Myosin-X is Dispensable for Spindle Morphogenesis and Positioning in the Mouse Oocyte

Overview

Journal Development

Specialty Biology

Date 2021 Mar 16

PMID 33722900

Citations 5

Authors

Flora Crozet

Christelle Da Silva

Marie-Helene Verlhac

Marie-Emilie Terret

Affiliations

Soon will be listed here.

Abstract

Off-center spindle positioning in mammalian oocytes enables asymmetric divisions in size, which are important for subsequent embryogenesis. The migration of the meiosis I spindle from the oocyte center to its cortex is mediated by F-actin. Specifically, an F-actin cage surrounds the microtubule spindle and applies forces to it. To better understand how F-actin transmits forces to the spindle, we studied a potential direct link between F-actin and microtubules. For this, we tested the implication of myosin-X, a known F-actin and microtubule binder involved in spindle morphogenesis and/or positioning in somatic cells, amphibian oocytes and embryos. Using a mouse strain conditionally invalidated for myosin-X in oocytes and by live-cell imaging, we show that myosin-X is not localized on the spindle, and is dispensable for spindle and F-actin assembly. It is not required for force transmission as spindle migration and chromosome alignment occur normally. More broadly, myosin-X is dispensable for oocyte developmental potential and female fertility. We therefore exclude a role for myosin-X in transmitting F-actin-mediated forces to the spindle, opening new perspectives regarding this mechanism in mouse oocytes, which differ from most mitotic cells.

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References

Yanez L, Han J, Behr B, Pera R, Camarillo D . Human oocyte developmental potential is predicted by mechanical properties within hours after fertilization. Nat Commun. 2016; 7:10809. PMC: 4770082. DOI: 10.1038/ncomms10809. View

Schuh M, Ellenberg J . Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007; 130(3):484-98. DOI: 10.1016/j.cell.2007.06.025. View

di Pietro F, Echard A, Morin X . Regulation of mitotic spindle orientation: an integrated view. EMBO Rep. 2016; 17(8):1106-30. PMC: 4967962. DOI: 10.15252/embr.201642292. View

Woolner S, OBrien L, Wiese C, Bement W . Myosin-10 and actin filaments are essential for mitotic spindle function. J Cell Biol. 2008; 182(1):77-88. PMC: 2447898. DOI: 10.1083/jcb.200804062. View

Mogessie B, Schuh M . Actin protects mammalian eggs against chromosome segregation errors. Science. 2017; 357(6353). DOI: 10.1126/science.aal1647. View

Brieno-Enriquez M, Moak S, Holloway J, Cohen P . NIMA-related kinase 1 (NEK1) regulates meiosis I spindle assembly by altering the balance between α-Adducin and Myosin X. PLoS One. 2017; 12(10):e0185780. PMC: 5628868. DOI: 10.1371/journal.pone.0185780. View

Tsurumi C, Hoffmann S, Geley S, Graeser R, Polanski Z . The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J Cell Biol. 2004; 167(6):1037-50. PMC: 2172623. DOI: 10.1083/jcb.200405165. View

Sandquist J, Larson M, Hine K . Myosin-10 independently influences mitotic spindle structure and mitotic progression. Cytoskeleton (Hoboken). 2016; 73(7):351-64. PMC: 5017926. DOI: 10.1002/cm.21311. View

Woolner S, Papalopulu N . Spindle position in symmetric cell divisions during epiboly is controlled by opposing and dynamic apicobasal forces. Dev Cell. 2012; 22(4):775-87. PMC: 3332010. DOI: 10.1016/j.devcel.2012.01.002. View

10.

Fink J, Carpi N, Betz T, Betard A, Chebah M, Azioune A . External forces control mitotic spindle positioning. Nat Cell Biol. 2011; 13(7):771-8. DOI: 10.1038/ncb2269. View

11.

Morin X, Bellaiche Y . Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev Cell. 2011; 21(1):102-19. DOI: 10.1016/j.devcel.2011.06.012. View

12.

Yi K, Rubinstein B, Unruh J, Guo F, Slaughter B, Li R . Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J Cell Biol. 2013; 200(5):567-76. PMC: 3587830. DOI: 10.1083/jcb.201211068. View

13.

Thery M, Racine V, Pepin A, Piel M, Chen Y, Sibarita J . The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol. 2005; 7(10):947-53. DOI: 10.1038/ncb1307. View

14.

Verlhac M, Lefebvre C, Guillaud P, Rassinier P, Maro B . Asymmetric division in mouse oocytes: with or without Mos. Curr Biol. 2000; 10(20):1303-6. DOI: 10.1016/s0960-9822(00)00753-3. View

15.

Szollosi D, Calarco P, Donahue R . Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci. 1972; 11(2):521-41. DOI: 10.1242/jcs.11.2.521. View

16.

So C, Seres K, Steyer A, Monnich E, Clift D, Pejkovska A . A liquid-like spindle domain promotes acentrosomal spindle assembly in mammalian oocytes. Science. 2019; 364(6447). PMC: 6629549. DOI: 10.1126/science.aat9557. View

17.

Bennabi I, Terret M, Verlhac M . Meiotic spindle assembly and chromosome segregation in oocytes. J Cell Biol. 2016; 215(5):611-619. PMC: 5147004. DOI: 10.1083/jcb.201607062. View

18.

Mitsushima M, Aoki K, Ebisuya M, Matsumura S, Yamamoto T, Matsuda M . Revolving movement of a dynamic cluster of actin filaments during mitosis. J Cell Biol. 2010; 191(3):453-62. PMC: 3003322. DOI: 10.1083/jcb.201007136. View

19.

Duan X, Li Y, Yi K, Guo F, Wang H, Wu P . Dynamic organelle distribution initiates actin-based spindle migration in mouse oocytes. Nat Commun. 2020; 11(1):277. PMC: 6959240. DOI: 10.1038/s41467-019-14068-3. View

20.

Chaigne A, Campillo C, Gov N, Voituriez R, Azoury J, Umana-Diaz C . A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat Cell Biol. 2013; 15(8):958-66. DOI: 10.1038/ncb2799. View