Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes
The first mitosis of the mammalian embryo must partition the parental genomes contained in two pronuclei. In rodent zygotes, sperm centrosomes are degraded, and instead, acentriolar microtubule organizing centers and microtubule self-organization guide the assembly of two separate spindles around th...
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| Veröffentlicht in: | The Journal of cell biology 2021-11, Vol.220 (11), p.1 |
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| creator | Schneider, Isabell de Ruijter-Villani, Marta Hossain, M Julius Stout, Tom A E Ellenberg, Jan |
| description | The first mitosis of the mammalian embryo must partition the parental genomes contained in two pronuclei. In rodent zygotes, sperm centrosomes are degraded, and instead, acentriolar microtubule organizing centers and microtubule self-organization guide the assembly of two separate spindles around the genomes. In nonrodent mammals, including human or bovine, centrosomes are inherited from the sperm and have been widely assumed to be active. Whether nonrodent zygotes assemble a single centrosomal spindle around both genomes or follow the dual spindle self-assembly pathway is unclear. To address this, we investigated spindle assembly in bovine zygotes by systematic immunofluorescence and real-time light-sheet microscopy. We show that two independent spindles form despite the presence of centrosomes, which had little effect on spindle structure and were only loosely connected to the two spindles. We conclude that the dual spindle assembly pathway is conserved in nonrodent mammals. This could explain whole parental genome loss frequently observed in blastomeres of human IVF embryos. |
| doi_str_mv | 10.1083/jcb.202010106 |
| format | Article |
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In rodent zygotes, sperm centrosomes are degraded, and instead, acentriolar microtubule organizing centers and microtubule self-organization guide the assembly of two separate spindles around the genomes. In nonrodent mammals, including human or bovine, centrosomes are inherited from the sperm and have been widely assumed to be active. Whether nonrodent zygotes assemble a single centrosomal spindle around both genomes or follow the dual spindle self-assembly pathway is unclear. To address this, we investigated spindle assembly in bovine zygotes by systematic immunofluorescence and real-time light-sheet microscopy. We show that two independent spindles form despite the presence of centrosomes, which had little effect on spindle structure and were only loosely connected to the two spindles. We conclude that the dual spindle assembly pathway is conserved in nonrodent mammals. This could explain whole parental genome loss frequently observed in blastomeres of human IVF embryos.</description><identifier>ISSN: 0021-9525</identifier><identifier>ISSN: 1540-8140</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.202010106</identifier><identifier>PMID: 34550316</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Blastomeres ; Cattle ; Cell Cycle and Division ; Centrosome - physiology ; Centrosomes ; Cytoskeleton ; Development ; Embryo, Mammalian - physiology ; Embryos ; Genome - physiology ; Genomes ; Immunofluorescence ; Light sheets ; Male ; Mammals ; Microtubule-Organizing Center - physiology ; Microtubules - physiology ; Mitosis ; Mitosis - physiology ; Self-assembly ; Signal Transduction - physiology ; Sperm ; Spermatozoa - physiology ; Spindle Apparatus - physiology ; Spindles ; Zygote - physiology ; Zygotes</subject><ispartof>The Journal of cell biology, 2021-11, Vol.220 (11), p.1</ispartof><rights>2021 Schneider et al.</rights><rights>Copyright Rockefeller University Press Nov 2021</rights><rights>2021 Schneider et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-9465c046f2fac530b4103f83a501fc2b1c19926164f83a41bbf22438c9034c473</citedby><cites>FETCH-LOGICAL-c481t-9465c046f2fac530b4103f83a501fc2b1c19926164f83a41bbf22438c9034c473</cites><orcidid>0000-0002-0640-3949 ; 0000-0003-3303-5755 ; 0000-0001-5321-8095 ; 0000-0002-6522-9493 ; 0000-0001-5909-701X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34550316$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schneider, Isabell</creatorcontrib><creatorcontrib>de Ruijter-Villani, Marta</creatorcontrib><creatorcontrib>Hossain, M Julius</creatorcontrib><creatorcontrib>Stout, Tom A E</creatorcontrib><creatorcontrib>Ellenberg, Jan</creatorcontrib><title>Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>The first mitosis of the mammalian embryo must partition the parental genomes contained in two pronuclei. In rodent zygotes, sperm centrosomes are degraded, and instead, acentriolar microtubule organizing centers and microtubule self-organization guide the assembly of two separate spindles around the genomes. In nonrodent mammals, including human or bovine, centrosomes are inherited from the sperm and have been widely assumed to be active. Whether nonrodent zygotes assemble a single centrosomal spindle around both genomes or follow the dual spindle self-assembly pathway is unclear. To address this, we investigated spindle assembly in bovine zygotes by systematic immunofluorescence and real-time light-sheet microscopy. We show that two independent spindles form despite the presence of centrosomes, which had little effect on spindle structure and were only loosely connected to the two spindles. We conclude that the dual spindle assembly pathway is conserved in nonrodent mammals. This could explain whole parental genome loss frequently observed in blastomeres of human IVF embryos.</description><subject>Animals</subject><subject>Blastomeres</subject><subject>Cattle</subject><subject>Cell Cycle and Division</subject><subject>Centrosome - physiology</subject><subject>Centrosomes</subject><subject>Cytoskeleton</subject><subject>Development</subject><subject>Embryo, Mammalian - physiology</subject><subject>Embryos</subject><subject>Genome - physiology</subject><subject>Genomes</subject><subject>Immunofluorescence</subject><subject>Light sheets</subject><subject>Male</subject><subject>Mammals</subject><subject>Microtubule-Organizing Center - physiology</subject><subject>Microtubules - physiology</subject><subject>Mitosis</subject><subject>Mitosis - physiology</subject><subject>Self-assembly</subject><subject>Signal Transduction - physiology</subject><subject>Sperm</subject><subject>Spermatozoa - physiology</subject><subject>Spindle Apparatus - physiology</subject><subject>Spindles</subject><subject>Zygote - physiology</subject><subject>Zygotes</subject><issn>0021-9525</issn><issn>1540-8140</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1LxDAQxYMouq4evUrAi5fq5LPtRZD1EwQv7jmk2al2aZvatIL-9WZdXVTmMDDz4zFvHiFHDM4YZOJ86YozDhxYLL1FJkxJSDImYZtMADhLcsXVHtkPYQkAMpVil-wJqRQIpidkfjXamoauahc1BmpDwKaokVYtLfxb1SL9eH_2Q1wtMFID0uEFaddjwNYh9SXt7IB9G0UctkPvg28wHJCd0tYBD7_7lMxvrp9md8nD4-397PIhcTJjQ5JLrRxIXfLSOiWgkAxEmQmrgJWOF8yxPOeaabkaSlYUJedSZC4HIZ1MxZRcrHW7sWhw8XWBrU3XV43t3423lfm7aasX8-zfTKa04FFlSk6_BXr_OmIYTFMFh3VtW_RjMFylSqSp4DyiJ__QpR9XxldULrSWmrNIJWvKxVeEHsvNMQzMKjATAzObwCJ__NvBhv5JSHwCktORIw</recordid><startdate>20211101</startdate><enddate>20211101</enddate><creator>Schneider, Isabell</creator><creator>de Ruijter-Villani, Marta</creator><creator>Hossain, M Julius</creator><creator>Stout, Tom A E</creator><creator>Ellenberg, Jan</creator><general>Rockefeller University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0640-3949</orcidid><orcidid>https://orcid.org/0000-0003-3303-5755</orcidid><orcidid>https://orcid.org/0000-0001-5321-8095</orcidid><orcidid>https://orcid.org/0000-0002-6522-9493</orcidid><orcidid>https://orcid.org/0000-0001-5909-701X</orcidid></search><sort><creationdate>20211101</creationdate><title>Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes</title><author>Schneider, Isabell ; de Ruijter-Villani, Marta ; Hossain, M Julius ; Stout, Tom A E ; Ellenberg, Jan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-9465c046f2fac530b4103f83a501fc2b1c19926164f83a41bbf22438c9034c473</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Blastomeres</topic><topic>Cattle</topic><topic>Cell Cycle and Division</topic><topic>Centrosome - physiology</topic><topic>Centrosomes</topic><topic>Cytoskeleton</topic><topic>Development</topic><topic>Embryo, Mammalian - physiology</topic><topic>Embryos</topic><topic>Genome - physiology</topic><topic>Genomes</topic><topic>Immunofluorescence</topic><topic>Light sheets</topic><topic>Male</topic><topic>Mammals</topic><topic>Microtubule-Organizing Center - physiology</topic><topic>Microtubules - physiology</topic><topic>Mitosis</topic><topic>Mitosis - physiology</topic><topic>Self-assembly</topic><topic>Signal Transduction - physiology</topic><topic>Sperm</topic><topic>Spermatozoa - physiology</topic><topic>Spindle Apparatus - physiology</topic><topic>Spindles</topic><topic>Zygote - physiology</topic><topic>Zygotes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schneider, Isabell</creatorcontrib><creatorcontrib>de Ruijter-Villani, Marta</creatorcontrib><creatorcontrib>Hossain, M Julius</creatorcontrib><creatorcontrib>Stout, Tom A E</creatorcontrib><creatorcontrib>Ellenberg, Jan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schneider, Isabell</au><au>de Ruijter-Villani, Marta</au><au>Hossain, M Julius</au><au>Stout, Tom A E</au><au>Ellenberg, Jan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>220</volume><issue>11</issue><spage>1</spage><pages>1-</pages><issn>0021-9525</issn><issn>1540-8140</issn><eissn>1540-8140</eissn><abstract>The first mitosis of the mammalian embryo must partition the parental genomes contained in two pronuclei. In rodent zygotes, sperm centrosomes are degraded, and instead, acentriolar microtubule organizing centers and microtubule self-organization guide the assembly of two separate spindles around the genomes. In nonrodent mammals, including human or bovine, centrosomes are inherited from the sperm and have been widely assumed to be active. Whether nonrodent zygotes assemble a single centrosomal spindle around both genomes or follow the dual spindle self-assembly pathway is unclear. To address this, we investigated spindle assembly in bovine zygotes by systematic immunofluorescence and real-time light-sheet microscopy. We show that two independent spindles form despite the presence of centrosomes, which had little effect on spindle structure and were only loosely connected to the two spindles. We conclude that the dual spindle assembly pathway is conserved in nonrodent mammals. 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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Animals Blastomeres Cattle Cell Cycle and Division Centrosome - physiology Centrosomes Cytoskeleton Development Embryo, Mammalian - physiology Embryos Genome - physiology Genomes Immunofluorescence Light sheets Male Mammals Microtubule-Organizing Center - physiology Microtubules - physiology Mitosis Mitosis - physiology Self-assembly Signal Transduction - physiology Sperm Spermatozoa - physiology Spindle Apparatus - physiology Spindles Zygote - physiology Zygotes |
| title | Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes |
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