ERMA (TMEM94) is a P-type ATPase transporter for Mg2+ uptake in the endoplasmic reticulum

Mol Cell. 2024 Apr 4;84(7):1321-1337.e11. doi: 10.1016/j.molcel.2024.02.033. Epub 2024 Mar 20.

Abstract

Intracellular Mg2+ (iMg2+) is bound with phosphometabolites, nucleic acids, and proteins in eukaryotes. Little is known about the intracellular compartmentalization and molecular details of Mg2+ transport into/from cellular organelles such as the endoplasmic reticulum (ER). We found that the ER is a major iMg2+ compartment refilled by a largely uncharacterized ER-localized protein, TMEM94. Conventional and AlphaFold2 predictions suggest that ERMA (TMEM94) is a multi-pass transmembrane protein with large cytosolic headpiece actuator, nucleotide, and phosphorylation domains, analogous to P-type ATPases. However, ERMA uniquely combines a P-type ATPase domain and a GMN motif for ERMg2+ uptake. Experiments reveal that a tyrosine residue is crucial for Mg2+ binding and activity in a mechanism conserved in both prokaryotic (mgtB and mgtA) and eukaryotic Mg2+ ATPases. Cardiac dysfunction by haploinsufficiency, abnormal Ca2+ cycling in mouse Erma+/- cardiomyocytes, and ERMA mRNA silencing in human iPSC-cardiomyocytes collectively define ERMA as an essential component of ERMg2+ uptake in eukaryotes.

Keywords: AlphaFold2; ERMA; GMN motif; P-type ATPase; RNAi screen; TMEM94; calcium; endoplasmic reticulum; hepatocytes; human cardiomyocytes; lactate; magnesium; mitochondria; mutations; refill; uptake.

MeSH terms

  • Adenosine Triphosphatases* / metabolism
  • Animals
  • Biological Transport
  • Calcium / metabolism
  • Endoplasmic Reticulum / genetics
  • Endoplasmic Reticulum / metabolism
  • Humans
  • Membrane Transport Proteins / metabolism
  • Mice
  • P-type ATPases* / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases

Substances

  • Adenosine Triphosphatases
  • Membrane Transport Proteins
  • P-type ATPases
  • Calcium
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases