Disulfide isomerase glucose-regulated protein 58 is required for the nuclear localization and degradation of retinoic acid receptor alpha

Reproduction. 2010 Apr;139(4):717-31. doi: 10.1530/REP-09-0527. Epub 2010 Feb 3.

Abstract

Retinoic acid receptor alpha (RARA) is critical for spermatogenesis, as shown by a sterility phenotype observed in Rara knockout mice. RARA is important in both Sertoli and germ cells of the testis. Here, we demonstrate that a disulfide isomerase glucose-regulated protein 58 (GRp58) participates in the nuclear import and degradation of RARA in Sertoli cells. GRp58 interacted with RARA in the presence of all-trans retinoic acid (ATRA) ligand and, as a complex, it was translocated from the cytoplasm to the nucleus and, then with time, GRp58 dissociated from RARA and was found in the cytoplasm. The GRp58 RNAi treatment disrupted ATRA-dependent RARA nuclear localization, indicating the requirement of GRp58 for RARA nuclear localization. Moreover, treatment with sulfhydryl-modifying agents that oxidize SH-groups of cysteine residues to disulfide bonds abolished ATRA-mediated RARA nuclear localization, suggesting that the thiol oxidoreductase activity of GRp58 may be required for RARA nuclear import. Additionally, the proteasome inhibitor treatment resulted in the co-localization of GRp58 and RARA at the endoplasmic reticulum (ER), suggesting that GRp58 may bring RARA to the ER for the ER-associated degradation (ERAD) of RARA before it is de-coupled from RARA for recycling. In this regard, proteasome inhibitor treatment also increased the interaction of RARA with UBE2J2, an ERAD-associated ubiquitin E2 enzyme. Collectively, the results indicate that GRp58 may act as a molecular chaperone that alters the protein conformation of RARA for its delivery to the nucleus and, then with time, accompanies RARA to the ER for RARA ubiquitination and proteasome-mediated ERAD.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • COS Cells
  • Cell Nucleus / metabolism*
  • Cells, Cultured
  • Chlorocebus aethiops
  • Male
  • Models, Biological
  • Molecular Sequence Data
  • Protein Disulfide-Isomerases / antagonists & inhibitors
  • Protein Disulfide-Isomerases / metabolism
  • Protein Disulfide-Isomerases / physiology*
  • Protein Processing, Post-Translational* / drug effects
  • RNA, Small Interfering / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Retinoic Acid / metabolism*
  • Retinoic Acid Receptor alpha
  • Sequence Homology, Amino Acid
  • Tissue Distribution / drug effects

Substances

  • RNA, Small Interfering
  • Rara protein, mouse
  • Rara protein, rat
  • Receptors, Retinoic Acid
  • Retinoic Acid Receptor alpha
  • PDIA3 protein, rat
  • Protein Disulfide-Isomerases