Measuring Mitotic Spindle and Microtubule Dynamics in Marine Embryos and Non-model Organisms.

Confocal live imaging Histone purification Marine embryos Microtubule dynamics Mitotic spindle Non-model organisms Tubulin labelling

Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2024
Historique:
medline: 23 2 2024
pubmed: 23 2 2024
entrez: 23 2 2024
Statut: ppublish

Résumé

During eukaryotic cell division a microtubule-based structure, the mitotic spindle, aligns and segregates chromosomes between daughter cells. Understanding how this cellular structure is assembled and coordinated in space and in time requires measuring microtubule dynamics and visualizing spindle assembly with high temporal and spatial resolution. Visualization is often achieved by the introduction and the detection of molecular probes and fluorescence microscopy. Microtubules and mitotic spindles are highly conserved across eukaryotes; however, several technical limitations have restricted these investigations to only a few species. The ability to monitor microtubule and chromosome choreography in a wide range of species is fundamental to reveal conserved mechanisms or unravel unconventional strategies that certain forms of life have developed to ensure faithful partitioning of chromosomes during cell division. Here, we describe a technique based on injection of purified proteins that enables the visualization of microtubules and chromosomes with a high contrast in several divergent marine embryos. We also provide analysis methods and tools to extract microtubule dynamics and monitor spindle assembly. These techniques can be adapted to a wide variety of species in order to measure microtubule dynamics and spindle assembly kinetics when genetic tools are not available or in parallel to the development of such techniques in non-model organisms.

Identifiants

pubmed: 38393477
doi: 10.1007/978-1-0716-3557-5_12
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

187-210

Informations de copyright

© 2024. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242
doi: 10.1038/312237a0 pubmed: 6504138
Walker RA, O’Brien ET, Pryer NK et al (1988) Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol 107:1437–1448
doi: 10.1083/jcb.107.4.1437 pubmed: 3170635
Shelden E, Wadsworth P (1993) Observation and quantification of individual microtubule behavior in vivo: microtubule dynamics are cell-type specific. J Cell Biol 120:935–945
doi: 10.1083/jcb.120.4.935 pubmed: 8432733
Zwetsloot AJ, Tut G, Straube A (2018) Measuring microtubule dynamics. Essays Biochem 62:725–735. https://doi.org/10.1042/EBC20180035
doi: 10.1042/EBC20180035 pubmed: 30287587 pmcid: 6281472
Verde F, Dogterom M, Stelzer E et al (1992) Control of microtubule dynamics and length by cyclin A- and cyclin B-dependent kinases in Xenopus egg extracts. J Cell Biol 118:1097–1108
doi: 10.1083/jcb.118.5.1097 pubmed: 1387400
Minden JS, Agard DA, Sedat JW, Alberts BM (1989) Direct cell lineage analysis in Drosophila melanogaster by time-lapse, three-dimensional optical microscopy of living embryos. J Cell Biol 109:505–516. https://doi.org/10.1083/jcb.109.2.505
doi: 10.1083/jcb.109.2.505 pubmed: 2503522
Kellogg DR, Mitchison TJ, Alberts BM (1988) Behaviour of microtubules and actin filaments in living Drosophila embryos. Development 103:675–686. https://doi.org/10.1242/dev.103.4.675
doi: 10.1242/dev.103.4.675 pubmed: 3248521
Wadsworth P, Sloboda RD (1983) Microinjection of fluorescent tubulin into dividing sea urchin cells. J Cell Biol 97:1249–1254. https://doi.org/10.1083/jcb.97.4.1249
doi: 10.1083/jcb.97.4.1249 pubmed: 6684663
Hamaguchi Y, Toriyama M, Sakai H, Hiramoto Y (1985) Distribution of fluorescently labeled tubulin injected into sand dollar eggs from fertilization through cleavage. J Cell Biol 100:1262–1272. https://doi.org/10.1083/jcb.100.4.1262
doi: 10.1083/jcb.100.4.1262 pubmed: 3920225
Salmon ED, Leslie RJ, Saxton WM et al (1984) Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J Cell Biol 99:2165–2174. https://doi.org/10.1083/jcb.99.6.2165
doi: 10.1083/jcb.99.6.2165 pubmed: 6501418
Castoldi M, Popov AV (2003) Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr Purif 32:83–88. https://doi.org/10.1016/S1046-5928(03)00218-3
doi: 10.1016/S1046-5928(03)00218-3 pubmed: 14680943
Hyman AA (1991) Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence. J Cell Sci Suppl 14:125–127
doi: 10.1242/jcs.1991.Supplement_14.25 pubmed: 1832165
Prodon F, Chenevert J, Hébras C et al (2010) Dual mechanism controls asymmetric spindle position in ascidian germ cell precursors. Development 137:2011–2021. https://doi.org/10.1242/dev.047845
doi: 10.1242/dev.047845 pubmed: 20463032
Lacroix B, Letort G, Pitayu L et al (2018) Microtubule dynamics scale with cell size to set spindle length and assembly timing. Dev Cell 45:496–511 e6. https://doi.org/10.1016/j.devcel.2018.04.022
Yasuo H, McDougall A (2018) Practical guide for ascidian microinjection: phallusia mammillata. Adv Exp Med Biol 1029:15–24. https://doi.org/10.1007/978-981-10-7545-2_3
doi: 10.1007/978-981-10-7545-2_3 pubmed: 29542077
Lacroix B, Bourdages KG, Dorn JF et al (2014) In situ imaging in C. elegans reveals developmental regulation of microtubule dynamics. Dev Cell 29:203–216. https://doi.org/10.1016/j.devcel.2014.03.007
doi: 10.1016/j.devcel.2014.03.007 pubmed: 24780738 pmcid: 4062621
Lacroix B, Maddox AS (2014) Microtubule dynamics followed through cell differentiation and tissue biogenesis in C. elegans. Worm 3:e967611. https://doi.org/10.4161/21624046.2014.967611
doi: 10.4161/21624046.2014.967611 pubmed: 26430551 pmcid: 4588219
Jaffe LA, Terasaki M (2004) Quantitative microinjection of oocytes, eggs, and embryos. Methods Cell Biol 74:219–242
doi: 10.1016/S0091-679X(04)74010-8 pubmed: 15575609 pmcid: 1945233
Belmont LD, Hyman AA, Sawin KE, Mitchison TJ (1990) Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62:579–589
doi: 10.1016/0092-8674(90)90022-7 pubmed: 2379239
Verde F, Labbe JC, Doree M, Karsenti E (1990) Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343:233–238. https://doi.org/10.1038/343233a0
doi: 10.1038/343233a0 pubmed: 2405278
Mitchison TJ, Ishihara K, Nguyen P, Wuhr M (2015) Size scaling of microtubule assemblies in early xenopus embryos. Cold Spring Harb Perspect Biol 7:a019182. https://doi.org/10.1101/cshperspect.a019182
doi: 10.1101/cshperspect.a019182 pubmed: 26261283 pmcid: 4588060
Rieckhoff EM, Berndt F, Elsner M et al (2020) Spindle scaling is governed by cell boundary regulation of microtubule nucleation. Curr Biol 30:4973–4983.e10. https://doi.org/10.1016/j.cub.2020.10.093
Srayko M, Kaya A, Stamford J, Hyman AA (2005) Identification and characterization of factors required for microtubule growth and nucleation in the early C. elegans embryo. Dev Cell 9:223–236. https://doi.org/10.1016/j.devcel.2005.07.003
doi: 10.1016/j.devcel.2005.07.003 pubmed: 16054029
Li G, Moore JK (2020) Microtubule dynamics at low temperature: evidence that tubulin recycling limits assembly. Mol Biol Cell 31:1154–1166. https://doi.org/10.1091/mbc.E19-11-0634
doi: 10.1091/mbc.E19-11-0634 pubmed: 32213119 pmcid: 7353160

Auteurs

Janet Chenevert (J)

Sorbonne Universités, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Villefranche-sur-mer, France.

Morgane L V Robert (MLV)

Université de Montpellier, Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), CNRS UMR 5237, Montpellier Cedex 5, France.

Jérémy Sallé (J)

CNRS, Institut Jacques Monod, Université Paris Cité, Paris, France.
Equipe Labellisée Ligue Contre le Cancer, Paris, France.

Sébastien Cacchia (S)

Université de Montpellier, Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), CNRS UMR 5237, Montpellier Cedex 5, France.

Thierry Lorca (T)

Université de Montpellier, Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), CNRS UMR 5237, Montpellier Cedex 5, France.

Anna Castro (A)

Université de Montpellier, Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), CNRS UMR 5237, Montpellier Cedex 5, France.
Programme équipes Labellisées Ligue Contre le Cancer, Paris, France.

Alex McDougall (A)

Sorbonne Universités, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Villefranche-sur-mer, France.

Nicolas Minc (N)

CNRS, Institut Jacques Monod, Université Paris Cité, Paris, France.
Equipe Labellisée Ligue Contre le Cancer, Paris, France.

Stefania Castagnetti (S)

Sorbonne Universités, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Villefranche-sur-mer, France.

Julien Dumont (J)

CNRS, Institut Jacques Monod, Université Paris Cité, Paris, France.

Benjamin Lacroix (B)

Université de Montpellier, Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), CNRS UMR 5237, Montpellier Cedex 5, France. benjamin.lacroix@crbm.cnrs.fr.

Classifications MeSH