publication . Article . Other literature type . 2016

Capturing a substrate in an activated RING E3/E2–SUMO complex

Frederick C. Streich; Christopher D. Lima; Christopher D. Lima;
Open Access
  • Published: 10 Aug 2016 Journal: Nature, volume 536, pages 304-308 (issn: 0028-0836, eissn: 1476-4687, Copyright policy)
  • Publisher: Springer Science and Business Media LLC
Abstract
Summary Post-translational protein modification by ubiquitin (Ub) and ubiquitin-like (Ubl) proteins such as small ubiquitin like modifier (SUMO) regulates processes including protein homeostasis, the DNA damage response, and the cell cycle. Proliferating cell nuclear antigen (PCNA) is modified by Ub or poly-Ub at Lys164 after DNA damage to recruit repair factors. Yeast PCNA is modified by SUMO on Lys164 and Lys127 during S-phase to recruit the anti-recombinogenic helicase Srs2. Lys164 modification requires specialized E2/E3 enzyme pairs for SUMO or Ub conjugation. For SUMO, Lys164 modification is strictly dependent on the E3 ligase Siz1, suggesting the E3 alters...
Subjects
free text keywords: Article, E3 ligase, E2 conjugating enzyme, PCNA, SUMO, Signal transduction, Replication, Proliferating cell nuclear antigen, biology.protein, biology, Small Ubiquitin-Related Modifier Proteins, Ubiquitin, Ubiquitin ligase, Ubiquitin-Protein Ligases, Helicase, Protein engineering, Biochemistry, DNA damage
Funded by
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| Structural Studies of SUMO Protein Modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM065872-12
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Structural studies of RNA processing and ubiquitin-like protein modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM118080-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
53 references, page 1 of 4

Kerscher, O, Felberbaum, R, Hochstrasser, M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006; 22: 159-180 [OpenAIRE] [PubMed]

Gareau, JR, Lima, CD. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol. 2010; 11: 861-871 [OpenAIRE] [PubMed]

Hochstrasser, M. Origin and function of ubiquitin-like proteins. Nature. 2009; 458: 422-429 [OpenAIRE] [PubMed]

Streich, FC, Lima, CD. Structural and functional insights to ubiquitin-like protein conjugation. Annu Rev Biophys. 2014; 43: 357-379 [OpenAIRE] [PubMed]

Sampson, DA, Wang, M, Matunis, MJ. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem. 2001; 276: 21664-21669 [PubMed]

Bernier-Villamor, V, Sampson, DA, Matunis, MJ, Lima, CD. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell. 2002; 108: 345-356 [PubMed]

Reverter, D, Lima, CD. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature. 2005; 435: 687-692 [OpenAIRE] [PubMed]

Yunus, AA, Lima, CD. Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat Struct Mol Biol. 2006; 13: 491-499 [PubMed]

Eddins, MJ, Carlile, CM, Gomez, KM, Pickart, CM, Wolberger, C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat Struct Mol Biol. 2006; 13: 915-920 [OpenAIRE] [PubMed]

Bosanac, I. Modulation of K11-linkage formation by variable loop residues within UbcH5A. J Mol Biol. 2011; 408: 420-431 [PubMed]

Wickliffe, KE, Lorenz, S, Wemmer, DE, Kuriyan, J, Rape, M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell. 2011; 144: 769-781 [OpenAIRE] [PubMed]

Saha, A, Lewis, S, Kleiger, G, Kuhlman, B, Deshaies, RJ. Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol Cell. 2011; 42: 75-83 [OpenAIRE] [PubMed]

Page, RC, Pruneda, JN, Amick, J, Klevit, RE, Misra, S. Structural insights into the conformation and oligomerization of E2~ubiquitin conjugates. Biochemistry. 2012; 51: 4175-4187 [OpenAIRE] [PubMed]

Rodrigo-Brenni, MC, Foster, SA, Morgan, DO. Catalysis of lysine 48-specific ubiquitin chain assembly by residues in E2 and ubiquitin. Mol Cell. 2010; 39: 548-559 [OpenAIRE] [PubMed]

Deshaies, RJ, Joazeiro, CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem. 2009; 78: 399-434 [OpenAIRE] [PubMed]

53 references, page 1 of 4
Abstract
Summary Post-translational protein modification by ubiquitin (Ub) and ubiquitin-like (Ubl) proteins such as small ubiquitin like modifier (SUMO) regulates processes including protein homeostasis, the DNA damage response, and the cell cycle. Proliferating cell nuclear antigen (PCNA) is modified by Ub or poly-Ub at Lys164 after DNA damage to recruit repair factors. Yeast PCNA is modified by SUMO on Lys164 and Lys127 during S-phase to recruit the anti-recombinogenic helicase Srs2. Lys164 modification requires specialized E2/E3 enzyme pairs for SUMO or Ub conjugation. For SUMO, Lys164 modification is strictly dependent on the E3 ligase Siz1, suggesting the E3 alters...
Subjects
free text keywords: Article, E3 ligase, E2 conjugating enzyme, PCNA, SUMO, Signal transduction, Replication, Proliferating cell nuclear antigen, biology.protein, biology, Small Ubiquitin-Related Modifier Proteins, Ubiquitin, Ubiquitin ligase, Ubiquitin-Protein Ligases, Helicase, Protein engineering, Biochemistry, DNA damage
Funded by
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| Structural Studies of SUMO Protein Modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM065872-12
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Structural studies of RNA processing and ubiquitin-like protein modification
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM118080-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
53 references, page 1 of 4

Kerscher, O, Felberbaum, R, Hochstrasser, M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006; 22: 159-180 [OpenAIRE] [PubMed]

Gareau, JR, Lima, CD. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol. 2010; 11: 861-871 [OpenAIRE] [PubMed]

Hochstrasser, M. Origin and function of ubiquitin-like proteins. Nature. 2009; 458: 422-429 [OpenAIRE] [PubMed]

Streich, FC, Lima, CD. Structural and functional insights to ubiquitin-like protein conjugation. Annu Rev Biophys. 2014; 43: 357-379 [OpenAIRE] [PubMed]

Sampson, DA, Wang, M, Matunis, MJ. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem. 2001; 276: 21664-21669 [PubMed]

Bernier-Villamor, V, Sampson, DA, Matunis, MJ, Lima, CD. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell. 2002; 108: 345-356 [PubMed]

Reverter, D, Lima, CD. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature. 2005; 435: 687-692 [OpenAIRE] [PubMed]

Yunus, AA, Lima, CD. Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat Struct Mol Biol. 2006; 13: 491-499 [PubMed]

Eddins, MJ, Carlile, CM, Gomez, KM, Pickart, CM, Wolberger, C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat Struct Mol Biol. 2006; 13: 915-920 [OpenAIRE] [PubMed]

Bosanac, I. Modulation of K11-linkage formation by variable loop residues within UbcH5A. J Mol Biol. 2011; 408: 420-431 [PubMed]

Wickliffe, KE, Lorenz, S, Wemmer, DE, Kuriyan, J, Rape, M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell. 2011; 144: 769-781 [OpenAIRE] [PubMed]

Saha, A, Lewis, S, Kleiger, G, Kuhlman, B, Deshaies, RJ. Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol Cell. 2011; 42: 75-83 [OpenAIRE] [PubMed]

Page, RC, Pruneda, JN, Amick, J, Klevit, RE, Misra, S. Structural insights into the conformation and oligomerization of E2~ubiquitin conjugates. Biochemistry. 2012; 51: 4175-4187 [OpenAIRE] [PubMed]

Rodrigo-Brenni, MC, Foster, SA, Morgan, DO. Catalysis of lysine 48-specific ubiquitin chain assembly by residues in E2 and ubiquitin. Mol Cell. 2010; 39: 548-559 [OpenAIRE] [PubMed]

Deshaies, RJ, Joazeiro, CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem. 2009; 78: 399-434 [OpenAIRE] [PubMed]

53 references, page 1 of 4
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