Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos
During female meiosis, meiotic spindles are positioned at the oocyte cortex to allow expulsion of chromosomes into polar bodies. In C. elegans, kinesin-dependent translocation of the entire spindle to the cortex precedes dynein-dependent rotation of one spindle pole toward the cortex. To elucidate t...
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description | During female meiosis, meiotic spindles are positioned at the oocyte cortex to allow expulsion of chromosomes into polar bodies. In C. elegans, kinesin-dependent translocation of the entire spindle to the cortex precedes dynein-dependent rotation of one spindle pole toward the cortex. To elucidate the role of kinesin-1 in spindle translocation, we examined the localization of kinesin subunits in meiotic embryos. Surprisingly, kinesin-1 was not associated with the spindle and instead was restricted to the cytoplasm in the middle of the embryo. Yolk granules moved on linear tracks, in a kinesin-dependent manner, away from the cortex, resulting in their concentration in the middle of the embryo where the kinesin was concentrated. These results suggest that cytoplasmic microtubules might be arranged with plus ends extending inward, away from the cortex. This microtubule arrangement would not be consistent with direct transport of the meiotic spindle toward the cortex by kinesin-1. In maturing oocytes, the nucleus underwent kinesin-dependent migration to the future site of spindle attachment at the anterior cortex. Thus the spindle translocation defect observed in kinesin-1 mutants may be a result of failed nuclear migration, which places the spindle too far from the cortex for the spindle translocation mechanism to function. |
doi_str_mv | 10.1016/j.ydbio.2009.12.021 |
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In C. elegans, kinesin-dependent translocation of the entire spindle to the cortex precedes dynein-dependent rotation of one spindle pole toward the cortex. To elucidate the role of kinesin-1 in spindle translocation, we examined the localization of kinesin subunits in meiotic embryos. Surprisingly, kinesin-1 was not associated with the spindle and instead was restricted to the cytoplasm in the middle of the embryo. Yolk granules moved on linear tracks, in a kinesin-dependent manner, away from the cortex, resulting in their concentration in the middle of the embryo where the kinesin was concentrated. These results suggest that cytoplasmic microtubules might be arranged with plus ends extending inward, away from the cortex. This microtubule arrangement would not be consistent with direct transport of the meiotic spindle toward the cortex by kinesin-1. In maturing oocytes, the nucleus underwent kinesin-dependent migration to the future site of spindle attachment at the anterior cortex. Thus the spindle translocation defect observed in kinesin-1 mutants may be a result of failed nuclear migration, which places the spindle too far from the cortex for the spindle translocation mechanism to function.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2009.12.021</identifier><identifier>PMID: 20036653</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Animals, Genetically Modified ; C. elegans ; Caenorhabditis elegans - embryology ; Cell Movement ; Cell Nucleus ; Kinesin ; Kinesin - physiology ; Meiosis ; Oocyte ; Oocytes ; RNA Interference ; Yolk Sac</subject><ispartof>Developmental biology, 2010-03, Vol.339 (1), p.126-140</ispartof><rights>2009 Elsevier Inc.</rights><rights>Copyright 2009 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c458t-92268a5d49a47868995209ebcb59719115e5849029267bfbc844678a5c04dbe3</citedby><cites>FETCH-LOGICAL-c458t-92268a5d49a47868995209ebcb59719115e5849029267bfbc844678a5c04dbe3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0012160609014274$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20036653$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McNally, Karen L.</creatorcontrib><creatorcontrib>Martin, Judy L.</creatorcontrib><creatorcontrib>Ellefson, Marina</creatorcontrib><creatorcontrib>McNally, Francis J.</creatorcontrib><title>Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>During female meiosis, meiotic spindles are positioned at the oocyte cortex to allow expulsion of chromosomes into polar bodies. In C. elegans, kinesin-dependent translocation of the entire spindle to the cortex precedes dynein-dependent rotation of one spindle pole toward the cortex. To elucidate the role of kinesin-1 in spindle translocation, we examined the localization of kinesin subunits in meiotic embryos. Surprisingly, kinesin-1 was not associated with the spindle and instead was restricted to the cytoplasm in the middle of the embryo. Yolk granules moved on linear tracks, in a kinesin-dependent manner, away from the cortex, resulting in their concentration in the middle of the embryo where the kinesin was concentrated. These results suggest that cytoplasmic microtubules might be arranged with plus ends extending inward, away from the cortex. This microtubule arrangement would not be consistent with direct transport of the meiotic spindle toward the cortex by kinesin-1. In maturing oocytes, the nucleus underwent kinesin-dependent migration to the future site of spindle attachment at the anterior cortex. Thus the spindle translocation defect observed in kinesin-1 mutants may be a result of failed nuclear migration, which places the spindle too far from the cortex for the spindle translocation mechanism to function.</description><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>C. elegans</subject><subject>Caenorhabditis elegans - embryology</subject><subject>Cell Movement</subject><subject>Cell Nucleus</subject><subject>Kinesin</subject><subject>Kinesin - physiology</subject><subject>Meiosis</subject><subject>Oocyte</subject><subject>Oocytes</subject><subject>RNA Interference</subject><subject>Yolk Sac</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcFu1DAQhiMEokvhCZCQb5wSbCd27ANIqIKCqMSlB26WY8-2XhI72M6i8Aw8dL27pYILp9Fovv-f0fxV9ZLghmDC3-ya1Q4uNBRj2RDaYEoeVRuCJasZ7749rjYYE1oTjvlZ9SylHca4FaJ9Wp0VScs5azfV7y_OQ3K-tjCDt-AzylH7NIeYUYS0jDkh59EcRh3dL7BocjdRZxc8CluUbwH5xYywHKkQzJohIe1taX_qWPCwh-lgW-g1jN9RUftlhCM_gQvZGQTTENeQnldPtnpM8OK-nlfXHz9cX3yqr75efr54f1WbjolcS0q50Mx2Une94EJKRrGEwQxM9kQSwoCJTmIqKe-H7WBE1_G-KAzu7ADtefXuZDsvwwTWlOuiHtUc3aTjqoJ26t-Jd7fqJuwVFbSVXBaD1_cGMfxYIGU1uWRgHLWHsCTVt61g5cW0kO2JNDGkFGH7sIVgdUhR7dQxRXVIURGqSopF9ervAx80f2IrwNsTAOVLewdRJePAG7AugsnKBvffBXctDLNL</recordid><startdate>20100301</startdate><enddate>20100301</enddate><creator>McNally, Karen L.</creator><creator>Martin, Judy L.</creator><creator>Ellefson, Marina</creator><creator>McNally, Francis J.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20100301</creationdate><title>Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos</title><author>McNally, Karen L. ; Martin, Judy L. ; Ellefson, Marina ; McNally, Francis J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c458t-92268a5d49a47868995209ebcb59719115e5849029267bfbc844678a5c04dbe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>C. elegans</topic><topic>Caenorhabditis elegans - embryology</topic><topic>Cell Movement</topic><topic>Cell Nucleus</topic><topic>Kinesin</topic><topic>Kinesin - physiology</topic><topic>Meiosis</topic><topic>Oocyte</topic><topic>Oocytes</topic><topic>RNA Interference</topic><topic>Yolk Sac</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McNally, Karen L.</creatorcontrib><creatorcontrib>Martin, Judy L.</creatorcontrib><creatorcontrib>Ellefson, Marina</creatorcontrib><creatorcontrib>McNally, Francis J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McNally, Karen L.</au><au>Martin, Judy L.</au><au>Ellefson, Marina</au><au>McNally, Francis J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2010-03-01</date><risdate>2010</risdate><volume>339</volume><issue>1</issue><spage>126</spage><epage>140</epage><pages>126-140</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>During female meiosis, meiotic spindles are positioned at the oocyte cortex to allow expulsion of chromosomes into polar bodies. 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subjects | Animals Animals, Genetically Modified C. elegans Caenorhabditis elegans - embryology Cell Movement Cell Nucleus Kinesin Kinesin - physiology Meiosis Oocyte Oocytes RNA Interference Yolk Sac |
title | Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos |
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