A novel germ cell-specific protein, SHIP1, forms a complex with chromatin remodeling activity during spermatogenesis

J Biol Chem. 2008 Dec 12;283(50):35283-94. doi: 10.1074/jbc.M805590200. Epub 2008 Oct 10.

Abstract

To determine the mechanisms of spermatogenesis, it is essential to identify and characterize germ cell-specific genes. Here we describe a protein encoded by a novel germ cell-specific gene, Mm.290718/ZFP541, identified from the mouse spermatocyte UniGene library. The protein contains specific motifs and domains potentially involved in DNA binding and chromatin reorganization. An antibody against Mm.290718/ZFP541 revealed the existence of the protein in testicular spermatogenic cells (159 kDa) but not testicular and mature sperm. Immunostaining analysis of cells at various stages of spermatogenesis consistently showed that the protein is present in spermatocytes and round spermatids only. Transfection assays and immunofluorescence studies indicate that the protein is localized specifically in the nucleus. Proteomic analyses performed to explore the functional characteristics of Mm.290718/ZFP541 showed that the protein forms a unique complex. Other major components of the complex included histone deacetylase 1 (HDAC1) and heat-shock protein A2. Disappearance of Mm.290718/ZFP541 was highly correlated with hyperacetylation in spermatids during spermatogenesis, and specific domains of the protein were involved in the regulation of interactions and nuclear localization of HDAC1. Furthermore, we found that premature hyperacetylation, induced by an HDAC inhibitor, is associated with an alteration in the integrity of Mm.290718/ZFP541 in spermatogenic cells. Our results collectively suggest that the Mm.290718/ZFP541 complex is implicated in chromatin remodeling during spermatogenesis, and we provide further information on the previously unknown molecular mechanism. Consequently, we re-designate Mm.290718/ZFP541 as "SHIP1" representing spermatogenic cell HDAC-interacting protein 1.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology*
  • Cell Nucleus / metabolism
  • Chromatin / chemistry*
  • Chromatin / metabolism
  • Chromosomal Proteins, Non-Histone / chemistry
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / physiology*
  • Histone Deacetylase 1
  • Histone Deacetylases / metabolism
  • Male
  • Mice
  • Models, Biological
  • Molecular Sequence Data
  • Sequence Homology, Amino Acid
  • Spermatogenesis*
  • Spermatozoa / metabolism
  • Testis / metabolism*
  • Transcription Factors
  • Zinc Fingers / genetics
  • Zinc Fingers / physiology*

Substances

  • Carrier Proteins
  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • Transcription Factors
  • ZFP541 protein, mouse
  • Hdac1 protein, mouse
  • Histone Deacetylase 1
  • Histone Deacetylases