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Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1

In many animals, including vertebrates, oocyte meiotic spindles are bipolar but assemble in the absence of centrosomes. Although meiotic spindle positioning in oocytes has been investigated extensively, much less is known about their assembly. In Caenorhabditis elegans, three genes previously shown...

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Autores principales: Connolly, Amy A., Osterberg, Valerie, Christensen, Sara, Price, Meredith, Lu, Chenggang, Chicas-Cruz, Kathy, Lockery, Shawn, Mains, Paul E., Bowerman, Bruce
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3982995/
https://www.ncbi.nlm.nih.gov/pubmed/24554763
http://dx.doi.org/10.1091/mbc.E13-11-0687
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author Connolly, Amy A.
Osterberg, Valerie
Christensen, Sara
Price, Meredith
Lu, Chenggang
Chicas-Cruz, Kathy
Lockery, Shawn
Mains, Paul E.
Bowerman, Bruce
author_facet Connolly, Amy A.
Osterberg, Valerie
Christensen, Sara
Price, Meredith
Lu, Chenggang
Chicas-Cruz, Kathy
Lockery, Shawn
Mains, Paul E.
Bowerman, Bruce
author_sort Connolly, Amy A.
collection PubMed
description In many animals, including vertebrates, oocyte meiotic spindles are bipolar but assemble in the absence of centrosomes. Although meiotic spindle positioning in oocytes has been investigated extensively, much less is known about their assembly. In Caenorhabditis elegans, three genes previously shown to contribute to oocyte meiotic spindle assembly are the calponin homology domain protein encoded by aspm-1, the katanin family member mei-1, and the kinesin-12 family member klp-18. We isolated temperature-sensitive alleles of all three and investigated their requirements using live-cell imaging to reveal previously undocumented requirements for aspm-1 and mei-1. Our results indicate that bipolar but abnormal oocyte meiotic spindles assemble in aspm-1(-) embryos, whereas klp-18(-) and mei-1(-) mutants assemble monopolar and apolar spindles, respectively. Furthermore, two MEI-1 functions—ASPM-1 recruitment to the spindle and microtubule severing—both contribute to monopolar spindle assembly in klp-18(-) mutants. We conclude that microtubule severing and ASPM-1 both promote meiotic spindle pole assembly in C. elegans oocytes, whereas the kinesin 12 family member KLP-18 promotes spindle bipolarity.
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spelling pubmed-39829952014-06-30 Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1 Connolly, Amy A. Osterberg, Valerie Christensen, Sara Price, Meredith Lu, Chenggang Chicas-Cruz, Kathy Lockery, Shawn Mains, Paul E. Bowerman, Bruce Mol Biol Cell Articles In many animals, including vertebrates, oocyte meiotic spindles are bipolar but assemble in the absence of centrosomes. Although meiotic spindle positioning in oocytes has been investigated extensively, much less is known about their assembly. In Caenorhabditis elegans, three genes previously shown to contribute to oocyte meiotic spindle assembly are the calponin homology domain protein encoded by aspm-1, the katanin family member mei-1, and the kinesin-12 family member klp-18. We isolated temperature-sensitive alleles of all three and investigated their requirements using live-cell imaging to reveal previously undocumented requirements for aspm-1 and mei-1. Our results indicate that bipolar but abnormal oocyte meiotic spindles assemble in aspm-1(-) embryos, whereas klp-18(-) and mei-1(-) mutants assemble monopolar and apolar spindles, respectively. Furthermore, two MEI-1 functions—ASPM-1 recruitment to the spindle and microtubule severing—both contribute to monopolar spindle assembly in klp-18(-) mutants. We conclude that microtubule severing and ASPM-1 both promote meiotic spindle pole assembly in C. elegans oocytes, whereas the kinesin 12 family member KLP-18 promotes spindle bipolarity. The American Society for Cell Biology 2014-04-15 /pmc/articles/PMC3982995/ /pubmed/24554763 http://dx.doi.org/10.1091/mbc.E13-11-0687 Text en © 2014 Connolly et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Connolly, Amy A.
Osterberg, Valerie
Christensen, Sara
Price, Meredith
Lu, Chenggang
Chicas-Cruz, Kathy
Lockery, Shawn
Mains, Paul E.
Bowerman, Bruce
Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title_full Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title_fullStr Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title_full_unstemmed Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title_short Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1
title_sort caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein aspm-1
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3982995/
https://www.ncbi.nlm.nih.gov/pubmed/24554763
http://dx.doi.org/10.1091/mbc.E13-11-0687
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