Spermatid head elongation with normal nuclear shaping requires ADPRibosyltransferase PARP11 (ARTD11) in mice

Mirella L. Meyer-Ficca, Motomasa Ihara, Jessica J. Bader, N. Adrian Leu, Sascha Beneke, Ralph G. Meyer

Research output: Contribution to journalArticlepeer-review

26 Citations (Scopus)

Abstract

Sperm are highly differentiated cells characterized by their species-specific nuclear shapes and extremely condensed chromatin. Abnormal head shapes represent a form of teratozoospermia that can impair fertilization capacity. This study shows that poly(ADP-ribose) polymerase-11 (ARTD11/PARP11), a member of the ADP-ribosyltransferase (ARTD) family, is expressed preferentially in spermatids undergoing nuclear condensation and differentiation. Deletion of the Parp11 gene results in teratozoospermia and male infertility in mice due to the formation of abnormally shaped fertilization-incompetent sperm, despite normal testis weights and sperm counts. At the subcellular level, PARP11-deficient elongating spermatids reveal structural defects in the nuclear envelope and chromatin detachment associated with abnormal nuclear shaping, suggesting functional relevance of PARP11 for nuclear envelope stability and nuclear reorganization during spermiogenesis. In vitro, PARP11 exhibits mono(ADP-ribosyl)ation activity with the ability to ADP-ribosylate itself. In transfected somatic cells, PARP11 colocalizes with nuclear pore components, such as NUP153. Amino acids Y77, Q86, and R95 in the N-terminal WWE domain, as well as presence of the catalytic domain, are essential for colocalization of PARP11 with the nuclear envelope, but catalytic activity of the protein is not required for colocalization with NUP153. This study demonstrates that PARP11 is a novel enzyme important for proper sperm head shaping and identifies it as a potential factor involved in idiopathic mammalian teratozoospermia.

Original languageEnglish
Article number80
JournalBiology of Reproduction
Volume92
Issue number3
DOIs
Publication statusPublished - 2015 Mar 1

Keywords

  • ADP-ribose
  • ARTD11
  • Acrosome
  • Condensation
  • Gametogenesis
  • Infertility
  • MAR
  • Male infertility
  • Mono(ADP-ribosyl)ation
  • Mouse
  • Nuclear envelope
  • PAR
  • PARG
  • PARP
  • PARP11
  • Poly(ADPribosyl) ation
  • Sperm
  • Sperm differentiation
  • Spermatid
  • Spermatogenesis
  • Spermiogenesis
  • Teratozoospermia
  • Testis
  • Transgenic/knockout model
  • WWE domain

ASJC Scopus subject areas

  • Reproductive Medicine
  • Cell Biology

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