Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase
Abstract
In all organisms, aminoacyl tRNA synthetases covalently attach amino acids to their cognate tRNAs. Many eukaryotic tRNA synthetases have acquired appended domains, whose origin, structure and function are poorly understood. The N-terminal appended domain (NTD) of glutaminyl-tRNA synthetase (GlnRS) is intriguing since GlnRS is primarily a eukaryotic enzyme, whereas in other kingdoms Gln-tRNAGln is primarily synthesized by first forming Glu-tRNAGln, followed by conversion to Gln-tRNAGln by a tRNA-dependent amidotransferase. We report a functional and structural analysis of the NTD of Saccharomyces cerevisiae GlnRS, Gln4. Yeast mutants lacking the NTD exhibit growth defects, and Gln4 lacking the NTD has reduced complementarity for tRNAGln and glutamine. The 187-amino acid Gln4 NTD, crystallized and solved at 2.3 Å resolution, consists of two subdomains, each exhibiting an extraordinary structural resemblance to adjacent tRNA specificity determining domains in the GatB subunit of the GatCAB amidotransferase, which forms Gln-tRNAGln. These subdomains are connected by an apparent hinge comprised of conserved residues. Mutation of these amino acids produces Gln4 variants with reduced affinity for tRNAGln, consistent with a hinge-closing mechanism proposed for GatB recognition of tRNA. Our results suggest a possible origin and function of the NTD that would link the phylogenetically diverse mechanisms of Gln-tRNAGln synthesis.
- Authors:
-
- State Univ. of New York (SUNY), Buffalo, NY (United States)
- Univ. of Rochester, NY (United States). Center for Pediatric Biomedical Research
- Univ. of California, Santa Barbara, CA (United States). Dept. of Chemistry and Biochemistry
- Univ. of Rochester, NY (United States). Center for Pediatric Biomedical Research; Univ. of Rochester, NY (United States). Medical School, Dept. of Biochemistry and Biophysics
- Univ. of Rochester, NY (United States). Center for Pediatric Biomedical Research; Univ. of Rochester, NY (United States). Medical School
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Defense Threat Reduction Agency (DTRA); National Institutes of Health (NIH)
- OSTI Identifier:
- 1625487
- Grant/Contract Number:
- AC02-76SF00515; HDTRA1-10- C-0057; U54 GM074899; GM63713
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 40; Journal Issue: 8; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology
Citation Formats
Grant, Thomas D., Snell, Edward H., Luft, Joseph R., Quartley, Erin, Corretore, Stephanie, Wolfley, Jennifer R., Elizabeth Snell, M., Hadd, Andrew, Perona, John J., Phizicky, Eric M., and Grayhack, Elizabeth J. Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase. United States: N. p., 2011.
Web. doi:10.1093/nar/gkr1223.
Grant, Thomas D., Snell, Edward H., Luft, Joseph R., Quartley, Erin, Corretore, Stephanie, Wolfley, Jennifer R., Elizabeth Snell, M., Hadd, Andrew, Perona, John J., Phizicky, Eric M., & Grayhack, Elizabeth J. Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase. United States. https://doi.org/10.1093/nar/gkr1223
Grant, Thomas D., Snell, Edward H., Luft, Joseph R., Quartley, Erin, Corretore, Stephanie, Wolfley, Jennifer R., Elizabeth Snell, M., Hadd, Andrew, Perona, John J., Phizicky, Eric M., and Grayhack, Elizabeth J. Fri .
"Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase". United States. https://doi.org/10.1093/nar/gkr1223. https://www.osti.gov/servlets/purl/1625487.
@article{osti_1625487,
title = {Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase},
author = {Grant, Thomas D. and Snell, Edward H. and Luft, Joseph R. and Quartley, Erin and Corretore, Stephanie and Wolfley, Jennifer R. and Elizabeth Snell, M. and Hadd, Andrew and Perona, John J. and Phizicky, Eric M. and Grayhack, Elizabeth J.},
abstractNote = {In all organisms, aminoacyl tRNA synthetases covalently attach amino acids to their cognate tRNAs. Many eukaryotic tRNA synthetases have acquired appended domains, whose origin, structure and function are poorly understood. The N-terminal appended domain (NTD) of glutaminyl-tRNA synthetase (GlnRS) is intriguing since GlnRS is primarily a eukaryotic enzyme, whereas in other kingdoms Gln-tRNAGln is primarily synthesized by first forming Glu-tRNAGln, followed by conversion to Gln-tRNAGln by a tRNA-dependent amidotransferase. We report a functional and structural analysis of the NTD of Saccharomyces cerevisiae GlnRS, Gln4. Yeast mutants lacking the NTD exhibit growth defects, and Gln4 lacking the NTD has reduced complementarity for tRNAGln and glutamine. The 187-amino acid Gln4 NTD, crystallized and solved at 2.3 Å resolution, consists of two subdomains, each exhibiting an extraordinary structural resemblance to adjacent tRNA specificity determining domains in the GatB subunit of the GatCAB amidotransferase, which forms Gln-tRNAGln. These subdomains are connected by an apparent hinge comprised of conserved residues. Mutation of these amino acids produces Gln4 variants with reduced affinity for tRNAGln, consistent with a hinge-closing mechanism proposed for GatB recognition of tRNA. Our results suggest a possible origin and function of the NTD that would link the phylogenetically diverse mechanisms of Gln-tRNAGln synthesis.},
doi = {10.1093/nar/gkr1223},
journal = {Nucleic Acids Research},
number = 8,
volume = 40,
place = {United States},
year = {Fri Dec 16 00:00:00 EST 2011},
month = {Fri Dec 16 00:00:00 EST 2011}
}
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