In Vivo Imaging Reveals a Role for Cdc42 in Spindle Positioning and Planar Orientation of Cell Divisions During Vertebrate Neural Tube Closure

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2009 Jun 25

PMID 19549689

Citations 24

Authors

Esther K Kieserman

John B Wallingford

Affiliations

Soon will be listed here.

Abstract

Specialization of the cell-division process is a common feature of developing embryos, but most studies on vertebrate cell division have focused on cells dividing in culture. Here, we used in vivo four-dimensional confocal microscopy to explore the role of Cdc42 in governing cell division in the developing neural epithelium of Xenopus laevis. We find that Cdc42 is crucial for stable positioning of the metaphase spindle in these cells, but was not required for spindle positioning in epidermal epithelial cells. We also find that divisions in the Xenopus neural plate are planar oriented, and that rotations of mitotic spindles are essential for establishing this orientation. When Cdc42 is disrupted, spindles over-rotate and the final orientation of divisions is changed. Finally, the planar orientation of cell divisions in this tissue seems to be independent of planar cell polarity (PCP) signaling and does not require normal neural morphogenesis. Our data provide new insights into the coordination of cell division and morphogenesis in epithelial cell sheets and reveal novel, cell-type-specific roles for Cdc42 in spindle positioning and spindle orientation.

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References

Gotta M, Abraham M, Ahringer J . CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr Biol. 2001; 11(7):482-8. DOI: 10.1016/s0960-9822(01)00142-7. View

Wallingford J, Harland R . Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development. 2002; 129(24):5815-25. DOI: 10.1242/dev.00123. View

Kwan K, Kirschner M . A microtubule-binding Rho-GEF controls cell morphology during convergent extension of Xenopus laevis. Development. 2005; 132(20):4599-610. PMC: 1783841. DOI: 10.1242/dev.02041. View

Haydar T, Ang Jr E, Rakic P . Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci U S A. 2003; 100(5):2890-5. PMC: 151436. DOI: 10.1073/pnas.0437969100. View

Philpott A, Yew P . The Xenopus cell cycle: an overview. Mol Biotechnol. 2008; 39(1):9-19. DOI: 10.1007/s12033-008-9033-z. View

Haigo S, Hildebrand J, Harland R, Wallingford J . Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr Biol. 2003; 13(24):2125-37. DOI: 10.1016/j.cub.2003.11.054. View

Couwenbergs C, Spilker A, Gotta M . Control of embryonic spindle positioning and Galpha activity by C. elegans RIC-8. Curr Biol. 2004; 14(20):1871-6. DOI: 10.1016/j.cub.2004.09.059. View

Yoshizaki H, Ohba Y, Kurokawa K, Itoh R, Nakamura T, Mochizuki N . Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol. 2003; 162(2):223-32. PMC: 2172791. DOI: 10.1083/jcb.200212049. View

Wallingford J . Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. Am J Med Genet C Semin Med Genet. 2005; 135C(1):59-68. DOI: 10.1002/ajmg.c.30054. View

10.

Hyman A, White J . Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol. 1987; 105(5):2123-35. PMC: 2114830. DOI: 10.1083/jcb.105.5.2123. View

11.

Palazzo A, JOSEPH H, Chen Y, Dujardin D, Alberts A, Pfister K . Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol. 2001; 11(19):1536-41. DOI: 10.1016/s0960-9822(01)00475-4. View

12.

Ban R, Irino Y, Fukami K, Tanaka H . Human mitotic spindle-associated protein PRC1 inhibits MgcRacGAP activity toward Cdc42 during the metaphase. J Biol Chem. 2004; 279(16):16394-402. DOI: 10.1074/jbc.M313257200. View

13.

Thery M, Bornens M . Cell shape and cell division. Curr Opin Cell Biol. 2006; 18(6):648-57. DOI: 10.1016/j.ceb.2006.10.001. View

14.

Karnoub A, Symons M, Campbell S, Der C . Molecular basis for Rho GTPase signaling specificity. Breast Cancer Res Treat. 2004; 84(1):61-71. DOI: 10.1023/B:BREA.0000018427.84929.5c. View

15.

Kieserman E, Glotzer M, Wallingford J . Developmental regulation of central spindle assembly and cytokinesis during vertebrate embryogenesis. Curr Biol. 2008; 18(2):116-23. DOI: 10.1016/j.cub.2007.12.028. View

16.

Deardorff M, Tan C, Conrad L, Klein P . Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. Development. 1998; 125(14):2687-700. DOI: 10.1242/dev.125.14.2687. View

17.

Na J, Zernicka-Goetz M . Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr Biol. 2006; 16(12):1249-54. DOI: 10.1016/j.cub.2006.05.023. View

18.

Gotz M, Huttner W . The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 2005; 6(10):777-88. DOI: 10.1038/nrm1739. View

19.

Wallingford J, Vogeli K, Harland R . Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. Int J Dev Biol. 2001; 45(1):225-7. View

20.

Garcia Z, Silio V, Marques M, Cortes I, Kumar A, Hernandez C . A PI3K activity-independent function of p85 regulatory subunit in control of mammalian cytokinesis. EMBO J. 2006; 25(20):4740-51. PMC: 1618105. DOI: 10.1038/sj.emboj.7601324. View