System-wide changes to sumo modifications in response to heat shock

Science Signaling

Volumn 2, Issue 72, 2009, Pages

  Golebiowski, Filip ^a   Matic, Ivan ^b   Tatham, Michael H ^a   Cole, Christian ^a   Yin, Yili ^a   Nakamura, Akihiro ^c   Cox, Jürgen ^b   Barton, Geoffrey J ^a   Mann, Matthias ^b   Hay, Ronald T ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c GUNMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN; BIOPOLYMER; PROTEOME; SUMO 1 PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL SURVIVAL; CONTROLLED STUDY; DATA ANALYSIS; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; ENZYME SUBSTRATE; HEAT SHOCK; HUMAN; HUMAN CELL; MASS SPECTROMETRY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; PROTEOMICS; QUANTITATIVE ANALYSIS; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; HEAT SHOCK RESPONSE; HELA CELL; METABOLISM; VALIDATION STUDY;

EUKARYOTA;

BIOPOLYMERS; CELL SURVIVAL; HEAT-SHOCK RESPONSE; HELA CELLS; HUMANS; PROTEOME; SUMO-1 PROTEIN;

EID: 67649173012     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000282     Document Type: Article

References (54)

1. J. Terzic, I. Marinovic-Terzic, F. Ikeda, I. Dikic, Ubiquitin signals in the NF-kB pathway. Biochem. Soc. Trans. 35, 942-945 (2007).
2. O. Kerscher, R. Felberbaum, M. Hochstrasser, Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180 (2006).
3. M. H. Tatham, E. Jaffray, O. A. Vaughan, J. M. Desterro, C. H. Botting, J. H. Naismith, R. T. Hay, Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368-35374 (2001).
4. A. C. Vertegaal, J. S. Andersen, S. C. Ogg, R. T. Hay, M. Mann, A. I. Lamond, Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 5, 2298-2310 (2006).
5. F. P. Zhang, L.Mikkonen, J. Toppari, J. J. Palvimo, I. Thesleff, O. A. Jänne, Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 28, 5381-5390 (2008).
6. I. Matic, M. van Hagen, J. Schimmel, B. Macek, S. C. Ogg, M. H. Tatham, R. T. Hay, A. I. Lamond, M. Mann, A. C. Vertegaal, In vivo identification of human small ubiquitinlike modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol. Cell. Proteomics 7, 132-144 (2008).
7. H. Saitoh, J. Hinchey, Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258 (2000).
8. E. S. Witze, W. M. Old, K. A. Resing, N. G. Ahn, Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4, 798-806 (2007).
9. M. H. Tatham, M. C. Geoffroy, L. Shen, A. Plechanovova, N. Hattersley, E. G. Jaffray, J. J. Palvimo, R. T. Hay, RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546 (2008).
10. G. Rigaut, A. Shevchenko, B. Rutz, M. Wilm, M. Mann, B. Séraphin, A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032 (1999).
11. M. Mann, Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7, 952-958 (2006).
12. J. Cox, M. Mann, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
13. V. Hietakangas, J. K. Ahlskog, A.M. Jakobsson, M. Hellesuo, N. M. Sahlberg, C. I. Holmberg, A. Mikhailov, J. J. Palvimo, L. Pirkkala, L. Sistonen, Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953-2968 (2003).
14. M. T. Vassileva, M. J. Matunis, SUMO modification of heterogeneous nuclear ribonucleoproteins. Mol. Cell. Biol. 24, 3623-3632 (2004).
15. S. Tian, H. Poukka, J. J. Palvimo, O. A. Jänne, Small ubiquitin-related modifier-1 (SUMO-1) modification of the glucocorticoid receptor. Biochem. J. 367, 907-911 (2002).
16. Y. Kawabe, M. Seki, T. Seki,W. S.Wang, O. Imamura, Y. Furuichi, H. Saitoh, T. Enomoto, Covalent modification of the Werner's syndrome gene product with the ubiquitin-related protein, SUMO-1. J. Biol. Chem. 275, 20963-20966 (2000).
17. M. S. Rodriguez, C. Dargemont, R. T. Hay, SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659 (2001).
18. F. Melchior, M. Schergaut, A. Pichler, SUMO: Ligases, isopeptidases and nuclear pores. Trends Biochem. Sci. 28, 612-618 (2003).
19. S. Weger, E. Hammer, R. Heilbronn, Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett. 579, 5007-5012 (2005).
20. S. Lindquist, The heat-shock response. Annu. Rev. Biochem. 55, 1151-1191 (1986).
21. L. H. Pearl, C. Prodromou, P. Workman, The Hsp90 molecular chaperone: An open and shut case for treatment. Biochem. J. 410, 439-453 (2008).
22. S. Dorion, J. Landry, Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress Chaperones 7, 200-206 (2002).
23. H. S. Skaggs, H. Xing, D. C. Wilkerson, L. A. Murphy, Y. Hong, C. N. Mayhew, K. D. Sarge, HSF1-TPR interaction facilitates export of stress-induced HSP70 mRNA. J. Biol. Chem. 282, 33902-33907 (2007).
24. H. Kaneko, K. Igarashi, K. Kataoka, M. Miura, Heat shock induces phosphorylation of histone H2AX in mammalian cells. Biochem. Biophys. Res. Commun. 328, 1101-1106 (2005).
25. A. Takahashi, H. Matsumoto, K. Nagayama, M. Kitano, S. Hirose, H. Tanaka, E. Mori, N. Yamakawa, J. Yasumoto, K. Yuki, K. Ohnishi, T. Ohnishi, Evidence for the involvement of double-strand breaks in heat-induced cell killing. Cancer Res. 64, 8839-8845 (2004).
26. H. M. Beere, Death versus survival: Functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J. Clin. Invest. 115, 2633-2639 (2005).
27. U. Bond, Stressed out! Effects of environmental stress on mRNA metabolism. FEMS Yeast Res. 6, 160-170 (2006).
28. S. Matsuoka, B. A. Ballif, A. Smogorzewska, E. R. McDonald III, K. E. Hurov, J. Luo, C. E. Bakalarski, Z. Zhao, N. Solimini, Y. Lerenthal, Y. Shiloh, S. P. Gygi, S. J. Elledge, ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007).
29. M. Ashburner, C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, G. Sherlock, Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (2000).
30. T. Dai, E. Rubie, C. C. Franklin, A. Kraft, D. A. Gillespie, J. Avruch, J. M. Kyriakis, J. R. Woodgett, Stress-activated protein kinases bind directly to the delta domain of c-Jun in resting cells: Implications for repression of c-Jun function. Oncogene 10, 849-855 (1995).
31. S. Muller, M. Berger, F. Lehembre, J. S. Seeler, Y. Haupt, A. Dejean, c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 275, 13321-13329 (2000).
32. S. Shivaswamy, V. R. Iyer, Stress-dependent dynamics of global chromatin remodeling in yeast: Dual role for SWI/SNF in the heat shock stress response. Mol. Cell. Biol. 28, 2221-2234 (2008).
33. A. V. Ivanov, H. Peng, V. Yurchenko, K. L. Yap, D. G. Negorev, D. C. Schultz, E. Psulkowski, W. J. Fredericks, D. E. White, G. G. Maul, M. J. Sadofsky, M. M. Zhou, F. J. Rauscher III, PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823-837 (2007).
34. B. Stielow, A. Sapetschnig, C. Wink, I. Kruger, G. Suske, SUMO-modified Sp3 represses transcription by provoking local heterochromatic gene silencing. EMBO Rep. 9, 899-906 (2008).
35. D. Nathan, K. Ingvarsdottir, D. E. Sterner, G. R. Bylebyl, M. Dokmanovic, J. A. Dorsey, K. A. Whelan, M. Krsmanovic, W. S. Lane, P. B. Meluh, E. S. Johnson, S. L. Berger, Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 20, 966-976 (2006).
36. Y. Shiio, R. N. Eisenman, Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 100, 13225-13230 (2003).
37. S. K. Ooi, T. H. Bestor, The colorful history of active DNA demethylation. Cell 133, 1145-1148 (2008).
38. H. J. Yost, S. Lindquist, RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45, 185-193 (1986). (Pubitemid 16043421)
39. R. P. VanderWaal, C. L. Griffith, W. D.Wright, M. J. Borrelli, J. L. Roti, Delaying S-phase progression rescues cells from heat-induced S-phase hypertoxicity. J. Cell. Physiol. 187, 236-243 (2001).
40. J. Schimmel, K. M. Larsen, I. Matic, M. van Hagen, J. Cox, M. Mann, J. S. Andersen, A. C. Vertegaal, The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol. Cell. Proteomics 7, 2107-2122 (2008).
41. R. T. Hay, SUMO: A history of modification. Mol. Cell 18, 1-12 (2005).
42. E. Evdokimov, P. Sharma, S. J. Lockett, M. Lualdi, M. R. Kuehn, Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J. Cell Sci. 121, 4106-4113 (2008).
43. S. Hobbs, S. Jitrapakdee, J. C. Wallace, Development of a bicistronic vector driven by the human polypeptide chain elongation factor 1a promoter for creation of stable mammalian cell lines that express very high levels of recombinant proteins. Biochem. Biophys. Res. Commun. 252, 368-372 (1998).
44. S. E. Ong, M. Mann, Stable isotope labeling by amino acids in cell culture for quantitative proteomics. Methods Mol. Biol. 359, 37-52 (2007).
45. A. Shevchenko, H. Tomas, J. Havlis, J. V. Olsen, M. Mann, In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860 (2006).
46. J. Rappsilber, M. Mann, Y. Ishihama, Protocol for micro-purification, enrichment, prefractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906 (2007).
47. D. F. Hunt, J. R. Yates III, J. Shabanowitz, S. Winston, C. R. Hauer, Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 83, 6233-6237 (1986).
48. P. J. Kersey, J. Duarte, A. Williams, Y. Karavidopoulou, E. Birney, R. Apweiler, The International Protein Index: An integrated database for proteomics experiments. Proteomics 4, 1985-1988 (2004).
49. D. Barrell, E. Dimmer, R. P. Huntley, D. Binns, C. O'Donovan, R. Apweiler, The GOA database in 2009-An integrated Gene Ontology Annotation resource. Nucleic Acids Res. 37, D396-D403 (2009).
50. D. M. Martin, M. Berriman, G. J. Barton, GOtcha: A new method for prediction of protein function assessed by the annotation of seven genomes. BMC Bioinformatics 5, 178 (2004).
51. H. B. Mann, D. R. Whitney, On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Statist. 18, 50-60 (1947).
52. Y. Xue, F. Zhou, C. Fu, Y. Xu, X. Yao, SUMOsp: A web server for sumoylation site prediction. Nucleic Acids Res. 34, W254-W257 (2006).
53. P. D. Thomas, A. Kejariwal, M. J. Campbell, H. Mi, K. Diemer, N. Guo, I. Ladunga, B. Ulitsky-Lazareva, A. Muruganujan, S. Rabkin, J. A. Vandergriff, O. Doremieux, PANTHER: A browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 31, 334-341 (2003).
54. F.G. was funded through an EU Marie Curie research fellowship. Work in the R.T.H. laboratory was funded by Cancer Research UK,Wellcome Trust, and the Biotechnology and Biological Sciences Research Council. I.M. was supported by the EU FP6 Rubicon consortium and a European Molecular Biology Organization short-term fellowship. C.C. was funded by the Scottish Funding Council through the Scottish Bioinformatics Research Network. We would like to acknowledge help from C. Botting, R. Antrobus, D. Martin, and M. Scott.