Cargando…

Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline

Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in...

Descripción completa

Detalles Bibliográficos
Autores principales: Macaraeg, Jommel, Reinhard, Isaac, Ward, Matthew, Carmeci, Danielle, Stanaway, Madison, Moore, Amy, Hagmann, Ethan, Brown, Katherine, Wynne, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9277076/
https://www.ncbi.nlm.nih.gov/pubmed/35678140
http://dx.doi.org/10.1242/bio.059277
_version_ 1784745872418930688
author Macaraeg, Jommel
Reinhard, Isaac
Ward, Matthew
Carmeci, Danielle
Stanaway, Madison
Moore, Amy
Hagmann, Ethan
Brown, Katherine
Wynne, David J.
author_facet Macaraeg, Jommel
Reinhard, Isaac
Ward, Matthew
Carmeci, Danielle
Stanaway, Madison
Moore, Amy
Hagmann, Ethan
Brown, Katherine
Wynne, David J.
author_sort Macaraeg, Jommel
collection PubMed
description Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in mitotic cells. Here, we generate strains containing new conditional or nonsense mutations in the Caenorhabditis elegans Haspin homologs hasp-1 and hasp-2 and characterize their phenotypes. We show that hasp-1 is responsible for all predicted functions of Haspin and that loss of function of hasp-1 using classical and conditional alleles produces defects in germline stem cell proliferation and spermatogenesis, and confirms its role in oocyte meiosis. Genetic analysis suggests that hasp-1 acts downstream of the Polo-like kinase plk-2 and shows synthetic interactions between hasp-1 and two genes expected to promote recruitment of the CPC by a parallel pathway that depends on the kinase Bub1. This work adds to the growing understanding of Haspin function by characterizing a variety of roles in an intact animal.
format Online
Article
Text
id pubmed-9277076
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-92770762022-07-13 Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline Macaraeg, Jommel Reinhard, Isaac Ward, Matthew Carmeci, Danielle Stanaway, Madison Moore, Amy Hagmann, Ethan Brown, Katherine Wynne, David J. Biol Open Research Article Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in mitotic cells. Here, we generate strains containing new conditional or nonsense mutations in the Caenorhabditis elegans Haspin homologs hasp-1 and hasp-2 and characterize their phenotypes. We show that hasp-1 is responsible for all predicted functions of Haspin and that loss of function of hasp-1 using classical and conditional alleles produces defects in germline stem cell proliferation and spermatogenesis, and confirms its role in oocyte meiosis. Genetic analysis suggests that hasp-1 acts downstream of the Polo-like kinase plk-2 and shows synthetic interactions between hasp-1 and two genes expected to promote recruitment of the CPC by a parallel pathway that depends on the kinase Bub1. This work adds to the growing understanding of Haspin function by characterizing a variety of roles in an intact animal. The Company of Biologists Ltd 2022-07-07 /pmc/articles/PMC9277076/ /pubmed/35678140 http://dx.doi.org/10.1242/bio.059277 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Macaraeg, Jommel
Reinhard, Isaac
Ward, Matthew
Carmeci, Danielle
Stanaway, Madison
Moore, Amy
Hagmann, Ethan
Brown, Katherine
Wynne, David J.
Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_full Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_fullStr Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_full_unstemmed Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_short Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_sort genetic analysis of caenorhabditis elegans haspin-like genes shows that hasp-1 plays multiple roles in the germline
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9277076/
https://www.ncbi.nlm.nih.gov/pubmed/35678140
http://dx.doi.org/10.1242/bio.059277
work_keys_str_mv AT macaraegjommel geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT reinhardisaac geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT wardmatthew geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT carmecidanielle geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT stanawaymadison geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT mooreamy geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT hagmannethan geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT brownkatherine geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline
AT wynnedavidj geneticanalysisofcaenorhabditiseleganshaspinlikegenesshowsthathasp1playsmultiplerolesinthegermline