DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Methionine Sulfoxide Reductase A (MsrA) and Its Function in Ubiquitin-Like Protein Modification in Archaea

Journal Article · · mBio (Online)
 [1];  [1];  [1];  [1];  [1];  [2];  [2];  [3]
  1. Univ. of Florida, Gainesville, FL (United States). Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences
  2. Univ. of Kansas, Lawrence, KS (United States). Department of Pharmacology and Toxicology
  3. Univ. of Florida, Gainesville, FL (United States). Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences and Genetics Institute

Methionine sulfoxide reductase A (MsrA) is an antioxidant enzyme found in all domains of life that catalyzes the reduction of methionine-S-sulfoxide (MSO) to methionine in proteins and free amino acids. We demonstrate that archaeal MsrA has a ubiquitin-like (Ubl) protein modification activity that is distinct from its stereospecific reduction of MSO residues. MsrA catalyzes this Ubl modification activity, with the Ubl-activating E1 UbaA, in the presence of the mild oxidant dimethyl sulfoxide (DMSO) and in the absence of reductant. In contrast, the MSO reductase activity of MsrA is inhibited by DMSO and requires reductant. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis reveals that MsrA-dependent Ubl conjugates are associated with DNA replication, protein remodeling, and oxidative stress and include the Ubl-modified MsrA, Orc3 (Orc1/Cdc6), and Cdc48d (Cdc48/p97 AAA+ ATPase). Overall, we found archaeal MsrA to have opposing MSO reductase and Ubl modifying activities that are associated with oxidative stress responses and controlled by exposure to mild oxidant.

Research Organization:
Univ. of Florida, Gainesville, FL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
Grant/Contract Number:
FG02-05ER15650
OSTI ID:
1429900
Journal Information:
mBio (Online), Vol. 8, Issue 5; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 18 works
Citation information provided by
Web of Science

References (42)

Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. journal March 1996
Inhibition of methionine sulfoxide reduction by dimethyl sulfoxide journal September 2009
Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii journal January 2010
Dimethyl sulfoxide elevates hydrogen peroxide-mediated cell death in Saccharomyces cerevisiae by inhibiting the antioxidant function of methionine sulfoxide reductase A journal September 2010
Structure of the DDB1–CRBN E3 ubiquitin ligase in complex with thalidomide journal July 2014
The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo journal September 1997
Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins journal June 1995
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
Ubiquitin–proteasome pathway and cellular responses to oxidative stress journal July 2011
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
Mechanistic insight into protein modification and sulfur mobilization activities of noncanonical E1 and associated ubiquitin-like proteins of Archaea journal October 2016
Regulating the 20S Proteasome Ubiquitin-Independent Degradation Pathway journal September 2014
Identification and Characterization of a Putative Active Site for Peptide Methionine Sulfoxide Reductase (MsrA) and Its Substrate Stereospecificity journal May 2000
[45] Escherichia coli peptide methionine sulfoxide reductase: Cloning, high expression, and purification book January 1995
Regulated protein turnover: snapshots of the proteasome in action journal January 2014
Structural and Functional Insights to Ubiquitin-Like Protein Conjugation journal May 2014
Genetic and Physical Mapping of DNA Replication Origins in Haloferax volcanii journal May 2007
E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea journal February 2011
Redox control of protein degradation journal December 2015
Structure of the human Cereblon–DDB1–lenalidomide complex reveals basis for responsiveness to thalidomide analogs journal August 2014
Characterization of the Amino Acids from Neisseria meningitidis MsrA Involved in the Chemical Catalysis of the Methionine Sulfoxide Reduction Step journal October 2006
Modification of Proteins by Ubiquitin and Ubiquitin-Like Proteins journal November 2006
Ubiquitin-Like Protein SAMP1 and JAMM/MPN+ Metalloprotease HvJAMM1 Constitute a System for Reversible Regulation of Metabolic Enzyme Activity in Archaea journal May 2015
Protein oxidation in aging and the removal of oxidized proteins journal October 2013
Empirical Statistical Model To Estimate the Accuracy of Peptide Identifications Made by MS/MS and Database Search journal October 2002
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii journal April 2016
Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius journal September 2015
The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB journal April 2002
Oxidative Stress Resistance in Deinococcus radiodurans journal March 2011
Ubiquitin-Like Proteasome System Represents a Eukaryotic-Like Pathway for Targeted Proteolysis in Archaea journal May 2016
Archaeal Ubiquitin-like SAMP3 is Isopeptide-linked to Proteins via a UbaA-dependent Mechanism journal October 2013
Selective oxidation and reduction of methionine residues in peptides and proteins by oxygen exchange between sulfoxide and sulfide. journal January 1986
Archaeal Inorganic Pyrophosphatase Displays Robust Activity under High-Salt Conditions and in Organic Solvents journal November 2015
GlpR Represses Fructose and Glucose Metabolic Enzymes at the Level of Transcription in the Haloarchaeon Haloferax volcanii journal October 2010
Development of a Gene Knockout System for the Halophilic Archaeon Haloferax volcanii by Use of the pyrE Gene journal February 2003
Development of Additional Selectable Markers for the Halophilic Archaeon Haloferax volcanii Based on the leuB and trpA Genes journal February 2004
Extracellular vesicles from symbiotic vaginal lactobacilli inhibit HIV-1 infection of human tissues journal December 2019
Genetic and physical mapping of DNA replication origins in Haloferax volcanii journal January 2005
Dimethyl Sulfoxide Elevates Hydrogen Peroxidemediated Cell Death in Saccharomyces cerevisiae by Inhibiting the Antioxidant Function of Methionine Sulfoxide Reductase A journal January 2010

Cited By (3)