The iron chaperone and nucleic acid-binding activities of poly(rC)-binding protein 1 are separable and independently essential

Proc Natl Acad Sci U S A. 2021 Jun 22;118(25):e2104666118. doi: 10.1073/pnas.2104666118.

Abstract

Poly(rC)-binding protein (PCBP1) is a multifunctional adaptor protein that can coordinate single-stranded nucleic acids and iron-glutathione complexes, altering the processing and transfer of these ligands through interactions with other proteins. Multiple phenotypes are ascribed to cells lacking PCBP1, but the relative contribution of RNA, DNA, or iron chaperone activity is not consistently clear. Here, we report the identification of amino acid residues required for iron coordination on each structural domain of PCBP1 and confirm the requirement of iron coordination for binding target proteins BolA2 and ferritin. We further construct PCBP1 variants that lack either nucleic acid- or iron-binding activity and examine their functions in human cells and mouse tissues depleted of endogenous PCBP1. We find that these activities are separable and independently confer essential functions. While iron chaperone activity controls cell cycle progression and suppression of DNA damage, RNA/DNA-binding activity maintains cell viability in both cultured cell and mouse models. The coevolution of RNA/DNA binding and iron chaperone activities on a single protein may prove advantageous for nucleic acid processing that depends on enzymes with iron cofactors.

Keywords: BolA2; DNA damage; RNA-binding protein; ferritin; hnRNP E1.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cell Cycle
  • Cell Death
  • Cell Survival
  • Cyclin-Dependent Kinase Inhibitor p21 / genetics
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism
  • DNA Damage
  • DNA-Binding Proteins / metabolism*
  • Fatty Liver / metabolism
  • Fatty Liver / pathology
  • Ferritins / metabolism
  • Glutathione / metabolism
  • HEK293 Cells
  • Hepatocytes / metabolism
  • Humans
  • Iron / metabolism*
  • Liver / metabolism
  • Mice
  • Molecular Chaperones / metabolism*
  • Nucleic Acids / metabolism*
  • Oligonucleotides / metabolism
  • RNA / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / metabolism*
  • Tetraspanin 28 / genetics
  • Tetraspanin 28 / metabolism

Substances

  • Cyclin-Dependent Kinase Inhibitor p21
  • DNA-Binding Proteins
  • Molecular Chaperones
  • Nucleic Acids
  • Oligonucleotides
  • PCBP1 protein, human
  • Pcbp1 protein, mouse
  • RNA, Messenger
  • RNA-Binding Proteins
  • Tetraspanin 28
  • RNA
  • Ferritins
  • Iron
  • Glutathione