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

Abstract

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),more » 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.« less

Authors:
 [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.
Publication Date:
Research Org.:
Univ. of Florida, Gainesville, FL (United States); Northwest A&F Univ., Yangling Shaanxi (China)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Inst. of Health (NIH) (United States); China Scholarship Council
OSTI Identifier:
1467086
Grant/Contract Number:  
FG02-05ER15650; R01 GM57498-15
Resource Type:
Accepted Manuscript
Journal Name:
Proteomics
Additional Journal Information:
Journal Volume: 16; Journal Issue: 7; Journal ID: ISSN 1615-9853
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; archaea; microbiology; oxidative stress; sampylation; sulfur mobilization; ubiquitin

Citation Formats

Dantuluri, Swathi, Wu, Yifei, Hepowit, Nathaniel L., Chen, Hui, Chen, Sixue, and Maupin-Furlow, Julie A. Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii. United States: N. p., 2016. Web. doi:10.1002/pmic.201500153.
Dantuluri, Swathi, Wu, Yifei, Hepowit, Nathaniel L., Chen, Hui, Chen, Sixue, & Maupin-Furlow, Julie A. Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii. United States. doi:10.1002/pmic.201500153.
Dantuluri, Swathi, Wu, Yifei, Hepowit, Nathaniel L., Chen, Hui, Chen, Sixue, and Maupin-Furlow, Julie A. Wed . "Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii". United States. doi:10.1002/pmic.201500153. https://www.osti.gov/servlets/purl/1467086.
@article{osti_1467086,
title = {Proteome targets of ubiquitin-like samp1ylation are associated with sulfur metabolism and oxidative stress in Haloferax volcanii},
author = {Dantuluri, Swathi and Wu, Yifei and Hepowit, Nathaniel L. and Chen, Hui and Chen, Sixue and Maupin-Furlow, Julie A.},
abstractNote = {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.},
doi = {10.1002/pmic.201500153},
journal = {Proteomics},
number = 7,
volume = 16,
place = {United States},
year = {2016},
month = {2}
}

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