title: Meiotic HORMA domain proteins prevent untimely centriole disengagement during Caenorhabditis elegans spermatocyte meiosis.
abstract: In many species where oocytes lack centrosomes, sperm contribute both genetic material and centriole(s) to the zygote. Correct centriole organization during male meiosis is critical to guarantee a normal bipolar mitotic spindle in the zygote. During Caenorhabditis elegans male meiosis, centrioles normally undergo two rounds of duplication, resulting in haploid sperm each containing a single tightly engaged centriole pair. Here we identify an unanticipated role for C. elegans HORMA (Hop1/Rev7/Mad2) domain proteins HTP-1/2 and HIM-3 in regulating centriole disengagement during spermatocyte meiosis. In him-3 and htp-1 htp-2 mutants, centrioles separate inappropriately during meiosis II, resulting in spermatids with disengaged centrioles. Moreover, extra centrosomes are detected in a subset of zygotes. Together, these data implicate HIM-3 and HTP-1/2 in preventing centriole disengagement during meiosis II. We showed previously that HTP-1/2 prevents premature loss of sister chromatid cohesion during the meiotic divisions by inhibiting removal of meiotic cohesin complexes containing the REC-8 subunit. Worms lacking REC-8, or expressing a mutant separase protein with elevated local concentration at centrosomes and in sperm, likewise exhibit inappropriate centriole separation during spermatocyte meiosis. These observations are consistent with HIM-3 and HTP-1/2 preventing centriole disengagement by inhibiting separase-dependent cohesin removal. Our data suggest that the same specialized meiotic mechanisms that function to prevent premature release of sister chromatid cohesion during meiosis I in C. elegans also function to inhibit centriole separation at meiosis II, thereby ensuring that the zygote inherits the appropriate complement of chromosomes and centrioles.
authors: Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA. maras1@stanford.edu
authors: Mara
authors: M
authors: Schvarzstein
authors: Divya
authors: D
authors: Pattabiraman
authors: Joshua N
authors: JN
authors: Bembenek
authors: Anne M
authors: AM
authors: Villeneuve
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology* / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000502:physiology*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000502:physiology; D002502:Centrioles / Q000502:physiology; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics / Q000502:physiology; D005260:Female; D017238:Genes, Helminth; D008297:Male; D008540:Meiosis / Q000235:genetics / Q000502:physiology; D008954:Models, Biological; D009154:Mutation; D064247:Separase; D013090:Spermatocytes / Q000166:cytology* / Q000502:physiology*; D013091:Spermatogenesis / Q000235:genetics / Q000502:physiology; D000097722:Cohesins
chemical_list: D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; D002868:Chromosomal Proteins, Non-Histone; D064247:Separase; D000097722:Cohesins; C121599:HIM-3 protein, C elegans; C506262:Htp-1 protein, C elegans; C577988:SEP-1 protein, C elegans
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