Site-Specific Identification of SUMO-2 Targets in Cells Reveals an Inverted SUMOylation Motif and a Hydrophobic Cluster SUMOylation Motif

Molecular Cell

Volumn 39, Issue 4, 2010, Pages 641-652

  Matic, Ivan ^a   Schimmel, Joost ^b   Hendriks, Ivo A ^b   van Santen, Maria A ^b   van de Rijke, Frans ^b   van Dam, Hans ^b   Gnad, Florian ^a   Mann, Matthias ^a   Vertegaal, Alfred C O ^b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Proteins

Indexed keywords

LYSINE; SERINE; SUMO 2 PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NOP5/NOP58 PROTEIN, HUMAN; NUCLEAR PROTEIN; RANGAP1 PROTEIN, HUMAN; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; SUMO PROTEIN; SUMO2 PROTEIN, HUMAN;

ARTICLE; CONJUGATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEOMICS; AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROCEDURES; PROTEIN PROCESSING; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; HYDROPHOBICITY; LYSINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TANDEM MASS SPECTROMETRY; TRANSFECTION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS;

EUKARYOTA;

EID: 77955999636     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.07.026     Document Type: Article

References (57)

1. Bergink S., Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009, 458:461-467.
2. Bernier-Villamor V., Sampson D.A., Matunis M.J., Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 2002, 108:345-356.
3. Blomster H.A., Imanishi S.Y., Siimes J., Kastu J., Morrice N.A., Eriksson J.E., Sistonen L. In vivo identification of sumoylation sites by a signature tag and cysteine-targeted affinity purification. J. Biol. Chem. 2010, 285:19324-19329.
4. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
5. Cox J., Mann M. Is proteomics the new genomics?. Cell 2007, 130:395-398.
6. 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, 26:1367-1372.
7. Cox J., Matic I., Hilger M., Nagaraj N., Selbach M., Olsen J.V., Mann M. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 2009, 4:698-705.
8. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., Greff Z., Keri G., Stemmann O., Mann M. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 2008, 31:438-448.
9. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Frohlich F., Walther T.C., Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
10. Denison C., Rudner A.D., Gerber S.A., Bakalarski C.E., Moazed D., Gygi S.P. A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol. Cell. Proteomics 2005, 4:246-254.
11. Deweindt C., Albagli O., Bernardin F., Dhordain P., Quief S., Lantoine D., Kerckaert J.P., Leprince D. The LAZ3/BCL6 oncogene encodes a sequence-specific transcriptional inhibitor: a novel function for the BTB/POZ domain as an autonomous repressing domain. Cell Growth Differ. 1995, 6:1495-1503.
12. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
13. Gill G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15:536-541.
14. Gnad F., Ren S., Cox J., Olsen J.V., Macek B., Oroshi M., Mann M. PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol. 2007, 8:R250.
15. Golebiowski F., Matic I., Tatham M.H., Cole C., Yin Y., Nakamura A., Cox J., Barton G.J., Mann M., Hay R.T. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal 2009, 2:ra24.
16. Hay R.T. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 2007, 17:370-376.
17. Hietakangas V., Anckar J., Blomster H.A., Fujimoto M., Palvimo J.J., Nakai A., Sistonen L. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 2006, 103:45-50.
18. Hsiao H.H., Meulmeester E., Frank B.T., Melchior F., Urlaub H. " ChopNspice" , a mass-spectrometric approach that allows identification of endogenous SUMO-conjugated peptides. Mol. Cell. Proteomics 2009, 8:2664-2675.
19. Ikeda F., Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep. 2008, 9:536-542.
20. Jeon B.N., Choi W.I., Yu M.Y., Yoon A.R., Kim M.H., Yun C.O., Hur M.W. ZBTB2, a novel master regulator of the p53 pathway. J. Biol. Chem. 2009, 284:17935-17946.
21. Jeram S.M., Srikumar T., Pedrioli P.G., Raught B. Using mass spectrometry to identify ubiquitin and ubiquitin-like protein conjugation sites. Proteomics 2009, 9:922-934.
22. Knuesel M., Cheung H.T., Hamady M., Barthel K.K., Liu X. A method of mapping protein sumoylation sites by mass spectrometry using a modified small ubiquitin-like modifier 1 (SUMO-1) and a computational program. Mol. Cell. Proteomics 2005, 4:1626-1636.
23. Koh D.I., Choi W.I., Jeon B.N., Lee C.E., Yun C.O., Hur M.W. A novel POK family transcription factor, ZBTB5, represses transcription of p21CIP1 gene. J. Biol. Chem. 2009, 284:19856-19866.
24. Li J.Y., English M.A., Ball H.J., Yeyati P.L., Waxman S., Licht J.D. Sequence-specific DNA binding and transcriptional regulation by the promyelocytic leukemia zinc finger protein. J. Biol. Chem. 1997, 272:22447-22455.
25. Macek B., Mann M., Olsen J.V. Global and site-specific quantitative phosphoproteomics: principles and applications. Annu. Rev. Pharmacol. Toxicol. 2009, 49:199-221.
26. Mahajan R., Gerace L., Melchior F. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 1998, 140:259-270.
27. Makhnevych T., Sydorskyy Y., Xin X., Srikumar T., Vizeacoumar F.J., Jeram S.M., Li Z., Bahr S., Andrews B.J., Boone C., Raught B. Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol. Cell 2009, 33:124-135.
28. Matic I., van Hagen M., Schimmel J., Macek B., Ogg S.C., Tatham M.H., Hay R.T., Lamond A.I., Mann M., Vertegaal A.C. In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol. Cell. Proteomics 2008, 7:132-144.
29. Matunis M.J., Wu J., Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 1998, 140:499-509.
30. Mayor T., Graumann J., Bryan J., MacCoss M.J., Deshaies R.J. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell. Proteomics 2007, 6:1885-1895.
31. Meulmeester E., Kunze M., Hsiao H.H., Urlaub H., Melchior F. Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell 2008, 30:610-619.
32. Mohideen F., Capili A.D., Bilimoria P.M., Yamada T., Bonni A., Lima C.D. A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 2009, 16:945-952.
33. Mukhopadhyay D., Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 2007, 32:286-295.
34. Numoto M., Niwa O., Kaplan J., Wong K.K., Merrell K., Kamiya K., Yanagihara K., Calame K. Transcriptional repressor ZF5 identifies a new conserved domain in zinc finger proteins. Nucleic Acids Res. 1993, 21:3767-3775.
35. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
36. Olsen J.V., Macek B., Lange O., Makarov A., Horning S., Mann M. Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 2007, 4:709-712.
37. Olsen J.V., Schwartz J.C., Griep-Raming J., Nielsen M.L., Damoc E., Denisov E., Lange O., Remes P., Taylor D., Splendore M., et al. A dual pressure linear ion trap orbitrap instrument with very high sequencing speed. Mol. Cell. Proteomics 2009, 8:2759-2769.
38. Pedrioli P.G., Raught B., Zhang X.D., Rogers R., Aitchison J., Matunis M., Aebersold R. Automated identification of SUMOylation sites using mass spectrometry and SUMmOn pattern recognition software. Nat. Methods 2006, 3:533-539.
39. Peng J., Schwartz D., Elias J.E., Thoreen C.C., Cheng D., Marsischky G., Roelofs J., Finley D., Gygi S.P. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 2003, 21:921-926.
40. Rappsilber J., Mann M., Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2007, 2:1896-1906.
41. Ross S., Best J.L., Zon L.I., Gill G. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 2002, 10:831-842.
42. Roukens M.G., Alloul-Ramdhani M., Vertegaal A.C., Anvarian Z., Balog C.I., Deelder A.M., Hensbergen P.J., Baker D.A. Identification of a new site of sumoylation on Tel (ETV6) uncovers a PIAS-dependent mode of regulating Tel function. Mol. Cell. Biol. 2008, 28:2342-2357.
43. Schimmel J., Larsen K.M., Matic I., van Hagen M., Cox J., Mann M., Andersen J.S., Vertegaal A.C. The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol. Cell. Proteomics 2008, 7:2107-2122.
44. Schimmel J., Balog C.I., Deelder A.M., Drijfhout J.W., Hensbergen P.J., Vertegaal A.C. Positively charged amino acids flanking a sumoylation consensus tetramer on the 110kDa tri-snRNP component SART1 enhance sumoylation efficiency. J. Proteomics 2010, 73:1523-1534.
45. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 2006, 1:2856-2860.
46. Soderberg O., Gullberg M., Jarvius M., Ridderstrale K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
47. Soderberg O., Leuchowius K.J., Gullberg M., Jarvius M., Weibrecht I., Larsson L.G., Landegren U. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 2008, 45:227-232.
48. Tashiro S., Muto A., Tanimoto K., Tsuchiya H., Suzuki H., Hoshino H., Yoshida M., Walter J., Igarashi K. Repression of PML nuclear body-associated transcription by oxidative stress-activated Bach2. Mol. Cell. Biol. 2004, 24:3473-3484.
49. Vertegaal A.C., Ogg S.C., Jaffray E., Rodriguez M.S., Hay R.T., Andersen J.S., Mann M., Lamond A.I. A proteomic study of SUMO-2 target proteins. J. Biol. Chem. 2004, 279:33791-33798.
50. Vertegaal A.C., Andersen J.S., Ogg S.C., Hay R.T., Mann M., Lamond A.I. Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 2006, 5:2298-2310.
51. Westman B.J., Verheggen C., Hutten S., Lam Y.W., Bertrand E., Lamond A. A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 2010, 39:618-631. this issue.
52. Wilson V.G., Heaton P.R. Ubiquitin proteolytic system: focus on SUMO. Expert Rev. Proteomics 2008, 5:121-135.
53. Witze E.S., Old W.M., Resing K.A., Ahn N.G. Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 2007, 4:798-806.
54. Wohlschlegel J.A., Johnson E.S., Reed S.I., Yates J.R. Improved identification of SUMO attachment sites using C-terminal SUMO mutants and tailored protease digestion strategies. J. Proteome Res. 2006, 5:761-770.
55. Xu L., Wei Y., Reboul J., Vaglio P., Shin T.H., Vidal M., Elledge S.J., Harper J.W. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 2003, 425:316-321.
56. Yang S.H., Galanis A., Witty J., Sharrocks A.D. An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J. 2006, 25:5083-5093.
57. Zhuang M., Calabrese M.F., Liu J., Waddell M.B., Nourse A., Hammel M., Miller D.J., Walden H., Duda D.M., Seyedin S.N., et al. Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases. Mol. Cell 2009, 36:39-50.