Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase
Abstract
E3 protein ligases enhance transfer of ubiquitin-like (Ubl) proteins from E2 conjugating enzymes to substrates by stabilizing the thioester-charged E2~Ubl in a closed configuration optimally aligned for nucleophilic attack. In this paper, we report biochemical and structural data that define the N-terminal domain of the Homo sapiens ZNF451 as the catalytic module for SUMO E3 ligase activity. The ZNF451 catalytic module contains tandem SUMO-interaction motifs (SIMs) bridged by a Pro-Leu-Arg-Pro (PLRP) motif. The first SIM and PLRP motif engage thioester-charged E2~SUMO while the next SIM binds a second molecule of SUMO bound to the back side of E2. We show that ZNF451 is SUMO2 specific and that SUMO modification of ZNF451 may contribute to activity by providing a second molecule of SUMO that interacts with E2. Finally, our results are consistent with ZNF451 functioning as a bona fide SUMO E3 ligase.
- Authors:
-
- Sloan Kettering Inst., New York, NY (United States). Structural Biology Program
- Max Planck Inst. of Immunobiology and Epigenetics, Freiburg (Germany). Dept. of Epigenetics
- Sloan Kettering Inst., New York, NY (United States). Structural Biology Program. Howard Hughes Medical Inst.
- Publication Date:
- Research Org.:
- Sloan Kettering Inst., New York, NY (United States); Max Planck Inst. of Immunobiology and Epigenetics, Freiburg (Germany)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States); Max Planck Society (Germany); German Research Foundation (DFG)
- OSTI Identifier:
- 1229890
- Grant/Contract Number:
- AC02-06CH11357; P41RR012408; P41GM103473; P41 GM103403; S10 RR029205; GM065872; P30 CA008748; DFG-SPP1365 PI 917/2-1
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Structural & Molecular Biology
- Additional Journal Information:
- Journal Volume: 22; Journal Issue: 12; Journal ID: ISSN 1545-9993
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Biochemistry; Structural biology; X-ray crystallography
Citation Formats
Cappadocia, Laurent, Pichler, Andrea, and Lima, Christopher D. Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase. United States: N. p., 2015.
Web. doi:10.1038/nsmb.3116.
Cappadocia, Laurent, Pichler, Andrea, & Lima, Christopher D. Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase. United States. https://doi.org/10.1038/nsmb.3116
Cappadocia, Laurent, Pichler, Andrea, and Lima, Christopher D. Mon .
"Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase". United States. https://doi.org/10.1038/nsmb.3116. https://www.osti.gov/servlets/purl/1229890.
@article{osti_1229890,
title = {Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase},
author = {Cappadocia, Laurent and Pichler, Andrea and Lima, Christopher D.},
abstractNote = {E3 protein ligases enhance transfer of ubiquitin-like (Ubl) proteins from E2 conjugating enzymes to substrates by stabilizing the thioester-charged E2~Ubl in a closed configuration optimally aligned for nucleophilic attack. In this paper, we report biochemical and structural data that define the N-terminal domain of the Homo sapiens ZNF451 as the catalytic module for SUMO E3 ligase activity. The ZNF451 catalytic module contains tandem SUMO-interaction motifs (SIMs) bridged by a Pro-Leu-Arg-Pro (PLRP) motif. The first SIM and PLRP motif engage thioester-charged E2~SUMO while the next SIM binds a second molecule of SUMO bound to the back side of E2. We show that ZNF451 is SUMO2 specific and that SUMO modification of ZNF451 may contribute to activity by providing a second molecule of SUMO that interacts with E2. Finally, our results are consistent with ZNF451 functioning as a bona fide SUMO E3 ligase.},
doi = {10.1038/nsmb.3116},
journal = {Nature Structural & Molecular Biology},
number = 12,
volume = 22,
place = {United States},
year = {Mon Nov 02 00:00:00 EST 2015},
month = {Mon Nov 02 00:00:00 EST 2015}
}
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- Ronau, Judith A.; Beckmann, John F.; Hochstrasser, Mark
- Cell Research, Vol. 26, Issue 4
Transposable Elements in Human Cancer: Causes and Consequences of Deregulation
journal, May 2017
- Anwar, Sumadi; Wulaningsih, Wahyu; Lehmann, Ulrich
- International Journal of Molecular Sciences, Vol. 18, Issue 5
SUMO, a small, but powerful, regulator of double-strand break repair
journal, August 2017
- Garvin, Alexander J.; Morris, Joanna R.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1731
Molecular mechanisms in SUMO conjugation
journal, December 2019
- Varejão, Nathalia; Lascorz, Jara; Li, Ying
- Biochemical Society Transactions, Vol. 48, Issue 1
DAXX in cancer: phenomena, processes, mechanisms and regulation
journal, July 2019
- Mahmud, Iqbal; Liao, Daiqing
- Nucleic Acids Research, Vol. 47, Issue 15
A genome-wide screen of Epstein-Barr virus proteins that modulate host SUMOylation identifies a SUMO E3 ligase conserved in herpesviruses
journal, July 2018
- De La Cruz-Herrera, Carlos F.; Shire, Kathy; Siddiqi, Umama Z.
- PLOS Pathogens, Vol. 14, Issue 7
Rhabdoviruses, Antiviral Defense, and SUMO Pathway
journal, December 2018
- Asmi, Faten El; Brantis-de-Carvalho, Carlos Eduardo; Blondel, Danielle
- Viruses, Vol. 10, Issue 12
Molecular mechanism of K65 acetylation-induced attenuation of Ubc9 and the NDSM interaction
journal, December 2017
- Naik, Mandar T.; Kang, Mooseok; Ho, Chun-Chen
- Scientific Reports, Vol. 7, Issue 1
Inhibiting ubiquitination causes an accumulation of SUMOylated newly synthesized nuclear proteins at PML bodies
journal, July 2019
- Sha, Zhe; Blyszcz, Tamara; González-Prieto, Román
- Journal of Biological Chemistry, Vol. 294, Issue 42
Structural mechanisms of HECT-type ubiquitin ligases
journal, January 2018
- Lorenz, Sonja
- Biological Chemistry, Vol. 399, Issue 2
The SUMO Pathway in Hematomalignancies and Their Response to Therapies
journal, August 2019
- Boulanger, Mathias; Paolillo, Rosa; Piechaczyk, Marc
- International Journal of Molecular Sciences, Vol. 20, Issue 16
Ubiquitin-like Protein Conjugation: Structures, Chemistry, and Mechanism
journal, February 2017
- Cappadocia, Laurent; Lima, Christopher D.
- Chemical Reviews, Vol. 118, Issue 3
Interplay between ubiquitylation and SUMOylation: Empowered by phase separation
journal, October 2019
- Jin, Jianping
- Journal of Biological Chemistry, Vol. 294, Issue 42
A comprehensive compilation of SUMO proteomics
journal, July 2016
- Hendriks, Ivo A.; Vertegaal, Alfred C. O.
- Nature Reviews Molecular Cell Biology, Vol. 17, Issue 9