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Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females

Using an antibody against the phosphorylated form of His2Av (γ-His2Av), we have described the time course for the series of events leading from the formation of a double-strand break (DSB) to a crossover in Drosophila female meiotic prophase. MEI-P22 is required for DSB formation and localizes to ch...

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Autores principales: Mehrotra, S, McKim, K. S
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2006
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1657055/
https://www.ncbi.nlm.nih.gov/pubmed/17166055
http://dx.doi.org/10.1371/journal.pgen.0020200
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author Mehrotra, S
McKim, K. S
author_facet Mehrotra, S
McKim, K. S
author_sort Mehrotra, S
collection PubMed
description Using an antibody against the phosphorylated form of His2Av (γ-His2Av), we have described the time course for the series of events leading from the formation of a double-strand break (DSB) to a crossover in Drosophila female meiotic prophase. MEI-P22 is required for DSB formation and localizes to chromosomes prior to γ-His2Av foci. Drosophila females, however, are among the group of organisms where synaptonemal complex (SC) formation is not dependent on DSBs. In the absence of two SC proteins, C(3)G and C(2)M, the number of DSBs in oocytes is significantly reduced. This is consistent with the appearance of SC protein staining prior to γ-His2Av foci. However, SC formation is incomplete or absent in the neighboring nurse cells, and γ-His2Av foci appear with the same kinetics as in oocytes and do not depend on SC proteins. Thus, competence for DSB formation in nurse cells occurs with a specific timing that is independent of the SC, whereas in the oocytes, some SC proteins may have a regulatory role to counteract the effects of a negative regulator of DSB formation. The SC is not sufficient for DSB formation, however, since DSBs were absent from the heterochromatin even though SC formation occurs in these regions. All γ-His2Av foci disappear before the end of prophase, presumably as repair is completed and crossovers are formed. However, oocytes in early prophase exhibit a slower response to X-ray–induced DSBs compared to those in the late pachytene stage. Assuming all DSBs appear as γ-His2Av foci, there is at least a 3:1 ratio of noncrossover to crossover products. From a comparison of the frequency of γ-His2Av foci and crossovers, it appears that Drosophila females have only a weak mechanism to ensure a crossover in the presence of a low number of DSBs.
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spelling pubmed-16570552006-11-29 Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females Mehrotra, S McKim, K. S PLoS Genet Research Article Using an antibody against the phosphorylated form of His2Av (γ-His2Av), we have described the time course for the series of events leading from the formation of a double-strand break (DSB) to a crossover in Drosophila female meiotic prophase. MEI-P22 is required for DSB formation and localizes to chromosomes prior to γ-His2Av foci. Drosophila females, however, are among the group of organisms where synaptonemal complex (SC) formation is not dependent on DSBs. In the absence of two SC proteins, C(3)G and C(2)M, the number of DSBs in oocytes is significantly reduced. This is consistent with the appearance of SC protein staining prior to γ-His2Av foci. However, SC formation is incomplete or absent in the neighboring nurse cells, and γ-His2Av foci appear with the same kinetics as in oocytes and do not depend on SC proteins. Thus, competence for DSB formation in nurse cells occurs with a specific timing that is independent of the SC, whereas in the oocytes, some SC proteins may have a regulatory role to counteract the effects of a negative regulator of DSB formation. The SC is not sufficient for DSB formation, however, since DSBs were absent from the heterochromatin even though SC formation occurs in these regions. All γ-His2Av foci disappear before the end of prophase, presumably as repair is completed and crossovers are formed. However, oocytes in early prophase exhibit a slower response to X-ray–induced DSBs compared to those in the late pachytene stage. Assuming all DSBs appear as γ-His2Av foci, there is at least a 3:1 ratio of noncrossover to crossover products. From a comparison of the frequency of γ-His2Av foci and crossovers, it appears that Drosophila females have only a weak mechanism to ensure a crossover in the presence of a low number of DSBs. Public Library of Science 2006-11 2006-11-24 /pmc/articles/PMC1657055/ /pubmed/17166055 http://dx.doi.org/10.1371/journal.pgen.0020200 Text en © 2006 Mehrotra and McKim. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Mehrotra, S
McKim, K. S
Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title_full Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title_fullStr Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title_full_unstemmed Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title_short Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females
title_sort temporal analysis of meiotic dna double-strand break formation and repair in drosophila females
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1657055/
https://www.ncbi.nlm.nih.gov/pubmed/17166055
http://dx.doi.org/10.1371/journal.pgen.0020200
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