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Title: Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O -phosphoseryl-tRNASec kinase

Abstract

Selenocysteine (Sec) biosynthesis in archaea and eukaryotes requires three steps: serylation of tRNASec by seryl-tRNA synthetase (SerRS), phosphorylation of Ser-tRNASec by O-phosphoseryl-tRNASec kinase (PSTK), and conversion of O-phosphoseryl-tRNASec (Sep-tRNASec) by SeptRNA:Sec-tRNA synthase (SepSecS) to SectRNASec. Although SerRS recognizes both tRNASec and tRNASer species, PSTK must discriminate SertRNASec from Ser-tRNASer. Based on a comparison of the sequences and secondary structures of archaeal tRNASec and tRNASer, we introduced mutations into Methanococcus maripaludis tRNASec to investigate how Methanocaldococcus jannaschii PSTK distinguishes tRNASec from tRNASer. Unlike eukaryotic PSTK, the archaeal enzyme was found to recognize the acceptor stem rather than the length and secondary structure of the D-stem. While the D-arm and T-loop provide minor identity elements, the acceptor stem base pairs G2-C71 and C3-G70 in tRNASec were crucial for discrimination from tRNASer. Furthermore, the A5-U68 base pair in tRNASer has some antideterminant properties for PSTK. Transplantation of these identity elements into the tRNASerUGA scaffold resulted in phosphorylation of the chimeric Ser-tRNA. The chimera was able to stimulate the ATPase activity of PSTK albeit at a lower level than tRNASec, whereas tRNASer did not. Additionally, the seryl moiety of Ser-tRNASec is not required for enzyme recognition, as PSTK efficiently phosphorylated Thr-tRNASec.

Authors:
 [1];  [1];  [2]
  1. Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
  2. Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry; Yale Univ., New Haven, CT (United States). Dept. of Chemistry
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)
OSTI Identifier:
1625437
Grant/Contract Number:  
GM22854; GM075602
Resource Type:
Accepted Manuscript
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Volume: 36; Journal Issue: 6; 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

Sherrer, R. Lynn, Ho, Joanne M. L., and Söll, Dieter. Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O -phosphoseryl-tRNASec kinase. United States: N. p., 2008. Web. doi:10.1093/nar/gkn036.
Sherrer, R. Lynn, Ho, Joanne M. L., & Söll, Dieter. Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O -phosphoseryl-tRNASec kinase. United States. https://doi.org/10.1093/nar/gkn036
Sherrer, R. Lynn, Ho, Joanne M. L., and Söll, Dieter. Mon . "Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O -phosphoseryl-tRNASec kinase". United States. https://doi.org/10.1093/nar/gkn036. https://www.osti.gov/servlets/purl/1625437.
@article{osti_1625437,
title = {Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O -phosphoseryl-tRNASec kinase},
author = {Sherrer, R. Lynn and Ho, Joanne M. L. and Söll, Dieter},
abstractNote = {Selenocysteine (Sec) biosynthesis in archaea and eukaryotes requires three steps: serylation of tRNASec by seryl-tRNA synthetase (SerRS), phosphorylation of Ser-tRNASec by O-phosphoseryl-tRNASec kinase (PSTK), and conversion of O-phosphoseryl-tRNASec (Sep-tRNASec) by SeptRNA:Sec-tRNA synthase (SepSecS) to SectRNASec. Although SerRS recognizes both tRNASec and tRNASer species, PSTK must discriminate SertRNASec from Ser-tRNASer. Based on a comparison of the sequences and secondary structures of archaeal tRNASec and tRNASer, we introduced mutations into Methanococcus maripaludis tRNASec to investigate how Methanocaldococcus jannaschii PSTK distinguishes tRNASec from tRNASer. Unlike eukaryotic PSTK, the archaeal enzyme was found to recognize the acceptor stem rather than the length and secondary structure of the D-stem. While the D-arm and T-loop provide minor identity elements, the acceptor stem base pairs G2-C71 and C3-G70 in tRNASec were crucial for discrimination from tRNASer. Furthermore, the A5-U68 base pair in tRNASer has some antideterminant properties for PSTK. Transplantation of these identity elements into the tRNASerUGA scaffold resulted in phosphorylation of the chimeric Ser-tRNA. The chimera was able to stimulate the ATPase activity of PSTK albeit at a lower level than tRNASec, whereas tRNASer did not. Additionally, the seryl moiety of Ser-tRNASec is not required for enzyme recognition, as PSTK efficiently phosphorylated Thr-tRNASec.},
doi = {10.1093/nar/gkn036},
journal = {Nucleic Acids Research},
number = 6,
volume = 36,
place = {United States},
year = {Mon Feb 11 00:00:00 EST 2008},
month = {Mon Feb 11 00:00:00 EST 2008}
}

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Purification and properties of suppressor seryl-tRNA:ATP phosphotransferase from bovine liver
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Transfer Ribonucleic Acids
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journal, November 1975

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Opal suppressor serine tRNAs from bovine liver form phosphoseryl-tRNA.
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journal, September 2000


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Yeast phenylalanine transfer RNA: atomic coordinates and torsion angles
journal, January 1975

  • Quigley, G. J.; Seeman, N. C.; Wang, A. H. -J.
  • Nucleic Acids Research, Vol. 2, Issue 12
  • DOI: 10.1093/nar/2.12.2329

Unique secondary and tertiary structural features of the eucaryotic selenocysteine tRNA Sec
journal, January 1993

  • Sturchler, Christine; Westhof, Eric; Carbon, Philippe
  • Nucleic Acids Research, Vol. 21, Issue 5
  • DOI: 10.1093/nar/21.5.1073

Universal rules and idiosyncratic features in tRNA identity
journal, November 1998


The characterization of phosphoseryl tRNA from lactating bovine mammary gland
journal, January 1977

  • Sharp, Stephen J.; Stewart, Thomas S.
  • Nucleic Acids Research, Vol. 4, Issue 7
  • DOI: 10.1093/nar/4.7.2123

ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences
journal, January 2004

  • Laslett, Dean; Canback, Bjorn
  • Nucleic Acids Research, Vol. 32, Issue 1, p. 11-16
  • DOI: 10.1093/nar/gkh152

The UCSC Archaeal Genome Browser
journal, January 2006


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journal, October 2006

  • Bailly, Marc; Giannouli, Stamatina; Blaise, Mickael
  • Nucleic Acids Research, Vol. 34, Issue 21
  • DOI: 10.1093/nar/gkl622

Characterization and evolutionary history of an archaeal kinase involved in selenocysteinyl-tRNA formation
journal, January 2008

  • Sherrer, R. Lynn; O’Donoghue, Patrick; Söll, Dieter
  • Nucleic Acids Research, Vol. 36, Issue 4, p. 1247-1259
  • DOI: 10.1093/nar/gkm1134

Biosynthesis of selenocysteine on its tRNA in eukaryotes
journal, April 2007


Selenocysteyl-tRNA occurs in the diatom Thalassiosira and in the ciliate Tetrahymena
journal, May 1991


Structural Basis of RNA-Dependent Recruitment of Glutamine to the Genetic Code
journal, June 2006


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