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Title: Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii

Journal Article · · Proteomics
 [1];  [2];  [1];  [3];  [4];  [5]
  1. Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science. Inst. of Food and Agricultural Sciences
  2. Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science. Inst. of Food and Agricultural Sciences; Northwest A&F Univ., Yangling Shaanxi (China). College of Forestry
  3. Northwest A&F Univ., Yangling Shaanxi (China). College of Forestry
  4. Univ. of Florida, Gainesville, FL (United States). Proteomics and Mass Spectrometry. Interdisciplinary Center for Biotechnology Research. Dept. of Biology. Genetics Inst.
  5. Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science. Inst. of Food and Agricultural Sciences. Genetics Inst.
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Small archeal modifier proteins (SAMPs) are related to ubiquitin in tertiary structure and in their isopeptide linkage to substrate proteins. SAMPs also function in sulfur mobilization to form biomolecules such as molybdopterin and thiolated tRNA. While SAMP1 is essential for anaerobic growth and covalently attached to lysine residues of its molybdopterin synthase partner MoaE (K240 and K247), the full diversity of proteins modified by samp1ylation is not known. In this paper, we expand the knowledge of proteins isopeptide linked to SAMP1. LC-MS/MS analysis of -Gly-Gly signatures derived from SAMP1 S85R conjugates cleaved with trypsin was used to detect sites of sampylation (23 lysine residues) that mapped to 11 target proteins. Many of the identified target proteins were associated with sulfur metabolism and oxidative stress including MoaE, SAMP-activating E1 enzyme (UbaA), methionine sulfoxide reductase homologs (MsrA and MsrB), and the Fe-S assembly protein SufB. Several proteins were found to have multiple sites of samp1ylation, and the isopeptide linkage at SAMP3 lysines (K18, K55, and K62) revealed hetero-SAMP chain topologies. Follow-up affinity purification of selected protein targets (UbaA and MoaE) confirmed the LC-MS/MS results. 3D homology modeling suggested sampy1ylation is autoregulatory in inhibiting the activity of its protein partners (UbaA and MoaE), while occurring on the surface of some protein targets, such as SufB and MsrA/B. Finally and overall, we provide evidence that SAMP1 is a ubiquitin-like protein modifier that is relatively specific in tagging its protein partners as well as proteins associated with oxidative stress response.

Research Organization:
Univ. of Florida, Gainesville, FL (United States); Northwest A&F Univ., Yangling Shaanxi (China)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); China Scholarship Council
Grant/Contract Number:
FG02-05ER15650; R01 GM57498-15
OSTI ID:
1467086
Journal Information:
Proteomics, Vol. 16, Issue 7; ISSN 1615-9853
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 13 works
Citation information provided by
Web of Science

References (27)

Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake journal April 2013
Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii journal January 2010
The Ubiquitin System journal June 1998
Archaeal Ubiquitin-like SAMP3 is Isopeptide-linked to Proteins via a UbaA-dependent Mechanism journal October 2013
The Ubiquitin–Proteasome System of Saccharomyces cerevisiae journal October 2012
Prokaryotic Ubiquitin-Like Protein Modification journal September 2014
Archaeal JAB1/MPN/MOV34 metalloenzyme (HvJAMM1) cleaves ubiquitin-like small archaeal modifier proteins (SAMPs) from protein-conjugates: Archaeal JAMM isopeptidase journal October 2012
Development of Additional Selectable Markers for the Halophilic Archaeon Haloferax volcanii Based on the leuB and trpA Genes journal February 2004
Crystal structure of the ubiquitin-like small archaeal modifier protein 2 from Haloferax volcanii : Structures of journal July 2013
Methionine sulfoxide reductase: Chemistry, substrate binding, recycling process and oxidase activity journal December 2014
A Statistical Model for Identifying Proteins by Tandem Mass Spectrometry journal September 2003
Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre
  • Bennett‐Lovsey, Riccardo M.; Herbert, Alex D.; Sternberg, Michael J. E.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 3 https://doi.org/10.1002/prot.21688
journal January 2008
Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling journal March 2013
E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea journal February 2011
Origin and function of ubiquitin-like proteins journal March 2009
Tryptic digestion of ubiquitin standards reveals an improved strategy for identifying ubiquitinated proteins by mass spectrometry journal March 2007
Solution Structure and Activation Mechanism of Ubiquitin-Like Small Archaeal Modifier Proteins journal January 2011
Ubiquitin-Like Protein SAMP1 and JAMM/MPN+ Metalloprotease HvJAMM1 Constitute a System for Reversible Regulation of Metabolic Enzyme Activity in Archaea journal May 2015
Crystal structure of ubiquitin-like small archaeal modifier protein 1 (SAMP1) from Haloferax volcanii journal February 2011
Protein structure prediction on the Web: a case study using the Phyre server journal February 2009
Empirical Statistical Model To Estimate the Accuracy of Peptide Identifications Made by MS/MS and Database Search journal October 2002
Dimethyl sulfoxide induces oxidative stress in the yeast Saccharomyces cerevisiae journal October 2013
Archaeal Tuc1/Ncs6 Homolog Required for Wobble Uridine tRNA Thiolation Is Associated with Ubiquitin-Proteasome, Translation, and RNA Processing System Homologs journal June 2014
Proteasomal Components Required for Cell Growth and Stress Responses in the Haloarchaeon Haloferax volcanii journal October 2008
An antioxidant function for DMSP and DMS in marine algae journal July 2002
Crosstalk between ubiquitin and other post-translational modifications on chromatin during double-strand break repair journal July 2014
Inactivation of MXR1 Abolishes Formation of Dimethyl Sulfide from Dimethyl Sulfoxide inSaccharomyces cerevisiae journal September 1999

Cited By (7)

Modifying Post‐Translational Modifications: A Strategy Used by Archaea for Adapting to Changing Environments?: Manipulating the Extent, Position, or Content of Post‐Translational Modifications May Help Archaea Adapt to Environmental Change journal March 2020
Rpn11-mediated ubiquitin processing in an ancestral archaeal ubiquitination system journal July 2018
Mechanistic insight into protein modification and sulfur mobilization activities of noncanonical E1 and associated ubiquitin-like proteins of Archaea journal October 2016
The secreted salivary proteome of Asian citrus psyllid Diaphorina citri: Saliva proteins of D. citri journal September 2018
Methionine Sulfoxide Reductase A (MsrA) and Its Function in Ubiquitin-Like Protein Modification in Archaea journal September 2017
Several One-Domain Zinc Finger µ-Proteins of Haloferax Volcanii Are Important for Stress Adaptation, Biofilm Formation, and Swarming journal May 2019
Methionine Sulfoxide Reductases of Archaea journal September 2018

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
archaea
microbiology
oxidative stress
sampylation
sulfur mobilization
ubiquitin