Crystal structure of a dimerization domain of human Caprin-1: insights into the assembly of an evolutionarily conserved ribonucleoprotein complex consisting of Caprin-1, FMRP and G3BP1

Acta Crystallogr D Struct Biol. 2016 Jun;72(Pt 6):718-27. doi: 10.1107/S2059798316004903. Epub 2016 May 25.

Abstract

Caprin-1 plays roles in many important biological processes, including cellular proliferation, innate immune response, stress response and synaptic plasticity. Caprin-1 has been implicated in several human diseases, including osteosarcoma, breast cancer, viral infection, hearing loss and neurodegenerative disorders. The functions of Caprin-1 depend on its molecular-interaction network. Direct interactions have been established between Caprin-1 and the fragile X mental retardation protein (FMRP), Ras GAP-activating protein-binding protein 1 (G3BP1) and the Japanese encephalitis virus (JEV) core protein. Here, crystal structures of a fragment (residues 132-251) of Caprin-1, which adopts a novel all-α-helical fold and mediates homodimerization through a substantial interface, are reported. Homodimerization creates a large and highly negatively charged concave surface suggestive of a protein-binding groove. The FMRP-interacting sequence motif forms an integral α-helix in the dimeric Caprin-1 structure in such a way that the binding of FMRP would not disrupt the homodimerization of Caprin-1. Based on insights from the structures and existing biochemical data, the existence of an evolutionarily conserved ribonucleoprotein (RNP) complex consisting of Caprin-1, FMRP and G3BP1 is proposed. The JEV core protein may bind Caprin-1 at the negatively charged putative protein-binding groove and an adjacent E-rich sequence to hijack the RNP complex.

Keywords: Caprin-1; Caprin-2; FMRP; G3BP1; JEV core protein; RNA stress granule.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Binding Sites
  • Carrier Proteins / metabolism*
  • Cell Cycle Proteins / chemistry*
  • Cell Cycle Proteins / metabolism*
  • DNA Helicases
  • Fragile X Mental Retardation Protein / metabolism*
  • Humans
  • Models, Molecular
  • Poly-ADP-Ribose Binding Proteins
  • Protein Binding
  • Protein Domains
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • RNA Helicases
  • RNA Recognition Motif Proteins
  • Sequence Alignment

Substances

  • CAPRIN1 protein, human
  • Carrier Proteins
  • Cell Cycle Proteins
  • FMR1 protein, human
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • Fragile X Mental Retardation Protein
  • DNA Helicases
  • G3BP1 protein, human
  • RNA Helicases