CoChat
Sign Up
Cited by 514

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

A comprehensive compilation of SUMO proteomics

Hendriks, Ivo A., Vertegaal, Alfred C. O.·2016·Nature Reviews Molecular Cell Biology
DOI 10.1038/nrm.2016.81
Open this paper in CoChat — free account

Abstract

Small ubiquitin-like modifiers (SUMOs) are essential for the regulation of several cellular processes and are potential therapeutic targets owing to their involvement in diseases such as cancer and Alzheimer disease. In the past decade, we have witnessed a rapid expansion of proteomic approaches for identifying sumoylated proteins, with recent advances in detecting site-specific sumoylation. In this Analysis, we combined all human SUMO proteomics data currently available into one cohesive database. We provide proteomic evidence for sumoylation of 3,617 proteins at 7,327 sumoylation sites, and insight into SUMO group modification by clustering the sumoylated proteins into functional networks. The data support sumoylation being a frequent protein modification (on par with other major protein modifications) with multiple nuclear functions, including in transcription, mRNA processing, DNA replication and the DNA-damage response.

Overview

Integrity signals

Registry

Crossref · 10.1038/nrm.2016.81

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The SUMOylation-deSUMOylation cycle governs many biological processes by affecting protein stability, activity, localization, and interactions.

    “The SUMOylation–deSUMOylation cycle governs many biological processes by affecting protein stability, activity, localization as well as their interaction with other proteins (21).”

    From SUMOylation of the ubiquitin ligase IDOL decreases LDL receptor levels and is reversed by SENP1 (2021) · cites this paper as [21]

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 146

  1. Golebiowski, F. et al. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2, ra24 (2009). · DOI
  2. Hendriks, I. A. et al. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat. Struct. Mol. Biol. 21, 927–936 (2014). The first site-specific proteomics paper reporting more than 1,000 sumoylation sites in standard growth conditions, and more than 4,000 sumoylation sites in total. · DOI
  3. Schimmel, J. et al. Uncovering SUMOylation dynamics during cell-cycle progression reveals FoxM1 as a key mitotic SUMO target protein. Mol. Cell 53, 1053–1066 (2014). · DOI
  4. Miura, K., Jin, J. B. & Hasegawa, P. M. Sumoylation, a post-translational regulatory process in plants. Curr. Opin. Plant Biol. 10, 495–502 (2007). · DOI
  5. Geiss-Friedlander, R. & Melchior, F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947–956 (2007). · DOI
  6. Flotho, A. & Melchior, F. Sumoylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem. 82, 357–385 (2013). · DOI
  7. Ulrich, H. D. & Walden, H. Ubiquitin signalling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 11, 479–489 (2010). · DOI
  8. Hickey, C. M., Wilson, N. R. & Hochstrasser, M. Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13, 755–766 (2012). · DOI
  9. Jackson, S. P. & Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795–807 (2013). · DOI · Paper page
  10. Eifler, K. & Vertegaal, A. C. Mapping the SUMOylated landscape. FEBS J. 282, 3669–3680 (2015). · DOI
  11. Eifler, K. & Vertegaal, A. C. SUMOylation-mediated regulation of cell cycle progression and cancer. Trends Biochem. Sci. 40, 779–793 (2015). · DOI
  12. Kessler, J. D. et al. A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science 335, 348–353 (2012). The involvement of SUMO in diseases such as cancer is exemplified by the ability of SUMO to orchestrate Myc-driven tumorigenesis. · DOI
  13. Lee, Y. J. & Hallenbeck, J. M. SUMO and ischemic tolerance. Neuromolecular Med. 15, 771–781 (2013). · DOI
  14. Wang, Y. & Dasso, M. SUMOylation and deSUMOylation at a glance. J. Cell Sci. 122, 4249–4252 (2009). · DOI
  15. Guo, D. et al. Proteomic analysis of SUMO4 substrates in HEK293 cells under serum starvation-induced stress. Biochem. Biophys. Res. Commun. 337, 1308–1318 (2005). · DOI
  16. Becker, J. et al. Detecting endogenous SUMO targets in mammalian cells and tissues. Nat. Struct. Mol. Biol. 20, 525–531 (2013). The first proteomics screen to identify hundreds of endogenous SUMO target proteins using immunoprecipitation. · DOI
  17. Matic, I. et al. 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 7, 132–144 (2008). · DOI
  18. Tatham, M. H. et al. 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). · DOI
  19. Seeler, J. S. & Dejean, A. Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 4, 690–699 (2003). · DOI
  20. Kamitani, T., Nguyen, H. P. & Yeh, E. T. Preferential modification of nuclear proteins by a novel ubiquitin-like molecule. J. Biol. Chem. 272, 14001–14004 (1997). · DOI
  21. Shiio, Y. & Eisenman, R. N. Histone sumoylation is associated with transcriptional repression. Proc. Natl Acad. Sci. USA 100, 13225–13230 (2003). · DOI
  22. Stielow, B. et al. Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol. Cell 29, 742–754 (2008). · DOI
  23. Uchimura, Y. et al. Involvement of SUMO modification in. J. Biol. Chem. 281, 23180–23190 (2006). · DOI
  24. Ishov, A. M. et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147, 221–234 (1999). · DOI
  25. Zhong, S. et al. Role of SUMO-1-modified PML in nuclear body formation. Blood 95, 2748–2752 (2000). · DOI
  26. Muller, S. & Dejean, A. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 73, 5137–5143 (1999). · DOI
  27. Shen, T. H., Lin, H. K., Scaglioni, P. P., Yung, T. M. & Pandolfi, P. P. The mechanisms of PML-nuclear body formation. Mol. Cell 24, 331–339 (2006). · DOI
  28. Bernardi, R. & Pandolfi, P. P. Role of PML and the PML-nuclear body in the control of programmed cell death. Oncogene 22, 9048–9057 (2003). · DOI
  29. Dellaire, G. & Bazett-Jones, D. P. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26, 963–977 (2004). · DOI
  30. Bergink, S. & Jentsch, S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461–467 (2009). · DOI
  31. Hardeland, U., Steinacher, R., Jiricny, J. & Schar, P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21, 1456–1464 (2002). · DOI
  32. Stelter, P. & Ulrich, H. D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188–191 (2003). · DOI
  33. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. & Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135–141 (2002). · DOI
  34. Morris, J. R. et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886–890 (2009). · DOI · Paper page
  35. Galanty, Y. et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935–939 (2009). · DOI
  36. Yin, Y. et al. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196–1208 (2012). · DOI · Paper page
  37. Vyas, R. et al. RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20, 490–502 (2013). · DOI
  38. Ouyang, K. J. et al. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol. 7, e1000252 (2009). · DOI
  39. Pichler, A. et al. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12, 264–269 (2005). · DOI
  40. Steinacher, R. & Schar, P. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15, 616–623 (2005). · DOI
  41. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P. & Dikic, I. Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117–16127 (2006). · DOI
  42. Sun, H. & Hunter, T. Poly-small ubiquitin-like modifier (PolySUMO)-binding proteins identified through a string search. J. Biol. Chem. 287, 42071–42083 (2012). · DOI
  43. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G. & Chen, Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl Acad. Sci. USA 101, 14373–14378 (2004). · DOI
  44. Keusekotten, K. et al. Multivalent interactions of the SUMO-interaction motifs in RING finger protein 4 determine the specificity for chains of the SUMO. Biochem. J. 457, 207–214 (2014). · DOI
  45. Merrill, J. C. et al. A role for non-covalent SUMO interaction motifs in Pc2/CBX4 E3 activity. PLoS ONE 5, e8794 (2010). · DOI
  46. Prudden, J. et al. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 26, 4089–4101 (2007). · DOI
  47. Perry, J. J., Tainer, J. A. & Boddy, M. N. A. SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 33, 201–208 (2008). · DOI
  48. Wang, Z. & Prelich, G. Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol. Cell. Biol. 29, 1694–1706 (2009). · DOI
  49. Nagai, S., Davoodi, N. & Gasser, S. M. Nuclear organization in genome stability: SUMO connections. Cell Res. 21, 474–485 (2011). · DOI
  50. Sun, H., Leverson, J. D. & Hunter, T. Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 26, 4102–4112 (2007). · DOI
  51. Tatham, M. H. et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538–546 (2008). · DOI
  52. Weisshaar, S. R. et al. Arsenic trioxide stimulates SUMO-2/3 modification leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett. 582, 3174–3178 (2008). · DOI
  53. Geoffroy, M. C., Jaffray, E. G., Walker, K. J. & Hay, R. T. Arsenic-induced SUMO-dependent recruitment of RNF4 into PML nuclear bodies. Mol. Biol. Cell 21, 4227–4239 (2010). · DOI
  54. Lallemand-Breitenbach, V. et al. Arsenic degrades PML or PML-RARα through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10, 547–555 (2008). · DOI
  55. Kosoy, A., Calonge, T. M., Outwin, E. A. & O'Connell, M. J. Fission yeast Rnf4 homologs are required for DNA repair. J. Biol. Chem. 282, 20388–20394 (2007). · DOI
  56. Guzzo, C. M. et al. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci. Signal. 5, ra88 (2012). · DOI
  57. Silver, H. R., Nissley, J. A., Reed, S. H., Hou, Y. M. & Johnson, E. S. A role for SUMO in nucleotide excision repair. DNA Repair (Amst.) 10, 1243–1251 (2011). · DOI
  58. Psakhye, I. & Jentsch, S. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807–820 (2012). An excellent example of SUMO group modification during the DDR in yeast. · DOI · Paper page
  59. Raman, N., Nayak, A. & Muller, S. The SUMO system: a master organizer of nuclear protein assemblies. Chromosoma 122, 475–485 (2013). · DOI
  60. Sahin, U. et al. Oxidative stress-induced assembly of PML nuclear bodies controls sumoylation of partner proteins. J. Cell Biol. 204, 931–945 (2014). · DOI
  61. Gonzalez-Prieto, R., Cuijpers, S. A., Luijsterburg, M. S., van Attikum, H. & Vertegaal, A. C. SUMOylation and PARylation cooperate to recruit and stabilize SLX4 at DNA damage sites. EMBO Rep. 16, 512–519 (2015). · DOI
  62. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425–479 (1998). · DOI · Paper page
  63. Pandey, A. & Mann, M. Proteomics to study genes and genomes. Nature 405, 837–846 (2000). · DOI
  64. Mann, M. & Jensen, O. N. Proteomic analysis of post-translational modifications. Nat. Biotechnol. 21, 255–261 (2003). · DOI
  65. Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011). · DOI
  66. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008). · DOI · Paper page
  67. Olsen, J. V. & Mann, M. Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol. Cell. Proteomics 12, 3444–3452 (2013). · DOI
  68. Choudhary, C. & Mann, M. Decoding signalling networks by mass spectrometry-based proteomics. Nat. Rev. Mol. Cell Biol. 11, 427–439 (2010). · DOI
  69. Choudhary, C. et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834–840 (2009). · DOI · Paper page
  70. Huttlin, E. L. et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174–1189 (2010). · DOI · Paper page
  71. Olsen, J. V. et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635–648 (2006). · DOI
  72. Guo, A. et al. Immunoaffinity enrichment and mass spectrometry analysis of protein methylation. Mol. Cell. Proteomics 13, 372–387 (2013). · DOI
  73. Emanuele, M. J. et al. Global identification of modular cullin-RING ligase substrates. Cell 147, 459–474 (2011). · DOI
  74. Wagner, S. A. et al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 10, M111.013284 (2011). · DOI
  75. Kim, W. et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325–340 (2011). · DOI
  76. Tammsalu, T. et al. Proteome-wide identification of SUMO2 modification sites. Sci. Signal. 7, rs2 (2014). The first site-specific SUMO proteomics study to report more than 1,000 sumoylation sites. · DOI
  77. Xiao, Z. et al. System-wide analysis of SUMOylation dynamics in response to replication stress reveals novel SUMO target proteins and acceptor lysines relevant for genome stability. Mol. Cell. Proteomics 14, 1419–1434 (2015). · DOI
  78. Hendriks, I. A., Treffers, L. W., Verlaan-de Vries, M., Olsen, J. V. & Vertegaal, A. C. SUMO-2 orchestrates chromatin modifiers in response to DNA damage. Cell Rep. 10, 1778–1791 (2015). · DOI
  79. Impens, F., Radoshevich, L., Cossart, P. & Ribet, D. Mapping of SUMO sites and analysis of SUMOylation changes induced by external stimuli. Proc. Natl Acad. Sci. USA 111, 12432–12437 (2014). · DOI
  80. Lamoliatte, F. et al. Large-scale analysis of lysine SUMOylation by SUMO remnant immunoaffinity profiling. Nat. Commun. 5, 5409 (2014). · DOI
  81. Hendriks, I. A., D'Souza, R. C., Chang, J. G., Mann, M. & Vertegaal, A. C. System-wide identification of wild-type SUMO-2 conjugation sites. Nat. Commun. 6, 7289 (2015). Describes the development of PRISM, the first proteomic method to be able to identify hundreds of sumoylation sites without relying on the use of mutant SUMO. · DOI
  82. 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. 140, 259–270 (1998). · DOI
  83. Eisenhardt, N. et al. A new vertebrate SUMO enzyme family reveals insights into SUMO-chain assembly. Nat. Struct. Mol. Biol. 22, 959–967 (2015). Identifies ZNF451, a newly discovered enzyme with SUMO E3 ligase activity that is able to elongate SUMO chains and mediate sumoylation dynamics in response to cellular stress. · DOI
  84. Cappadocia, L., Pichler, A. & Lima, C. D. Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase. Nat. Struct. Mol. Biol. 22, 968–975 (2015). · DOI
  85. Schimmel, J. et al. The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol. Cell. Proteomics 7, 2107–2122 (2008). · DOI
  86. Pinto, M. P. et al. Heat shock induces a massive but differential inactivation of SUMO-specific proteases. Biochim. Biophys. Acta 1823, 1958–1966 (2012). · DOI
  87. Guo, L. et al. A cellular system that degrades misfolded proteins and protects against neurodegeneration. Mol. Cell 55, 15–30 (2014). · DOI
  88. Bursomanno, S. et al. Proteome-wide analysis of SUMO2 targets in response to pathological DNA replication stress in human cells. DNA Repair (Amst.) 25, 84–96 (2015). · DOI
  89. Seifert, A., Schofield, P., Barton, G. J. & Hay, R. T. Proteotoxic stress reprograms the chromatin landscape of SUMO modification. Sci. Signal. 8, rs7 (2015). · DOI
  90. Li, T. et al. Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. Proc. Natl Acad. Sci. USA 101, 8551–8556 (2004). · DOI
  91. Vassileva, M. T. & Matunis, M. J. SUMO modification of heterogeneous nuclear ribonucleoproteins. Mol. Cell. Biol. 24, 3623–3632 (2004). · DOI
  92. Pelisch, F., Pozzi, B., Risso, G., Munoz, M. J. & Srebrow, A. DNA damage-induced heterogeneous nuclear ribonucleoprotein K sumoylation regulates p53 transcriptional activation. J. Biol. Chem. 287, 30789–30799 (2012). · DOI
  93. Lee, S. W. et al. SUMOylation of hnRNP-K is required for p53-mediated cell-cycle arrest in response to DNA damage. EMBO J. 31, 4441–4452 (2012). · DOI
  94. Panse, V. G. et al. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic. 7, 1311–1321 (2006). · DOI
  95. Finkbeiner, E., Haindl, M. & Muller, S. The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J. 30, 1067–1078 (2011). · DOI
  96. Westman, B. J. et al. A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 39, 618–631 (2010). · DOI
  97. Zemp, I. & Kutay, U. Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581, 2783–2793 (2007). · DOI
  98. Hang, J. & Dasso, M. Association of the human SUMO-1 protease SENP2 with the nuclear pore. J. Biol. Chem. 277, 19961–19966 (2002). · DOI
  99. Lewis, A., Felberbaum, R. & Hochstrasser, M. A nuclear envelope protein linking nuclear pore basket assembly, SUMO protease regulation, and mRNA surveillance. J. Cell Biol. 178, 813–827 (2007). · DOI
  100. Yang, S. H. & Sharrocks, A. D. SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13, 611–617 (2004). · DOI
  101. Kirsh, O. et al. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21, 2682–2691 (2002). · DOI
  102. Bueno, M. T. & Richard, S. SUMOylation negatively modulates target gene occupancy of the KDM5B, a histone lysine demethylase. Epigenetics 8, 1162–1175 (2013). · DOI
  103. Sriramachandran, A. M. & Dohmen, R. J. SUMO-targeted ubiquitin ligases. Biochim. Biophys. Acta 1843, 75–85 (2014). · DOI
  104. Ryu, H., Gygi, S. P., Azuma, Y., Arnaoutov, A. & Dasso, M. SUMOylation of Psmd1 controls Adrm1 interaction with the proteasome. Cell Rep. 7, 1842–1848 (2014). · DOI
  105. Nacerddine, K. et al. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9, 769–779 (2005). · DOI
  106. Myatt, S. S. et al. SUMOylation inhibits FOXM1 activity and delays mitotic transition. Oncogene 33, 4316–4329 (2013). · DOI
  107. Zhang, X. D. et al. SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol. Cell 29, 729–741 (2008). · DOI
  108. Luo, K., Zhang, H., Wang, L., Yuan, J. & Lou, Z. Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31, 3008–3019 (2012). · DOI
  109. Gonzalez-Prieto, R., Cuijpers, S. A., Kumar, R., Hendriks, I. A. & Vertegaal, A. C. c-Myc is targeted to the proteasome for degradation in a SUMOylation-dependent manner, regulated by PIAS1, SENP7 and RNF4. Cell Cycle 14, 1859–1872 (2015). · DOI
  110. Sabo, A., Doni, M. & Amati, B. SUMOylation of Myc-family proteins. PLoS ONE 9, e91072 (2014). · DOI
  111. Schou, J., Kelstrup, C. D., Hayward, D. G., Olsen, J. V. & Nilsson, J. Comprehensive identification of SUMO2/3 targets and their dynamics during mitosis. PLoS ONE 9, e100692 (2014). · DOI
  112. Cubenas-Potts, C. et al. Identification of SUMO-2/3-modified proteins associated with mitotic chromosomes. Proteomics 15, 763–772 (2015). · DOI
  113. Bursomanno, S., McGouran, J. F., Kessler, B. M., Hickson, I. D. & Liu, Y. Regulation of SUMO2 target proteins by the proteasome in human cells exposed to replication stress. J. Proteome Res. 14, 1687–1699 (2015). · DOI
  114. Rodriguez, M. S., Dargemont, C. & Hay, R. T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654–12659 (2001). · DOI
  115. 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 108, 345–356 (2002). · DOI
  116. Matic, I. et al. Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol. Cell 39, 641–652 (2010). · DOI
  117. Yang, S. H., Galanis, A., Witty, J. & Sharrocks, A. D. An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J. 25, 5083–5093 (2006). · DOI
  118. Hietakangas, V. et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl Acad. Sci. USA 103, 45–50 (2006). · DOI
  119. Kubota, Y., O'Grady, P., Saito, H. & Takekawa, M. Oncogenic Ras abrogates MEK SUMOylation that suppresses the ERK pathway and cell transformation. Nat. Cell Biol. 13, 282–291 (2011). · DOI
  120. Girdwood, D. et al. P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11, 1043–1054 (2003). · DOI
  121. Ullmann, R., Chien, C. D., Avantaggiati, M. L. & Muller, S. An acetylation switch regulates SUMO-dependent protein interaction networks. Mol. Cell 46, 759–770 (2012). · DOI
  122. Wagner, S. A. et al. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteomics 11, 1578–1585 (2012). · DOI
  123. Danielsen, J. M. et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell. Proteomics 10, M110.003590 (2011). · DOI
  124. Olsen, J. V. et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3 (2010). · DOI
  125. Choudhary, C. et al. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Mol. Cell 36, 326–339 (2009). · DOI
  126. Swatek, K. N. & Komander, D. Ubiquitin modifications. Cell Res. 26, 399–422 (2016). · DOI
  127. Herhaus, L. & Dikic, I. Expanding the ubiquitin code through post-translational modification. EMBO Rep. 16, 1071–1083 (2015). · DOI
  128. Ordureau, A. et al. Defining roles of PARKIN and ubiquitin phosphorylation by PINK1 in mitochondrial quality control using a ubiquitin replacement strategy. Proc. Natl Acad. Sci. USA 112, 6637–6642 (2015). · DOI · Paper page
  129. Kane, L. A. et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205, 143–153 (2014). · DOI · Paper page
  130. Vertegaal, A. C. SUMO chains: polymeric signals. Biochem. Soc. Trans. 38, 46–49 (2010). · DOI
  131. Desterro, J. M., Rodriguez, M. S., Kemp, G. D. & Hay, R. T. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274, 10618–10624 (1999). · DOI
  132. Azuma, Y. et al. Expression and regulation of the mammalian SUMO-1 E1 enzyme. FASEB J. 15, 1825–1827 (2001). · DOI
  133. Hay, R. T. SUMO: a history of modification. Mol. Cell 18, 1–12 (2005). · DOI
  134. Johnson, E. S. Protein modification by SUMO. Annu. Rev. Biochem. 73, 355–382 (2004). · DOI
  135. Reverter, D. & Lima, C. D. Insights into E3 ligase activity revealed by a SUMO-–RanGAP1–Ubc9–Nup358 complex. Nature 435, 687–692 (2005). · DOI
  136. Sampson, D. A., Wang, M. & Matunis, M. J. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21 664–21669 (2001). · DOI
  137. Li, S. J. & Hochstrasser, M. A new protease required for cell-cycle progression in yeast. Nature 398, 246–251 (1999). · DOI
  138. Mukhopadhyay, D. & Dasso, M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286–295 (2007). · DOI
  139. Di, B. A. et al. The SUMO-specific protease SENP5 is required for cell division. Mol. Cell. Biol. 26, 4489–4498 (2006). · DOI
  140. Cheng, J., Kang, X., Zhang, S. & Yeh, E. T. SUMO-specific protease 1 is essential for stabilization of HIF1α during hypoxia. Cell 131, 584–595 (2007). · DOI · Paper page
  141. Vertegaal, A. C. et al. Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 5, 2298–2310 (2006). · DOI
  142. Matafora, V., D'Amato, A., Mori, S., Blasi, F. & Bachi, A. Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol. Cell. Proteomics 8, 2243–2255 (2009). · DOI
  143. Bruderer, R. et al. Purification and identification of endogenous polySUMO conjugates. EMBO Rep. 12, 142–148 (2011). · DOI
  144. Tatham, M. H., Matic, I., Mann, M. & Hay, R. T. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4, rs4 (2011). · DOI
  145. Sohn, S. Y., Bridges, R. G. & Hearing, P. Proteomic analysis of ubiquitin-like posttranslational modifications induced by the adenovirus E4-ORF3 protein. J. Virol. 89, 1744–1755 (2015). · DOI
  146. Tu, J. et al. Functional proteomics study reveals SUMOylation of TFII-I is involved in liver cancer cell proliferation. J. Proteome Res. 14, 2385–2397 (2015). · DOI

Cited by

Sorted by citations

Metadata

Authors
Hendriks, I. A., & Vertegaal, A. C. O.
Venue
Nature Reviews Molecular Cell Biology
Publisher
Springer Science and Business Media LLC
Published
2016-07-20
Volume
17
Issue
9
Pages
581-595
ISSN
  • 1471-0072
  • 1471-0080
DOI
10.1038/nrm.2016.81
Cited by
514
References
3
Language
en
Licence
www.springer.com/tdm (tdm)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review