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Sci. Signal., 26 May 2009
Vol. 2, Issue 72, p. ra24
[DOI: 10.1126/scisignal.2000282]


Editor's Summary

SUMO Status Revealed
Posttranslational modification of proteins through their conjugation to small ubiquitin-like modifier (SUMO) proteins is important in the nucleus for the repair of damaged DNA and the maintenance of chromosome structure, as well as for a number of cytoplasmic processes. Although the machinery involved in attaching SUMO moieties to target proteins is well characterized, less is known about the upstream signals that trigger this modification. Golebiowski et al. designed a highly stringent, quantitative approach, involving protein purification and mass spectrometric techniques, to perform a system-wide analysis of the SUMOylation states of hundreds of proteins in HeLa cells in response to heat shock. The authors also analyzed the dynamic nature of SUMOylation in cells during the subsequent recovery phase. In addition to identifying many previously unknown substrates of SUMO-2, this proteome-wide analysis of SUMOylation revealed a rapid and dramatic redistribution of SUMO-2 among proteins involved in short- or long-term responses to heat stress. This new approach should also prove valuable in systems-wide analysis of other posttranslational modifications.

Citation: F. Golebiowski, I. Matic, M. H. Tatham, C. Cole, Y. Yin, A. Nakamura, J. Cox, G. J. Barton, M. Mann, R. T. Hay, System-Wide Changes to SUMO Modifications in Response to Heat Shock. Sci. Signal. 2, ra24 (2009).

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J. Biol. Chem. 288, 27724-27736
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F. Lamoliatte, E. Bonneil, C. Durette, O. Caron-Lizotte, D. Wildemann, J. Zerweck, H. Wenshuk, and P. Thibault (2013)
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Mol. Cell. Proteomics 12, 449-463
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Briefings in Functional Genomics 12, 66-71
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Rap80 Protein Recruitment to DNA Double-strand Breaks Requires Binding to Both Small Ubiquitin-like Modifier (SUMO) and Ubiquitin Conjugates.
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J. Biol. Chem. 287, 25510-25519
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SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage.
Y. Yin, A. Seifert, J. S. Chua, J.-F. Maure, F. Golebiowski, and R. T. Hay (2012)
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Small Ubiquitin-like Modifier (SUMO) Modification of Zinc Finger Protein 131 Potentiates Its Negative Effect on Estrogen Signaling.
Y. Oh and K. C. Chung (2012)
J. Biol. Chem. 287, 17517-17529
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Small Ubiquitin-like Modifier (SUMO) Modification of E1 Cys Domain Inhibits E1 Cys Domain Enzymatic Activity.
K. Truong, T. D. Lee, and Y. Chen (2012)
J. Biol. Chem. 287, 15154-15163
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The Role of Small Ubiquitin-like Modifier-interacting Motif in the Assembly and Regulation of Metal-responsive Transcription Factor 1.
Y.-C. Liu, M.-C. Lin, H.-C. Chen, M. F. Tam, and L.-Y. Lin (2011)
J. Biol. Chem. 286, 42818-42829
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Regulation of Vaccinia Virus E3 Protein by Small Ubiquitin-Like Modifier Proteins.
J. Gonzalez-Santamaria, M. Campagna, M. A. Garcia, L. Marcos-Villar, D. Gonzalez, P. Gallego, F. Lopitz-Otsoa, S. Guerra, M. S. Rodriguez, M. Esteban, et al. (2011)
J. Virol. 85, 12890-12900
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The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup107-160 nucleoporin subcomplex.
J. Goeres, P.-K. Chan, D. Mukhopadhyay, H. Zhang, B. Raught, and M. J. Matunis (2011)
Mol. Biol. Cell 22, 4868-4882
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SUMOylation-regulated Protein Phosphorylation, Evidence from Quantitative Phosphoproteomics Analyses.
Q. Yao, H. Li, B.-Q. Liu, X.-Y. Huang, and L. Guo (2011)
J. Biol. Chem. 286, 27342-27349
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Comparative Proteomic Analysis Identifies a Role for SUMO in Protein Quality Control.
M. H. Tatham, I. Matic, M. Mann, and R. T. Hay (2011)
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Characterizing the N- and C-terminal Small Ubiquitin-like Modifier (SUMO)-interacting Motifs of the Scaffold Protein DAXX.
E. Escobar-Cabrera, M. Okon, D. K. W. Lau, C. F. Dart, A. M. J. J. Bonvin, and L. P. McIntosh (2011)
J. Biol. Chem. 286, 19816-19829
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The Dynamics and Mechanism of SUMO Chain Deconjugation by SUMO-specific Proteases.
M. Bekes, J. Prudden, T. Srikumar, B. Raught, M. N. Boddy, and G. S. Salvesen (2011)
J. Biol. Chem. 286, 10238-10247
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Small Ubiquitin-related Modifier (SUMO)-1 Promotes Glycolysis in Hypoxia.
T. A. Agbor, A. Cheong, K. M. Comerford, C. C. Scholz, U. Bruning, A. Clarke, E. P. Cummins, G. Cagney, and C. T. Taylor (2011)
J. Biol. Chem. 286, 4718-4726
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Inducible SUMO modification of TANK alleviates its repression of TLR7 signalling.
F. Renner, V. V. Saul, A. Pagenstecher, T. Wittwer, and M. L. Schmitz (2011)
EMBO Rep. 12, 129-135
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Purification and identification of endogenous polySUMO conjugates.
R. Bruderer, M. H. Tatham, A. Plechanovova, I. Matic, A. K. Garg, and R. T. Hay (2011)
EMBO Rep. 12, 142-148
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A Novel Proteomics Approach to Identify SUMOylated Proteins and Their Modification Sites in Human Cells.
F. Galisson, L. Mahrouche, M. Courcelles, E. Bonneil, S. Meloche, M. K. Chelbi-Alix, and P. Thibault (2011)
Mol. Cell. Proteomics 10, M110.004796
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Pregnane X Receptor Is SUMOylated to Repress the Inflammatory Response.
G. Hu, C. Xu, and J. L. Staudinger (2010)
J. Pharmacol. Exp. Ther. 335, 342-350
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Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes.
N. Elrouby and G. Coupland (2010)
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M. J. Miller, G. A. Barrett-Wilt, Z. Hua, and R. D. Vierstra (2010)
PNAS 107, 16512-16517
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The serine/arginine-rich protein SF2/ASF regulates protein sumoylation.
F. Pelisch, J. Gerez, J. Druker, I. E. Schor, M. J. Munoz, G. Risso, E. Petrillo, B. J. Westman, A. I. Lamond, E. Arzt, et al. (2010)
PNAS 107, 16119-16124
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Connecting the Dots: Interplay between Ubiquitylation and SUMOylation at DNA Double-Strand Breaks.
J.-b. Tang and R. A. Greenberg (2010)
Genes & Cancer 1, 787-796
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In Vivo Identification of Sumoylation Sites by a Signature Tag and Cysteine-targeted Affinity Purification.
H. A. Blomster, S. Y. Imanishi, {i. } {image}{image}, J. Siimes, J. Kastu, N. A. Morrice, J. E. Eriksson, and L. Sistonen (2010)
J. Biol. Chem. 285, 19324-19329
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SUMO proteins are involved in the stress response during spermatogenesis and are localized to DNA double-strand breaks in germ cells.
V. Shrivastava, M. Pekar, E. Grosser, J. Im, and M. Vigodner (2010)
Reproduction 139, 999-1010
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Differential Effects of Sumoylation on Transcription and Alternative Splicing by Transcription Elongation Regulator 1 (TCERG1).
M. Sanchez-Alvarez, M. Montes, N. Sanchez-Hernandez, C. Hernandez-Munain, and C. Sune (2010)
J. Biol. Chem. 285, 15220-15233
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Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals.
B. Leitao, M. C. Jones, L. Fusi, J. Higham, Y. Lee, M. Takano, T. Goto, M. Christian, E. W. F. Lam, and J. J. Brosens (2010)
FASEB J 24, 1541-1551
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N. T. Seyfried, Y. M. Gozal, E. B. Dammer, Q. Xia, D. M. Duong, D. Cheng, J. J. Lah, A. I. Levey, and J. Peng (2010)
Mol. Cell. Proteomics 9, 705-718
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S. J. L. van Wijk and H. T. M. Timmers (2010)
FASEB J 24, 981-993
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M. B. Yaffe and A. M. VanHook (2010)
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PARP-1 transcriptional activity is regulated by sumoylation upon heat shock.
N. Martin, K. Schwamborn, V. Schreiber, A. Werner, C. Guillier, X.-D. Zhang, O. Bischof, J.-S. Seeler, and A. Dejean (2009)
EMBO J. 28, 3534-3548
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