The A3243G tRNALeu(UUR) MELAS mutation causes amino acid misincorporation and a combined respiratory chain assembly defect partially suppressed by overexpression of EFTu and EFG2

Hum Mol Genet. 2008 Dec 1;17(23):3697-707. doi: 10.1093/hmg/ddn265. Epub 2008 Aug 27.

Abstract

The majority of patients with MELAS (mitochondrial encephalomyophathy, lactic acidosis, stroke-like episodes) carry a heteroplasmic A3243G mutation in the mitochondrial tRNA(Leu(UUR)). The mutation prevents modification of the wobble U base, impairing translation at UUA and UUG codons; however, whether this results in amino acid misincorporation in the mitochondrial translation products remains controversial. We tested this hypothesis in homoplasmic mutant myoblasts isolated from a MELAS patient and investigated whether overexpression of the mitochondrial translation elongation factors could suppress the translation defect. Blue-Native gel electrophoretic analysis demonstrated an almost complete lack of assembly of respiratory chain complexes I, IV and V in MELAS myoblasts. This phenotype could be partially suppressed by overexpression of EFTu or EFG2 but not EFTs or EFG1. Despite the severity of the assembly defect, overall mitochondrial protein synthesis was only moderately affected, but some anomalously migrating translation products were present. Pulse-chase labeling showed reduced stability of all mitochondrial translation products consistent with the assembly defect. Labeling patterns of the translation products were similar with [(3)H]-leucine or [(3)H]-phenylalanine, showing that loss of the wobble U modification did not permit decoding of UUY codons; however, endoproteinase fingerprint analysis showed clear evidence of amino acid misincorporation in three polypeptides: CO III, CO II and ATP6. Taken together, these data demonstrate that the A3243G mutation produces both loss- and gain-of-function phenotypes, explaining the apparent discrepancy between the severity of the translation and respiratory chain assembly defects, and suggest a function for EFG2 in quality control of translation elongation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / genetics
  • Amino Acids / metabolism*
  • Antigens, Neoplasm / chemistry
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / metabolism*
  • Cells, Cultured
  • Child
  • Electron Transport Chain Complex Proteins / genetics
  • Electron Transport Chain Complex Proteins / metabolism*
  • Female
  • Gene Expression*
  • Humans
  • MELAS Syndrome / genetics*
  • MELAS Syndrome / metabolism
  • Mitochondria / chemistry
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mitochondrial Proteins / chemistry
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Mutation, Missense*
  • Myoblasts / chemistry
  • Myoblasts / metabolism
  • Peptide Elongation Factor G / chemistry
  • Peptide Elongation Factor G / genetics
  • Peptide Elongation Factor G / metabolism*
  • Peptide Elongation Factor Tu / chemistry
  • Peptide Elongation Factor Tu / genetics
  • Peptide Elongation Factor Tu / metabolism*
  • Protein Biosynthesis
  • Protein Stability
  • RNA, Transfer, Leu / genetics*
  • RNA, Transfer, Leu / metabolism

Substances

  • Amino Acids
  • Antigens, Neoplasm
  • Electron Transport Chain Complex Proteins
  • GFM2 protein, human
  • Mitochondrial Proteins
  • Peptide Elongation Factor G
  • RNA, Transfer, Leu
  • TUFM protein, human
  • Peptide Elongation Factor Tu