation of Syndecan4. J Biol Chem 285(38):29546-29555.
13. Boutet SC, Disatnik MH, Chan LS, Iori K, Rando TA (2007) Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130(2):349-362.
14. Kravtsova-Ivantsiv Y, Cohen S, Ciechanover A (2009) Modification by single ubiquitin moieties rather than polyubiquitination is sufficient for proteasomal processing of the p105 NF-kappaB precursor. Mol Cell 33(4):496-504.
15. Shabek N, et al. (2012) The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation. Mol Cell 48(1): 87-97.
16. Braten O, Shabek N, Kravtsova-Ivantsiv Y, Ciechanover A (2012) Generation of free ubiquitin chains is up-regulated in stress and facilitated by the HECT domain ubiquitin ligases UFD4 and HUL5. Biochem J 444(3):611-617.
17. Hospenthal MK, Freund SM, Komander D (2013) Assembly, analysis and architecture of atypical ubiquitin chains. Nat Struct Mol Biol 20(5):555-565.
18. Sun T, et al. (2011) The role of monoubiquitination in endocytic degradation of human ether-a-go-go-related gene (hERG) channels under low K+ conditions. J Biol Chem 286(8):6751-6759.
19. Ward CL, Omura S, Kopito RR (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83(1):121-127.
20. Finley D, et al. (1994) Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. MolCellBiol14(8):5501-5509.
21. Xu M, Skaug B, Zeng W, Chen ZJ (2009) A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol Cell 36(2):302-314.
22. Emanuele MJ, et al. (2011) Global identification of modular cullin-RING ligase substrates. Cell 147(2):459-474.
23. Mayor T, Graumann J, Bryan J, MacCoss MJ, Deshaies RJ (2007) Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol Cell Proteomics 6(11):1885-1895.
24. Kim W, et al. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44(2):325-340.
25. Tompa P (2011) Unstructural biology coming of age. Curr Opin Struct Biol 21(3): 419-425.
26. van der Lee R, et al. (2014) Classification of intrinsically disordered regions and proteins. Chem Rev 114(13):6589-6631.
27. Guharoy M, Bhowmick P, Tompa P (2016) Design principles involving protein disorder facilitate specific substrate selection and degradation by the ubiquitin-proteasome system. J Biol Chem 291(13):6723-6731.
28. Guharoy M, Bhowmick P, Sallam M, Tompa P (2016) Tripartite degrons confer diversity and specificity on regulated protein degradation in the ubiquitin-proteasome system. Nat Commun 7:10239.
29. Inobe T, Fishbain S, Prakash S, Matouschek A (2011) Defining the geometry of the two-component proteasome degron. Nat Chem Biol 7(3):161-167.
30. Ravid T, Hochstrasser M (2008) Diversity of degradation signals in the ubiquitinproteasome system. Nat Rev Mol Cell Biol 9(9):679-690.
31. King RW, Glotzer M, Kirschner MW (1996) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol Biol Cell 7(9):1343-1357.
32. Iakoucheva LM, et al. (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32(3):1037-1049.
33. Dunker AK, et al. (2001) Intrinsically disordered protein. J Mol Graph Model 19(1): 26-59.
34. Landry CR, Levy ED, Michnick SW (2009) Weak functional constraints on phosphoproteomes. Trends Genet 25(5):193-197.
35. Eden E, Lipson D, Yogev S, Yakhini Z (2007) Discovering motifs in ranked lists of DNA sequences. PLoS Comput Biol 3(3):e39.
36. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z (2009) GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
37. Amanchy R, et al. (2007) A curated compendium of phosphorylation motifs. Nat Biotechnol 25(3):285-286.
38. Basu A, et al. (2009) Proteome-wide prediction of acetylation substrates. Proc Natl Acad Sci USA 106(33):13785-13790.
39. Chou MF, Schwartz D (2011) Biological sequence motif discovery using Motif-X. Curr Protoc Bioinformatics Chap 13:Unit 13.15-24.
40. Hershko A, Ganoth D, Pehrson J, Palazzo RE, Cohen LH (1991) Methylated ubiquitin inhibits cyclin degradation in clam embryo extracts. J Biol Chem 266(25):16376-16379.
41. Amerik AYu, Swaminathan S, Krantz BA, Wilkinson KD, Hochstrasser M (1997) In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J 16(16):4826-4838.
42. Lee DH, Goldberg AL (1996) Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J Biol Chem 271(44):27280-27284.
43. Milner E, et al. (2013) The effect of proteasome inhibition on the generation of the human leukocyte antigen (HLA) peptidome. Mol Cell Proteomics 12(7):1853-1864.
44. Udeshi ND, et al. (2013) Refined preparation and use of anti-diglycine remnant (K-e-GG) antibody enables routine quantification of 10,000s of ubiquitination sites in single proteomics experiments. Mol Cell Proteomics 12(3):825-831.
45. Haglund K, et al. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5(5):461-466.
46. Liu X, Yu X, Zack DJ, Zhu H, Qian J (2008) TiGER: A database for tissue-specific gene expression and regulation. BMC Bioinformatics 9:271.
47. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141-172.
48. Ikner A, Shiozaki K (2005) Yeast signaling pathways in the oxidative stress response. Mutat Res 569(1-2):13-27.
49. Gasch AP, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11(12):4241-4257.
50. David Y, Ziv T, Admon A, Navon A (2010) The E2 ubiquitin-conjugating enzymes direct polyubiquitination to preferred lysines. J Biol Chem 285(12):8595-8604.
51. Rape M, Kirschner MW (2004) Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432(7017):588-595.
52. Ravid T, Hochstrasser M (2007) Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat Cell Biol 9(4):422-427.
53. Amemiya Y, Azmi P, Seth A (2008) Autoubiquitination of BCA2 RING E3 ligase regulates its own stability and affects cell migration. Mol Cancer Res 6(9):1385-1396.
54. Lorick KL, et al. (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA 96(20):11364-11369.
55. Noels H, et al. (2009) Auto-ubiquitination-induced degradation of MALT1-API2 prevents BCL10 destabilization in t(11;18)(q21;q21)-positive MALT lymphoma. PLoS One 4(3):e4822.
56. Danielsen JM, et al. (2011) Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteomics 10(3):M110.003590.
57. Spence J, Sadis S, Haas AL, Finley D (1995) A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol Cell Biol 15(3):1265-1273.
58. Hershko A, Eytan E, Ciechanover A, Haas AL (1982) Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins. J Biol Chem 257(23):13964-13970.
59. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108(2):193-199.
60. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
61. Gietz RD, Woods RA (2006) Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol Biol 313:107-120.
62. Dormond E, et al. (2010) An efficient process for the purification of helper-dependent adenoviral vector and removal of helper virus by iodixanol ultracentrifugation. J Virol Methods 165(1):83-89.
63. Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21(16):3433-3434.