Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus.
Wolbachia is a bacteria endosymbiont that rapidly infects insect populations through a mechanism known as cytoplasmic incompatibility (CI). In CI, crosses between Wolbachia-infected males and uninfected females produce severe cell cycle defects in the male pronucleus resulting in early embryonic let...
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2009
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oai:doaj.org-article:e5636bb2b5a8438f864bdb77529792ad2021-11-25T05:47:11ZWolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus.1553-73661553-737410.1371/journal.ppat.1000343https://doaj.org/article/e5636bb2b5a8438f864bdb77529792ad2009-03-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19300496/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Wolbachia is a bacteria endosymbiont that rapidly infects insect populations through a mechanism known as cytoplasmic incompatibility (CI). In CI, crosses between Wolbachia-infected males and uninfected females produce severe cell cycle defects in the male pronucleus resulting in early embryonic lethality. In contrast, viable progeny are produced when both parents are infected (the Rescue cross). An important consequence of CI-Rescue is that infected females have a selective advantage over uninfected females facilitating the rapid spread of Wolbachia through insect populations. CI disrupts a number of prophase and metaphase events in the male pronucleus, including Cdk1 activation, chromosome condensation, and segregation. Here, we demonstrate that CI disrupts earlier interphase cell cycle events. Specifically, CI delays the H3.3 and H4 deposition that occurs immediately after protamine removal from the male pronucleus. In addition, we find prolonged retention of the replication factor PCNA in the male pronucleus into metaphase, indicating progression into mitosis with incompletely replicated DNA. We propose that these CI-induced interphase defects in de novo nucleosome assembly and replication are the cause of the observed mitotic condensation and segregation defects. In addition, these interphase chromosome defects likely activate S-phase checkpoints, accounting for the previously described delays in Cdk1 activation. These results have important implications for the mechanism of Rescue and other Wolbachia-induced phenotypes.Frédéric LandmannGuillermo A OrsiBenjamin LoppinWilliam SullivanPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 5, Iss 3, p e1000343 (2009) |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Frédéric Landmann Guillermo A Orsi Benjamin Loppin William Sullivan Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
description |
Wolbachia is a bacteria endosymbiont that rapidly infects insect populations through a mechanism known as cytoplasmic incompatibility (CI). In CI, crosses between Wolbachia-infected males and uninfected females produce severe cell cycle defects in the male pronucleus resulting in early embryonic lethality. In contrast, viable progeny are produced when both parents are infected (the Rescue cross). An important consequence of CI-Rescue is that infected females have a selective advantage over uninfected females facilitating the rapid spread of Wolbachia through insect populations. CI disrupts a number of prophase and metaphase events in the male pronucleus, including Cdk1 activation, chromosome condensation, and segregation. Here, we demonstrate that CI disrupts earlier interphase cell cycle events. Specifically, CI delays the H3.3 and H4 deposition that occurs immediately after protamine removal from the male pronucleus. In addition, we find prolonged retention of the replication factor PCNA in the male pronucleus into metaphase, indicating progression into mitosis with incompletely replicated DNA. We propose that these CI-induced interphase defects in de novo nucleosome assembly and replication are the cause of the observed mitotic condensation and segregation defects. In addition, these interphase chromosome defects likely activate S-phase checkpoints, accounting for the previously described delays in Cdk1 activation. These results have important implications for the mechanism of Rescue and other Wolbachia-induced phenotypes. |
format |
article |
author |
Frédéric Landmann Guillermo A Orsi Benjamin Loppin William Sullivan |
author_facet |
Frédéric Landmann Guillermo A Orsi Benjamin Loppin William Sullivan |
author_sort |
Frédéric Landmann |
title |
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
title_short |
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
title_full |
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
title_fullStr |
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
title_full_unstemmed |
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
title_sort |
wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2009 |
url |
https://doaj.org/article/e5636bb2b5a8438f864bdb77529792ad |
work_keys_str_mv |
AT fredericlandmann wolbachiamediatedcytoplasmicincompatibilityisassociatedwithimpairedhistonedepositioninthemalepronucleus AT guillermoaorsi wolbachiamediatedcytoplasmicincompatibilityisassociatedwithimpairedhistonedepositioninthemalepronucleus AT benjaminloppin wolbachiamediatedcytoplasmicincompatibilityisassociatedwithimpairedhistonedepositioninthemalepronucleus AT williamsullivan wolbachiamediatedcytoplasmicincompatibilityisassociatedwithimpairedhistonedepositioninthemalepronucleus |
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1718414492137684992 |