Early development of Drosophila embryos requires Smc5/6 function during oogenesis

Mutations in structural maintenance of chromosomes (Smc) proteins are frequently associated with chromosomal abnormalities commonly observed in developmental disorders. However, the role of Smc proteins in development still remains elusive. To investigate Smc5/6 function during early embryogenesis w...

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Main Authors: Martin Tran, Vasilios Tsarouhas, Andreas Kegel
Format: Article
Language:English
Published: The Company of Biologists 2016-07-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/5/7/928
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author Martin Tran
Vasilios Tsarouhas
Andreas Kegel
author_facet Martin Tran
Vasilios Tsarouhas
Andreas Kegel
author_sort Martin Tran
collection DOAJ
description Mutations in structural maintenance of chromosomes (Smc) proteins are frequently associated with chromosomal abnormalities commonly observed in developmental disorders. However, the role of Smc proteins in development still remains elusive. To investigate Smc5/6 function during early embryogenesis we examined smc5 and smc6 mutants of the fruit fly Drosophila melanogaster using a combination of reverse genetics and microscopy approaches. Smc5/6 exhibited a maternally contributed function in maintaining chromosome stability during early embryo development, which manifested as female subfertility in its absence. Loss of Smc5/6 caused an arrest and a considerable delay in embryo development accompanied by fragmented nuclei and increased anaphase-bridge formation, respectively. Surprisingly, early embryonic arrest was attributable to the absence of Smc5/6 during oogenesis, which resulted in insufficient repair of pre-meiotic and meiotic DNA double-strand breaks. Thus, our findings contribute to the understanding of Smc proteins in higher eukaryotic development by highlighting a maternal function in chromosome maintenance and a link between oogenesis and early embryogenesis.
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spelling doaj.art-d098fbaa6d034cbb8c1a49037b71d6ec2022-12-21T22:44:15ZengThe Company of BiologistsBiology Open2046-63902016-07-015792894110.1242/bio.019000019000Early development of Drosophila embryos requires Smc5/6 function during oogenesisMartin Tran0Vasilios Tsarouhas1Andreas Kegel2 Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm S-17177, Sweden Department of Molecular Bioscience, The Wenner-Gren Institute, Stockholm University, Stockholm S-10691, Sweden Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm S-17177, Sweden Mutations in structural maintenance of chromosomes (Smc) proteins are frequently associated with chromosomal abnormalities commonly observed in developmental disorders. However, the role of Smc proteins in development still remains elusive. To investigate Smc5/6 function during early embryogenesis we examined smc5 and smc6 mutants of the fruit fly Drosophila melanogaster using a combination of reverse genetics and microscopy approaches. Smc5/6 exhibited a maternally contributed function in maintaining chromosome stability during early embryo development, which manifested as female subfertility in its absence. Loss of Smc5/6 caused an arrest and a considerable delay in embryo development accompanied by fragmented nuclei and increased anaphase-bridge formation, respectively. Surprisingly, early embryonic arrest was attributable to the absence of Smc5/6 during oogenesis, which resulted in insufficient repair of pre-meiotic and meiotic DNA double-strand breaks. Thus, our findings contribute to the understanding of Smc proteins in higher eukaryotic development by highlighting a maternal function in chromosome maintenance and a link between oogenesis and early embryogenesis.http://bio.biologists.org/content/5/7/928Smc proteinsDNA DSBsChromosomesAnaphase bridgesPachytene arrestKaryosome
spellingShingle Martin Tran
Vasilios Tsarouhas
Andreas Kegel
Early development of Drosophila embryos requires Smc5/6 function during oogenesis
Biology Open
Smc proteins
DNA DSBs
Chromosomes
Anaphase bridges
Pachytene arrest
Karyosome
title Early development of Drosophila embryos requires Smc5/6 function during oogenesis
title_full Early development of Drosophila embryos requires Smc5/6 function during oogenesis
title_fullStr Early development of Drosophila embryos requires Smc5/6 function during oogenesis
title_full_unstemmed Early development of Drosophila embryos requires Smc5/6 function during oogenesis
title_short Early development of Drosophila embryos requires Smc5/6 function during oogenesis
title_sort early development of drosophila embryos requires smc5 6 function during oogenesis
topic Smc proteins
DNA DSBs
Chromosomes
Anaphase bridges
Pachytene arrest
Karyosome
url http://bio.biologists.org/content/5/7/928
work_keys_str_mv AT martintran earlydevelopmentofdrosophilaembryosrequiressmc56functionduringoogenesis
AT vasiliostsarouhas earlydevelopmentofdrosophilaembryosrequiressmc56functionduringoogenesis
AT andreaskegel earlydevelopmentofdrosophilaembryosrequiressmc56functionduringoogenesis