Online citations, reference lists, and bibliographies.

Structure Determination Of The Small Ubiquitin-related Modifier SUMO-1.

P. Bayer, A. Arndt, S. Metzger, R. Mahajan, F. Melchior, R. Jaenicke, J. Becker
Published 1998 · Chemistry, Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
The recently discovered small ubiquitin-related modifier SUMO-1 belongs to the growing family of ubiquitin-related proteins involved in postranslational protein modification. Unlike ubiquitin, SUMO-1 does not appear to target proteins for degradation but seems to be involved in the modulation of protein-protein interactions. Independent studies demonstrate an essential function of SUMO-1 in the regulation of nucleo-cytoplasmic transport, and suggest a role in cell-cycle regulation and apoptosis. Here, we present the first three-dimensional structure of SUMO-1 solved by NMR. Although having only 18% amino acid sequence identity with ubiquitin, the overall structure closely resembles that of ubiquitin, featuring the betabetaalphabetabetaalphabeta fold of the ubiquitin protein family. In addition, the position of the two C-terminal Gly residues required for isopeptide bond formation is conserved between ubiquitin and SUMO-1. The most prominent feature of SUMO-1 is a long and highly flexible N terminus, which protrudes from the core of the protein and which is absent in ubiquitin. Furthermore, ubiquitin Lys48, required to generate ubiquitin polymers, is substituted in SUMO-1 by Gln69 at the same position, which provides an explanation of why SUMO-1 has not been observed to form polymers. Moreover, the hydrophobic core of SUMO-1 and ubiquitin is maintained by conserved hydrophobic residues, whereas the overall charge topology of SUMO-1 and ubiquitin differs significantly, suggesting specific modifying enzymes and target proteins for both proteins.
This paper references
10.1016/S0962-8924(97)01132-X
SUMO-1: Ubiquitin gains weight.
P. Johnson (1997)
10.1083/JCB.140.3.499
SUMO-1 Modification and Its Role in Targeting the Ran GTPase-activating Protein, RanGAP1, to the Nuclear Pore Complex
M. Matunis (1998)
10.1074/jbc.273.11.6503
Modification of Ran GTPase-activating Protein by the Small Ubiquitin-related Modifier SUMO-1 Requires Ubc9, an E2-type Ubiquitin-conjugating Enzyme Homologue*
G. Lee (1998)
10.1016/j.bbrc.2012.08.018
Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of (1)H-(1)H spin-spin coupling constants in proteins. 1983.
D. Marion (1983)
10.1016/S0968-0004(96)10054-2
Lessons from the discovery ofthe ubiquitin system
A. Hershko (1996)
10.1073/pnas.74.3.864
Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24.
I. Goldknopf (1977)
10.1016/0955-0674(95)80031-X
Ubiquitin, proteasomes, and the regulation of intracellular protein degradation.
M. Hochstrasser (1995)
10.1074/jbc.272.22.14001
Preferential Modification of Nuclear Proteins by a Novel Ubiquitin-like Molecule*
T. Kamitani (1997)
10.1091/MBC.6.7.793
Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C.
P. Meluh (1995)
10.1016/S0968-0004(97)01122-5
The ubiquitin system.
A. Varshavsky (1997)
10.1006/BBRC.1996.0717
Cloning and expression of human homolog HSMT3 to yeast SMT3 suppressor of MIF2 mutations in a centromere protein gene.
Hideyuki Mannen (1996)
PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia.
M. N. Boddy (1996)
10.1002/PROT.340110407
Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons.
A. Nicholls (1991)
10.1007/978-1-4899-2049-2_4
Ubiquitin Activation and Ligation
C. Pickart (1988)
10.1016/0006-291X(80)90695-6
A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules.
A. Kumar (1980)
10.1051/epn/19861701011
NMR of proteins and nucleic acids
K. Wüthrich (1986)
10.1083/JCB.135.6.1457
A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex
M. Matunis (1996)
10.1083/JCB.133.6.1331
Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center
S. Biggins (1996)
10.1038/376184A0
A giant nucleopore protein that binds Ran/TC4
N. Yokoyama (1995)
10.1021/bi00444a016
Determination of the three-dimensional solution structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing.
J. Kraulis (1989)
10.1021/bi00891a003
EQUILIBRIUM ULTRACENTRIFUGATION OF DILUTE SOLUTIONS.
D. A. Yphantis (1964)
10.1016/S0092-8674(00)81862-0
A Small Ubiquitin-Related Polypeptide Involved in Targeting RanGAP1 to Nuclear Pore Complex Protein RanBP2
R. Mahajan (1997)
10.1021/BI00181A032
Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR.
T. Gallagher (1994)
10.1006/GENO.1996.4556
SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family.
V. Lapenta (1997)
10.1038/365661A0
The GTP-binding protein Ran/TC4 is required for protein import into the nucleus
M. S. Moore (1993)
10.1073/PNAS.94.8.3736
RanBP2 associates with Ubc9p and a modified form of RanGAP1.
H. Saitoh (1997)
10.1016/S0092-8674(00)80982-4
Ubiquitination of a Yeast Plasma Membrane Receptor Signals Its Ligand-Stimulated Endocytosis
L. Hicke (1996)
10.1016/S0014-5793(97)01076-4
Ras‐binding domains: predicting function versus folding
G. Kalhammer (1997)
10.1016/0006-291X(83)91225-1
Improved spectral resolution in cosy 1H NMR spectra of proteins via double quantum filtering.
M. Rance (1983)
10.1074/jbc.272.43.26799
Ubc9p Is the Conjugating Enzyme for the Ubiquitin-like Protein Smt3p*
E. Johnson (1997)
10.1073/PNAS.92.5.1749
Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport.
F. Bischoff (1995)
10.1006/BBRC.1997.6709
Identification and characterization of the SMT3 cDNA and gene from nematode Caenorhabditis elegans.
B. K. Choudhury (1997)
10.1016/S0014-5793(97)01305-7
Ubch9 conjugates SUMO but not ubiquitin
J. M. Desterro (1997)
Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin.
T. Okura (1996)
10.1007/BF00211777
1H, 13C and 15N chemical shift referencing in biomolecular NMR
D. Wishart (1995)
10.1016/S0022-2836(83)80144-2
Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance.
K. Wüthrich (1983)
10.1038/NSB0997-694
Structure of the Ras-binding domain of RalGEF and implications for Ras binding and signalling
M. Geyer (1997)
10.1006/GENO.1996.0462
UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins.
Z. Shen (1996)
10.1016/S0092-8674(00)81064-8
Site-Specific Phosphorylation of IκBα by a Novel Ubiquitination-Dependent Protein Kinase Activity
Z. Chen (1996)
10.1107/S0108767390010224
Improved methods for building protein models in electron density maps and the location of errors in these models.
T. Jones (1991)
10.1093/emboj/16.18.5509
The ubiquitin‐like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer
E. Johnson (1997)
10.1128/MCB.13.12.7757
The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function.
J. F. Watkins (1993)
10.1002/bip.360221211
Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features
W. Kabsch (1983)
10.1016/0092-8674(95)90021-7
Selective protein degradation: A journey's end within the proteasome
S. Jentsch (1995)
10.1021/ja00231a044
Clean TOCSY for proton spin system identification in macromolecules
C. Griesinger (1988)
10.1128/MCB.14.12.8408
Conjugates of ubiquitin cross-reactive protein distribute in a cytoskeletal pattern.
K. Loeb (1994)
10.1083/JCB.130.5.1017
Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import
A. Corbett (1995)
10.1038/375554A0
The 2.2 Å crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with RaplA and a GTP analogue
N. Nassar (1995)
10.1016/0092-8674(87)90149-8
Arthrin, a myofibrillar protein of insect flight muscle, is an actin-ubiquitin conjugate
E. Ball (1987)
10.1017/S0033583500005515
Heteronuclear three-dimensional NMR spectroscopy of isotopically labelled biological macromolecules.
S. Fesik (1990)
10.1074/JBC.270.20.11860
RNA1 Encodes a GTPase-activating Protein Specific for Gsp1p, the Ran/TC4 Homologue of Saccharomyces cerevisiae(*)
J. Becker (1995)
10.1007/BF00211764
1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects
D. Wishart (1995)
10.1021/BI00121A010
The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy.
D. Wishart (1992)
10.1007/BF02192855
Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions
M. Piotto (1992)
10.1083/JCB.140.2.259
Molecular Characterization of the SUMO-1 Modification of RanGAP1 and Its Role in Nuclear Envelope Association
R. Mahajan (1998)
The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins.
K. Loeb (1992)
10.1146/ANNUREV.GENET.30.1.405
Ubiquitin-dependent protein degradation.
M. Hochstrasser (1996)
10.1021/JA00079A052
The Importance of Not Saturating H2o in Protein NMR : application to Sensitivity Enhancement and Noe Measurements
S. Grzesiek (1993)
10.1016/S0022-2836(05)80330-4
Structure of the [2Fe-2S] ferredoxin I from the blue-green alga Aphanothece sacrum at 2.2 A resolution.
T. Tsukihara (1990)
Human RanGTPase activating protein RanGAP1 is a homolog of yeast RNA1p involved in messenger RNA processing and transport
F. Bischoff (1995)
10.1006/GENO.1996.0540
Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system.
Z. Shen (1996)
10.1074/JBC.270.23.14209
Nup358, a Cytoplasmically Exposed Nucleoporin with Peptide Repeats, Ran-GTP Binding Sites, Zinc Fingers, a Cyclophilin A Homologous Domain, and a Leucine-rich Region (*)
J. Wu (1995)
10.1021/BI961144M
Structure of Synechococcus elongatus [Fe2S2] ferredoxin in solution.
B. Baumann (1996)
10.1038/372631A0
Protein superfamilles and domain superfolds
C. Orengo (1994)
10.1016/0092-8674(94)90396-4
The ubiquitin-proteasome proteolytic pathway
A. Ciechanover (1994)
10.1083/JCB.123.6.1649
Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor [published erratum appears in J Cell Biol 1994 Jan;124(1-2):217]
F. Melchior (1993)
10.1126/SCIENCE.2047852
Structures of larger proteins in solution: three- and four-dimensional heteronuclear NMR spectroscopy.
G. Clore (1991)



This paper is referenced by
10.1038/sj.onc.1204758
SUMO: of branched proteins and nuclear bodies
Jacob-S. Seeler (2001)
10.1074/jbc.M110.114660
Role of the Zn2+ Motif of E1 in SUMO Adenylation*
Jianghai Wang (2010)
10.1038/35056591
Ubiquitin and proteasomes: Sumo, ubiquitin's mysterious cousin
S. Müller (2001)
10.1016/J.JMB.2007.04.007
Structure of a SUMO-binding-motif mimic bound to Smt3p-Ubc9p: conservation of a non-covalent ubiquitin-like protein-E2 complex as a platform for selective interactions within a SUMO pathway.
David M. Duda (2007)
Regulación de la proteína quinasa Akt por conjugación a SUMO
Guillermo J. Risso (2013)
10.1016/J.APSUSC.2016.10.195
Atomic Force Microscopy and Spectroscopic Ellipsometry combined analysis of Small Ubiquitin-like Modifier adsorption on functional monolayers
I. Solano (2017)
Identification and functional characterization of the novel MAR-binding protein, SATB2
G. Dobreva (2004)
Molecular and Genetic Analysis of the effects of SUMOylation on the regulation of floral transition in Arabidopsis
Mitzi Villajuana Bonequi (2011)
The enzymology and substrate selectivity of the ISG15 conjugation system
L. Durfee (2010)
10.2741/S388
Sumo paralogs: redundancy and divergencies.
Simona Citro (2013)
10.1016/j.bpj.2013.04.008
Single-molecule studies on PolySUMO proteins reveal their mechanical flexibility.
Hema Chandra Kotamarthi (2013)
10.1016/J.BBAMCR.2004.09.021
SUMO protein modification.
R. Dohmen (2004)
10.1529/BIOPHYSJ.105.071746
Local structural preferences and dynamics restrictions in the urea-denatured state of SUMO-1: NMR characterization.
A. Kumar (2006)
10.1007/s12017-013-8258-6
SUMO Rules: Regulatory Concepts and Their Implication in Neurologic Functions
Mathias Droescher (2013)
10.1007/s13361-014-0902-3
PAS-cal: a Generic Recombinant Peptide Calibration Standard for Mass Spectrometry
Joscha Breibeck (2014)
of Ubiquitin-Like Proteins Conjugating and Deconjugating Enzymes Specific and Covalent Targeting of
J. Hemelaar (2003)
A STUDY ON THE E3 LIGASE TRIM21/RO52
Alexander Espinosa (2008)
Probing Septin Function Through Interaction Screens: Identification of Novel Septins and Possible Regulatory Mechanisms
Jonathan D. Steels (2008)
10.1016/j.str.2020.04.002
Characterization of a C-Terminal SUMO-Interacting Motif Present in Select PIAS-Family Proteins.
Mathieu Lussier-Price (2020)
10.1074/jbc.274.18.12555
The Nuclear Dot Protein Sp100, Characterization of Domains Necessary for Dimerization, Subcellular Localization, and Modification by Small Ubiquitin-like Modifiers*
T. Sternsdorf (1999)
10.2741/GOET
Structural attributes in the conjugation of ubiquitin, SUMO and RUB to protein substrates
Sandra Goettsch (2002)
10.1021/PR0341080
Chemistry-based functional proteomics: mechanism-based activity-profiling tools for ubiquitin and ubiquitin-like specific proteases.
J. Hemelaar (2004)
10.1042/BJ20041991
Nep1, a Schizosaccharomyces pombe deneddylating enzyme.
Lihong Zhou (2005)
10.1073/PNAS.0604876103
Solution structure of Urm1 and its implications for the origin of protein modifiers.
Junjie Xu (2006)
10.1007/s11064-020-03066-3
A Critical Role for ISGylation, Ubiquitination and, SUMOylation in Brain Damage: Implications for Neuroprotection
Venkata Prasuja Nakka (2020)
Studies on the small ubiquitin-like modifier (SUMO) E2 conjugases of the SUMOylation system in Chlamydomonas reinhardtii and their role in stress physiology
Amy R Knobbe (2012)
10.3390/ijms130911804
Modification by Ubiquitin-Like Proteins: Significance in Apoptosis and Autophagy Pathways
Umar-Faruq Cajee (2012)
SUMO and ubiquitin : The Yin and Yang of IGF-1R function
B. Sehat (2007)
10.1096/fj.12-216473
Impaired SIRT1 nucleocytoplasmic shuttling in the senescent heart during ischemic stress
C. Tong (2013)
10.1371/journal.pone.0134950
Biosynthesis of SUMOylated Proteins in Bacteria Using the Trypanosoma brucei Enzymatic System
P. A. Iribarren (2015)
10.1095/biolreprod63.2.619
Production, Purification, and Carboxy-Terminal Sequencing of Bioactive Recombinant Bovine Interferon-Stimulated Gene Product 171
J. Pru (2000)
MOLECULAR DETERMINANTS OF ANDROGEN ACTION
H. Santti (2004)
See more
Semantic Scholar Logo Some data provided by SemanticScholar