Comprehensive profiling of proteome changes upon sequential deletion of deubiquitylating enzymes

Journal of Proteomics

Volumn 75, Issue 13, 2012, Pages 3886-3897

  Poulsen, Jon W ^a   Madsen, Christian T ^a   Young, Clifford ^a   Kelstrup, Christian D ^a   Grell, Heidi C ^a   Henriksen, Peter ^a   Juhl Jensen, Lars ^a   Nielsen, Michael L ^a  

^a University of Copenhagen   (Denmark)

Author keywords

Bioinformatic analysis; Deubiquitylating enzymes; Q exactive; Quantitative mass spectrometry; Yeast

Indexed keywords

CELL PROTEIN; DEUBIQUITYLATING ENZYME; PROTEINASE; PROTEOME; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; ENZYME SUBSTRATE; EUKARYOTIC CELL; FUNCTIONAL PROTEOMICS; FUNGAL STRAIN; GENE REGULATORY NETWORK; ISOTOPE LABELING; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE;

ENDOPEPTIDASES; GENE KNOCKOUT TECHNIQUES; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84862676006     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.04.055     Document Type: Article

References (51)

1. van Kasteren S.I., Kramer H.B., Jensen H.H., Campbell S.J., Kirkpatrick J., Oldham N.J., et al. Expanding the diversity of chemical protein modification allows post-translational mimicry. Nature 2007, 446(7139):1105-1109.
2. Mann M., Jensen O.N. Proteomic analysis of post-translational modifications. Nat Biotechnol 2003, 21(3):255-261.
3. Hershko A., Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
4. Finley D., Ciechanover A., Varshavsky A. Ubiquitin as a central cellular regulator. Cell 2004, 116(2 Suppl.):S29-S32. 2 pp. following S32.
5. Pickart C.M. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001, 70:503-533.
6. Scheffner M., Nuber U., Huibregtse J.M. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 1995, 373(6509):81-83.
7. Wilkinson K.D. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 1997, 11(14):1245-1256.
8. Reyes-Turcu F.E., Ventii K.H., Wilkinson K.D. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009, 78:363-397.
9. Kessler B.M., Fortunati E., Melis M., Pals C.E., Clevers H., Maurice M.M. Proteome changes induced by knock-down of the deubiquitylating enzyme HAUSP/USP7. J Proteome Res 2007, 6(11):4163-4172.
10. Hochstrasser M. Ubiquitin-dependent protein degradation. Annu Rev Genet 1996, 30:405-439.
11. Goffeau A., Barrell B.G., Bussey H., Davis R.W., Dujon B., Feldmann H., et al. Life with 6000 genes. Science 1996, 274(5287). 546, 563-7.
12. Danielsen J.M., Sylvestersen K.B., Bekker-Jensen S., Szklarczyk D., Poulsen J.W., Horn H., et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteomics 2011, 10(3). M110 003590.
13. Xu G., Paige J.S., Jaffrey S.R. Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat Biotechnol 2010, 28(8):868-873.
14. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 2011, 44(2):325-340.
15. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., et al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 2011, 10(10). M111 013284.
16. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002, 1(5):376-386.
17. Nielsen M.L., Vermeulen M., Bonaldi T., Cox J., Moroder L., Mann M. Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nat Methods 2008, 5(6):459-460.
18. Rappsilber J., Ishihama Y., Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 2003, 75(3):663-670.
19. Michalski A., Damoc E., Hauschild J.P., Lange O., Wieghaus A., Makarov A., et al. Mass Spectrometry-based Proteomics Using Q Exactive, a High-performance Benchtop Quadrupole Orbitrap Mass Spectrometer. Mol Cell Proteomics 2011, 10(9). M111 011015.
20. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26(12):1367-1372.
21. Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 2011, 10(4):1794-1805.
22. D. Abdulrehman, P.T. Monteiro, M.C. Teixeira, N.P. Mira, A.B. Lourenco, S.C. dos Santos et al. YEASTRACT: providing a programmatic access to curated transcriptional regulatory associations in Saccharomyces cerevisiae through a web services interface. Nucleic Acids Res 2011;39(Database issue):D136-40.
23. Amerik A.Y., Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta 2004, 1695(1-3):189-207.
24. Nijman S.M., Luna-Vargas M.P., Velds A., Brummelkamp T.R., Dirac A.M., Sixma T.K., et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123(5):773-786.
25. Kirisako T., Ichimura Y., Okada H., Kabeya Y., Mizushima N., Yoshimori T., et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 2000, 151(2):263-276.
26. Amerik A.Y., Li S.J., Hochstrasser M. Analysis of the deubiquitinating enzymes of the yeast Saccharomyces cerevisiae. Biol Chem 2000, 381(9-10):981-992.
27. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Frohlich F., et al. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455(7217):1251-1254.
28. Soufi B., Kelstrup C.D., Stoehr G., Frohlich F., Walther T.C., Olsen J.V. Global analysis of the yeast osmotic stress response by quantitative proteomics. Mol Biosyst 2009, 5(11):1337-1346.
29. Ong S.E., Mann M. Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 2005, 1(5):252-262.
30. Emre N.C., Ingvarsdottir K., Wyce A., Wood A., Krogan N.J., Henry K.W., et al. Maintenance of low histone ubiquitylation by Ubp10 correlates with telomere-proximal Sir2 association and gene silencing. Mol Cell 2005, 17(4):585-594.
31. Daniel J.A., Torok M.S., Sun Z.W., Schieltz D., Allis C.D., Yates J.R., et al. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 2004, 279(3):1867-1871.
32. Gardner R.G., Nelson Z.W., Gottschling D.E. Ubp10/Dot4p regulates the persistence of ubiquitinated histone H2B: distinct roles in telomeric silencing and general chromatin. Mol Cell Biol 2005, 25(14):6123-6139.
33. Nogales-Cadenas R., Carmona-Saez P., Vazquez M., Vicente C., Yang X., Tirado F., et al. GeneCodis: interpreting gene lists through enrichment analysis and integration of diverse biological information. Nucleic Acids Res 2009, 37:W317-W322. [Web Server issue].
34. Robzyk K., Recht J., Osley M.A. Rad6-dependent ubiquitination of histone H2B in yeast. Science 2000, 287(5452):501-504.
35. Qin S., Wang Q., Ray A., Wani G., Zhao Q., Bhaumik S.R., et al. Sem1p and Ubp6p orchestrate telomeric silencing by modulating histone H2B ubiquitination and H3 acetylation. Nucleic Acids Res 2009, 37(6):1843-1853.
36. Singer J.D., Manning B.M., Formosa T. Coordinating DNA replication to produce one copy of the genome requires genes that act in ubiquitin metabolism. Mol Cell Biol 1996, 16(4):1356-1366.
37. Regelmann J., Schule T., Josupeit F.S., Horak J., Rose M., Entian K.D., et al. Catabolite degradation of fructose-1,6-bisphosphatase in the yeast Saccharomyces cerevisiae: a genome-wide screen identifies eight novel GID genes and indicates the existence of two degradation pathways. Mol Biol Cell 2003, 14(4):1652-1663.
38. Moazed D., Johnson D. A deubiquitinating enzyme interacts with SIR4 and regulates silencing in S. cerevisiae. Cell 1996, 86(4):667-677.
39. Cohen M., Stutz F., Belgareh N., Haguenauer-Tsapis R., Dargemont C. Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat Cell Biol 2003, 5(7):661-667.
40. Cohen M., Stutz F., Dargemont C. Deubiquitination, a new player in Golgi to endoplasmic reticulum retrograde transport. J Biol Chem 2003, 278(52):51989-51992.
41. Peng J., Schwartz D., Elias J.E., Thoreen C.C., Cheng D., Marsischky G., et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 2003, 21(8):921-926.
42. Schmitz C., Kinner A., Kolling R. The deubiquitinating enzyme Ubp1 affects sorting of the ATP-binding cassette-transporter Ste6 in the endocytic pathway. Mol Biol Cell 2005, 16(3):1319-1329.
43. Kolling R., Hollenberg C.P. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J 1994, 13(14):3261-3271.
44. Hellauer K., Akache B., MacPherson S., Sirard E., Turcotte B. Zinc cluster protein Rdr1p is a transcriptional repressor of the PDR5 gene encoding a multidrug transporter. J Biol Chem 2002, 277(20):17671-17676.
45. Hikkel I., Lucau-Danila A., Delaveau T., Marc P., Devaux F., Jacq C. A general strategy to uncover transcription factor properties identifies a new regulator of drug resistance in yeast. J Biol Chem 2003, 278(13):11427-11432.
46. Gao C., Wang L., Milgrom E., Shen W.C. On the mechanism of constitutive Pdr1 activator-mediated PDR5 transcription in Saccharomyces cerevisiae: evidence for enhanced recruitment of coactivators and altered nucleosome structures. J Biol Chem 2004, 279(41):42677-42686.
47. Coe J.G., Murray L.E., Dawes I.W. Identification of a sporulation-specific promoter regulating divergent transcription of two novel sporulation genes in Saccharomyces cerevisiae. Mol Gen Genet 1994, 244(6):661-672.
48. Deutschbauer A.M., Williams R.M., Chu A.M., Davis R.W. Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2002, 99(24):15530-15535.
49. Santiago T.C., Mamoun C.B. Genome expression analysis in yeast reveals novel transcriptional regulation by inositol and choline and new regulatory functions for Opi1p, Ino2p, and Ino4p. J Biol Chem 2003, 278(40):38723-38730.
50. G.M. Carman, G.S. Han. Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem 80:859-83.
51. Jesch S.A., Zhao X., Wells M.T., Henry S.A. Genome-wide analysis reveals inositol, not choline, as the major effector of Ino2p-Ino4p and unfolded protein response target gene expression in yeast. J Biol Chem 2005, 280(10):9106-9118.