Balancing of mitochondrial translation through METTL8-mediated m3C modification of mitochondrial tRNAs

Mol Cell. 2021 Dec 2;81(23):4810-4825.e12. doi: 10.1016/j.molcel.2021.10.018. Epub 2021 Nov 12.

Abstract

Mitochondria contain a specific translation machinery for the synthesis of mitochondria-encoded respiratory chain components. Mitochondrial tRNAs (mt-tRNAs) are also generated from the mitochondrial DNA and, similar to their cytoplasmic counterparts, are post-transcriptionally modified. Here, we find that the RNA methyltransferase METTL8 is a mitochondrial protein that facilitates 3-methyl-cytidine (m3C) methylation at position C32 of the mt-tRNASer(UCN) and mt-tRNAThr. METTL8 knockout cells show a reduction in respiratory chain activity, whereas overexpression increases activity. In pancreatic cancer, METTL8 levels are high, which correlates with lower patient survival and an enhanced respiratory chain activity. Mitochondrial ribosome profiling uncovered mitoribosome stalling on mt-tRNASer(UCN)- and mt-tRNAThr-dependent codons. Further analysis of the respiratory chain complexes using mass spectrometry revealed reduced incorporation of the mitochondrially encoded proteins ND6 and ND1 into complex I. The well-balanced translation of mt-tRNASer(UCN)- and mt-tRNAThr-dependent codons through METTL8-mediated m3C32 methylation might, therefore, facilitate the optimal composition and function of the mitochondrial respiratory chain.

Keywords: METTL8; RNA modification; m(3)C; mt-tRNA; translation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anticodon
  • Cell Proliferation
  • Codon
  • Cytoplasm
  • DNA, Mitochondrial / metabolism
  • Electron Transport
  • Green Fluorescent Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Methyltransferases / metabolism*
  • Mice
  • Mitochondria / metabolism
  • Mitochondrial Membranes
  • Mitochondrial Proteins / chemistry
  • Oxygen Consumption
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / mortality
  • RNA, Mitochondrial / chemistry*
  • RNA, Transfer / chemistry*
  • Ribosomes / metabolism
  • Up-Regulation

Substances

  • Anticodon
  • Codon
  • DNA, Mitochondrial
  • Mitochondrial Proteins
  • RNA, Mitochondrial
  • Green Fluorescent Proteins
  • RNA, Transfer
  • METTL8 protein, human
  • Methyltransferases
  • Mettl8 protein, mouse
  • m(5)C rRNA methyltransferase