Biogenesis of glutaminyl-mt tRNAGln in human mitochondria

Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16209-14. doi: 10.1073/pnas.0907602106. Epub 2009 Sep 9.

Abstract

Mammalian mitochondrial (mt) tRNAs, which are required for mitochondrial protein synthesis, are all encoded in the mitochondrial genome, while mt aminoacyl-tRNA synthetases (aaRSs) are encoded in the nuclear genome. However, no mitochondrial homolog of glutaminyl-tRNA synthetase (GlnRS) has been identified in mammalian genomes, implying that Gln-tRNA(Gln) is synthesized via an indirect pathway in the mammalian mitochondria. We demonstrate here that human mt glutamyl-tRNA synthetase (mtGluRS) efficiently misaminoacylates mt tRNA(Gln) to form Glu-tRNA(Gln). In addition, we have identified a human homolog of the Glu-tRNA(Gln) amidotransferase, the hGatCAB heterotrimer. When any of the hGatCAB subunits were inactivated by siRNA-mediated knock down in human cells, the Glu-charged form of tRNA(Gln) accumulated and defects in respiration could be observed. We successfully reconstituted in vitro Gln-tRNA(Gln) formation catalyzed by the recombinant mtGluRS and hGatCAB. The misaminoacylated form of tRNA(Gln) has a weak binding affinity to the mt elongation factor Tu (mtEF-Tu), indicating that the misaminoacylated form of tRNA(Gln) is rejected from the translational apparatus to maintain the accuracy of mitochondrial protein synthesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acyl-tRNA Synthetases / genetics
  • Amino Acyl-tRNA Synthetases / metabolism*
  • Animals
  • Blotting, Northern
  • Cattle
  • Glutamate-tRNA Ligase / genetics
  • Glutamate-tRNA Ligase / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HeLa Cells
  • Humans
  • Kinetics
  • Microscopy, Fluorescence
  • Mitochondria / metabolism*
  • Molecular Sequence Data
  • Nitrogenous Group Transferases / genetics
  • Nitrogenous Group Transferases / metabolism
  • Nucleic Acid Conformation
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • RNA Interference
  • RNA, Transfer, Amino Acyl / biosynthesis*
  • RNA, Transfer, Amino Acyl / chemistry
  • RNA, Transfer, Gln / biosynthesis*
  • RNA, Transfer, Gln / chemistry
  • RNA, Transfer, Glu / biosynthesis
  • RNA, Transfer, Glu / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Transfection
  • Transfer RNA Aminoacylation

Substances

  • Protein Subunits
  • RNA, Transfer, Amino Acyl
  • RNA, Transfer, Gln
  • RNA, Transfer, Glu
  • Recombinant Fusion Proteins
  • glutamyl-tRNA(Gln)
  • Green Fluorescent Proteins
  • Nitrogenous Group Transferases
  • Amino Acyl-tRNA Synthetases
  • Glutamate-tRNA Ligase
  • glutaminyl-tRNA synthetase