Mammalian sperm head formation involves different polarization of two novel LINC complexes

PLoS One. 2010 Aug 10;5(8):e12072. doi: 10.1371/journal.pone.0012072.

Abstract

Background: LINC complexes are nuclear envelope bridging protein structures formed by interaction of SUN and KASH proteins. They physically connect the nucleus with the peripheral cytoskeleton and are critically involved in a variety of dynamic processes, such as nuclear anchorage, movement and positioning and meiotic chromosome dynamics. Moreover, they are shown to be essential for maintaining nuclear shape.

Findings: Based on detailed expression analysis and biochemical approaches, we show here that during mouse sperm development, a terminal cell differentiation process characterized by profound morphogenic restructuring, two novel distinctive LINC complexes are established. They consist either of spermiogenesis-specific Sun3 and Nesprin1 or Sun1eta, a novel non-nuclear Sun1 isoform, and Nesprin3. We could find that these two LINC complexes specifically polarize to opposite spermatid poles likely linking to sperm-specific cytoskeletal structures. Although, as shown in co-transfection/immunoprecipitation experiments, SUN proteins appear to arbitrarily interact with various KASH partners, our study demonstrates that they actually are able to confine their binding to form distinct LINC complexes.

Conclusions: Formation of the mammalian sperm head involves assembly and different polarization of two novel spermiogenesis-specific LINC complexes. Together, our findings suggest that theses LINC complexes connect the differentiating spermatid nucleus to surrounding cytoskeletal structures to enable its well-directed shaping and elongation, which in turn is a critical parameter for male fertility.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cytoskeletal Proteins
  • Cytoskeleton / metabolism*
  • Gene Expression Regulation
  • Humans
  • Male
  • Meiosis
  • Membrane Proteins / metabolism
  • Mice
  • Molecular Sequence Data
  • Nerve Tissue Proteins / metabolism
  • Nuclear Envelope / metabolism*
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / metabolism*
  • Organ Specificity
  • Protein Isoforms / chemistry
  • Protein Isoforms / metabolism
  • Protein Transport
  • Sperm Head / metabolism*
  • Spermatids / metabolism
  • Spermatogenesis
  • Testis / metabolism

Substances

  • Cytoskeletal Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Protein Isoforms
  • Syne1 protein, mouse
  • nesprin-3 protein, mouse