Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics
Natural populations of the house mouse Mus musculus domesticus show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile...
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| Veröffentlicht in: | Chromosoma 2019-06, Vol.128 (2), p.149-163 |
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| creator | Ribagorda, Marta Berríos, Soledad Solano, Emanuela Ayarza, Eliana Martín-Ruiz, Marta Gil-Fernández, Ana Parra, María Teresa Viera, Alberto Rufas, Julio S. Capanna, Ernesto Castiglia, Riccardo Fernández-Donoso, Raúl Page, Jesús |
| description | Natural populations of the house mouse
Mus musculus domesticus
show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile hybrid individuals due to impaired meiotic development. In this study, we have analyzed prophase-I spermatocytes of hybrids formed by crossing mice from Vulcano and Lipari island populations. Both populations have a 2n = 26 karyotype but different combinations of Robertsonian translocations. We studied the progress of synapsis, recombination, and meiotic silencing of unsynapsed chromosomes during prophase-I through the immunolocalization of the proteins SYCP3, SYCP1, γH2AX, RAD51, and MLH1. In these hybrids, a hexavalent is formed that, depending on the degree of synapsis between chromosomes, can adopt an open chain, a ring, or a closed configuration. The frequency of these configurations varies throughout meiosis, with the maximum degree of synapsis occurring at mid pachytene. In addition, we observed the appearance of heterologous synapsis between telocentric and metacentric chromosomes; however, this synapsis seems to be transient and unstable and unsynapsed regions are frequently observed in mid-late pachytene. Interestingly, we found that chiasmata are frequently located at the boundaries of unsynapsed chromosomal regions in the hexavalent during late pachytene. These results provide new clues about synapsis dynamics during meiosis. We propose that mechanical forces generated along chromosomes may induce premature desynapsis, which, in turn, might be counteracted by the location of chiasmata. Despite these and additional meiotic features, such as the accumulation of γH2AX on unsynapsed chromosome regions, we observed a large number of cells that progressed to late stages of prophase-I, indicating that synapsis defects may not trigger a meiotic crisis in these hybrids. |
| doi_str_mv | 10.1007/s00412-019-00695-8 |
| format | Article |
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Mus musculus domesticus
show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile hybrid individuals due to impaired meiotic development. In this study, we have analyzed prophase-I spermatocytes of hybrids formed by crossing mice from Vulcano and Lipari island populations. Both populations have a 2n = 26 karyotype but different combinations of Robertsonian translocations. We studied the progress of synapsis, recombination, and meiotic silencing of unsynapsed chromosomes during prophase-I through the immunolocalization of the proteins SYCP3, SYCP1, γH2AX, RAD51, and MLH1. In these hybrids, a hexavalent is formed that, depending on the degree of synapsis between chromosomes, can adopt an open chain, a ring, or a closed configuration. The frequency of these configurations varies throughout meiosis, with the maximum degree of synapsis occurring at mid pachytene. In addition, we observed the appearance of heterologous synapsis between telocentric and metacentric chromosomes; however, this synapsis seems to be transient and unstable and unsynapsed regions are frequently observed in mid-late pachytene. Interestingly, we found that chiasmata are frequently located at the boundaries of unsynapsed chromosomal regions in the hexavalent during late pachytene. These results provide new clues about synapsis dynamics during meiosis. We propose that mechanical forces generated along chromosomes may induce premature desynapsis, which, in turn, might be counteracted by the location of chiasmata. Despite these and additional meiotic features, such as the accumulation of γH2AX on unsynapsed chromosome regions, we observed a large number of cells that progressed to late stages of prophase-I, indicating that synapsis defects may not trigger a meiotic crisis in these hybrids.</description><identifier>ISSN: 0009-5915</identifier><identifier>EISSN: 1432-0886</identifier><identifier>DOI: 10.1007/s00412-019-00695-8</identifier><identifier>PMID: 30826871</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Animal Genetics and Genomics ; Animals ; Biochemistry ; Biomedical and Life Sciences ; Cell Biology ; Chromosome Pairing ; Chromosome rearrangements ; Chromosome translocations ; Chromosomes ; Developmental Biology ; Eukaryotic Microbiology ; Female ; Heterozygote ; Human Genetics ; Hybrids ; Karyotype ; Life Sciences ; Male ; Meiosis ; Meiotic Prophase I ; Mice - genetics ; MLH1 protein ; Original Article ; Pachytene ; Prophase ; Recombination ; Spermatocytes ; Spermatocytes - cytology ; Translocation, Genetic</subject><ispartof>Chromosoma, 2019-06, Vol.128 (2), p.149-163</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2019</rights><rights>Chromosoma is a copyright of Springer, (2019). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-f55a85845930ef933bf52358b76339ac3409f3ccaf2ea8c75363653606927e1c3</citedby><cites>FETCH-LOGICAL-c375t-f55a85845930ef933bf52358b76339ac3409f3ccaf2ea8c75363653606927e1c3</cites><orcidid>0000-0001-8381-324X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00412-019-00695-8$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00412-019-00695-8$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,781,785,27929,27930,41493,42562,51324</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30826871$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ribagorda, Marta</creatorcontrib><creatorcontrib>Berríos, Soledad</creatorcontrib><creatorcontrib>Solano, Emanuela</creatorcontrib><creatorcontrib>Ayarza, Eliana</creatorcontrib><creatorcontrib>Martín-Ruiz, Marta</creatorcontrib><creatorcontrib>Gil-Fernández, Ana</creatorcontrib><creatorcontrib>Parra, María Teresa</creatorcontrib><creatorcontrib>Viera, Alberto</creatorcontrib><creatorcontrib>Rufas, Julio S.</creatorcontrib><creatorcontrib>Capanna, Ernesto</creatorcontrib><creatorcontrib>Castiglia, Riccardo</creatorcontrib><creatorcontrib>Fernández-Donoso, Raúl</creatorcontrib><creatorcontrib>Page, Jesús</creatorcontrib><title>Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics</title><title>Chromosoma</title><addtitle>Chromosoma</addtitle><addtitle>Chromosoma</addtitle><description>Natural populations of the house mouse
Mus musculus domesticus
show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile hybrid individuals due to impaired meiotic development. In this study, we have analyzed prophase-I spermatocytes of hybrids formed by crossing mice from Vulcano and Lipari island populations. Both populations have a 2n = 26 karyotype but different combinations of Robertsonian translocations. We studied the progress of synapsis, recombination, and meiotic silencing of unsynapsed chromosomes during prophase-I through the immunolocalization of the proteins SYCP3, SYCP1, γH2AX, RAD51, and MLH1. In these hybrids, a hexavalent is formed that, depending on the degree of synapsis between chromosomes, can adopt an open chain, a ring, or a closed configuration. The frequency of these configurations varies throughout meiosis, with the maximum degree of synapsis occurring at mid pachytene. In addition, we observed the appearance of heterologous synapsis between telocentric and metacentric chromosomes; however, this synapsis seems to be transient and unstable and unsynapsed regions are frequently observed in mid-late pachytene. Interestingly, we found that chiasmata are frequently located at the boundaries of unsynapsed chromosomal regions in the hexavalent during late pachytene. These results provide new clues about synapsis dynamics during meiosis. We propose that mechanical forces generated along chromosomes may induce premature desynapsis, which, in turn, might be counteracted by the location of chiasmata. Despite these and additional meiotic features, such as the accumulation of γH2AX on unsynapsed chromosome regions, we observed a large number of cells that progressed to late stages of prophase-I, indicating that synapsis defects may not trigger a meiotic crisis in these hybrids.</description><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Cell Biology</subject><subject>Chromosome Pairing</subject><subject>Chromosome rearrangements</subject><subject>Chromosome translocations</subject><subject>Chromosomes</subject><subject>Developmental Biology</subject><subject>Eukaryotic Microbiology</subject><subject>Female</subject><subject>Heterozygote</subject><subject>Human Genetics</subject><subject>Hybrids</subject><subject>Karyotype</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Meiosis</subject><subject>Meiotic Prophase I</subject><subject>Mice - genetics</subject><subject>MLH1 protein</subject><subject>Original Article</subject><subject>Pachytene</subject><subject>Prophase</subject><subject>Recombination</subject><subject>Spermatocytes</subject><subject>Spermatocytes - 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genetics</topic><topic>MLH1 protein</topic><topic>Original Article</topic><topic>Pachytene</topic><topic>Prophase</topic><topic>Recombination</topic><topic>Spermatocytes</topic><topic>Spermatocytes - cytology</topic><topic>Translocation, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ribagorda, Marta</creatorcontrib><creatorcontrib>Berríos, Soledad</creatorcontrib><creatorcontrib>Solano, Emanuela</creatorcontrib><creatorcontrib>Ayarza, Eliana</creatorcontrib><creatorcontrib>Martín-Ruiz, Marta</creatorcontrib><creatorcontrib>Gil-Fernández, Ana</creatorcontrib><creatorcontrib>Parra, María Teresa</creatorcontrib><creatorcontrib>Viera, Alberto</creatorcontrib><creatorcontrib>Rufas, Julio S.</creatorcontrib><creatorcontrib>Capanna, Ernesto</creatorcontrib><creatorcontrib>Castiglia, Riccardo</creatorcontrib><creatorcontrib>Fernández-Donoso, Raúl</creatorcontrib><creatorcontrib>Page, Jesús</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Chromosoma</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ribagorda, Marta</au><au>Berríos, Soledad</au><au>Solano, Emanuela</au><au>Ayarza, Eliana</au><au>Martín-Ruiz, Marta</au><au>Gil-Fernández, Ana</au><au>Parra, María Teresa</au><au>Viera, Alberto</au><au>Rufas, Julio S.</au><au>Capanna, Ernesto</au><au>Castiglia, Riccardo</au><au>Fernández-Donoso, Raúl</au><au>Page, Jesús</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics</atitle><jtitle>Chromosoma</jtitle><stitle>Chromosoma</stitle><addtitle>Chromosoma</addtitle><date>2019-06-01</date><risdate>2019</risdate><volume>128</volume><issue>2</issue><spage>149</spage><epage>163</epage><pages>149-163</pages><issn>0009-5915</issn><eissn>1432-0886</eissn><abstract>Natural populations of the house mouse
Mus musculus domesticus
show great diversity in chromosomal number due to the presence of chromosomal rearrangements, mainly Robertsonian translocations. Breeding between two populations with different chromosomal configurations generates subfertile or sterile hybrid individuals due to impaired meiotic development. In this study, we have analyzed prophase-I spermatocytes of hybrids formed by crossing mice from Vulcano and Lipari island populations. Both populations have a 2n = 26 karyotype but different combinations of Robertsonian translocations. We studied the progress of synapsis, recombination, and meiotic silencing of unsynapsed chromosomes during prophase-I through the immunolocalization of the proteins SYCP3, SYCP1, γH2AX, RAD51, and MLH1. In these hybrids, a hexavalent is formed that, depending on the degree of synapsis between chromosomes, can adopt an open chain, a ring, or a closed configuration. The frequency of these configurations varies throughout meiosis, with the maximum degree of synapsis occurring at mid pachytene. In addition, we observed the appearance of heterologous synapsis between telocentric and metacentric chromosomes; however, this synapsis seems to be transient and unstable and unsynapsed regions are frequently observed in mid-late pachytene. Interestingly, we found that chiasmata are frequently located at the boundaries of unsynapsed chromosomal regions in the hexavalent during late pachytene. These results provide new clues about synapsis dynamics during meiosis. We propose that mechanical forces generated along chromosomes may induce premature desynapsis, which, in turn, might be counteracted by the location of chiasmata. Despite these and additional meiotic features, such as the accumulation of γH2AX on unsynapsed chromosome regions, we observed a large number of cells that progressed to late stages of prophase-I, indicating that synapsis defects may not trigger a meiotic crisis in these hybrids.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>30826871</pmid><doi>10.1007/s00412-019-00695-8</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-8381-324X</orcidid></addata></record> |
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| ispartof | Chromosoma, 2019-06, Vol.128 (2), p.149-163 |
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| language | eng |
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| source | MEDLINE; SpringerNature Journals |
| subjects | Animal Genetics and Genomics Animals Biochemistry Biomedical and Life Sciences Cell Biology Chromosome Pairing Chromosome rearrangements Chromosome translocations Chromosomes Developmental Biology Eukaryotic Microbiology Female Heterozygote Human Genetics Hybrids Karyotype Life Sciences Male Meiosis Meiotic Prophase I Mice - genetics MLH1 protein Original Article Pachytene Prophase Recombination Spermatocytes Spermatocytes - cytology Translocation, Genetic |
| title | Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics |
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