TFB2M and POLRMT are essential for mammalian mitochondrial DNA replication

Biochim Biophys Acta Mol Cell Res. 2022 Jan;1869(1):119167. doi: 10.1016/j.bbamcr.2021.119167. Epub 2021 Oct 30.

Abstract

Two classes of replication intermediates have been observed from mitochondrial DNA (mtDNA) in many mammalian tissue and cells with two-dimensional agarose gel electrophoresis. One is assigned to leading-strand synthesis in the absence of synchronous lagging-strand synthesis (strand-asynchronous replication), and the other has properties of coupled leading- and lagging-strand synthesis (strand-coupled replication). While strand-asynchronous replication is primed by long noncoding RNA synthesized from a defined transcription initiation site, little is known about the commencement of strand-coupled replication. To investigate it, we attempted to abolish strand-asynchronous replication in cultured human cybrid cells by knocking out the components of the transcription initiation complexes, mitochondrial transcription factor B2 (TFB2M/mtTFB2) and mitochondrial RNA polymerase (POLRMT/mtRNAP). Unexpectedly, removal of either protein resulted in complete mtDNA loss, demonstrating for the first time that TFB2M and POLRMT are indispensable for the maintenance of human mtDNA. Moreover, a lack of TFB2M could not be compensated for by mitochondrial transcription factor B1 (TFB1M/mtTFB1). These findings indicate that TFB2M and POLRMT are crucial for the priming of not only strand-asynchronous but also strand-coupled replication, providing deeper insights into the molecular basis of mtDNA replication initiation.

Keywords: Mitochondrial DNA; Mitochondrial RNA polymerase; Mitochondrial transcription factor; Replication initiation; Strand-asynchronous replication; Strand-coupled replication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA Replication*
  • DNA, Mitochondrial / genetics*
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism*
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Methyltransferases / genetics
  • Methyltransferases / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • DNA, Mitochondrial
  • Mitochondrial Proteins
  • Transcription Factors
  • Methyltransferases
  • TFB2M protein, human
  • DNA-Directed RNA Polymerases
  • POLRMT protein, human