A Dynamic Microtubule Cytoskeleton Directs Medial Actomyosin Function During Tube Formation

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2014 Jun 11

PMID 24914560

Citations 55

Authors

Alexander J R Booth

Guy B Blanchard

Richard J Adams

Katja Roper

Affiliations

Soon will be listed here.

Abstract

The cytoskeleton is a major determinant of cell-shape changes that drive the formation of complex tissues during development. Important roles for actomyosin during tissue morphogenesis have been identified, but the role of the microtubule cytoskeleton is less clear. Here, we show that during tubulogenesis of the salivary glands in the fly embryo, the microtubule cytoskeleton undergoes major rearrangements, including a 90° change in alignment relative to the apicobasal axis, loss of centrosomal attachment, and apical stabilization. Disruption of the microtubule cytoskeleton leads to failure of apical constriction in placodal cells fated to invaginate. We show that this failure is due to loss of an apical medial actomyosin network whose pulsatile behavior in wild-type embryos drives the apical constriction of the cells. The medial actomyosin network interacts with the minus ends of acentrosomal microtubule bundles through the cytolinker protein Shot, and disruption of Shot also impairs apical constriction.

Citing Articles

Differential regulation of the proteome and phosphoproteome along the dorso-ventral axis of the early embryo.

Gomez J, Nolte H, Vogelsang E, Dey B, Takeda M, Giudice G Elife. 2024; 13.

PMID: 39221782 PMC: 11466282. DOI: 10.7554/eLife.99263.

β-H-Spectrin is a key component of an apical-medial hub of proteins during cell wedging in tube morphogenesis.

Gillard G, Roper K J Cell Sci. 2024; 137(15).

PMID: 38988298 PMC: 11361641. DOI: 10.1242/jcs.261946.

α-Spectrin regulates cell shape changes during disassembly of microtubule-driven protrusions in wings.

Tran N, Montanari M, Lubenets D, Fischbach L, Antson H, Okada Y MicroPubl Biol. 2024; 2024.

PMID: 38690064 PMC: 11058509. DOI: 10.17912/micropub.biology.001169.

Dynamic interplay of microtubule and actomyosin forces drive tissue extension.

Singh A, Thale S, Leibner T, Lamparter L, Ricker A, Nusse H Nat Commun. 2024; 15(1):3198.

PMID: 38609383 PMC: 11014958. DOI: 10.1038/s41467-024-47596-8.

Mechanical state transitions in the regulation of tissue form and function.

Mao Y, Wickstrom S Nat Rev Mol Cell Biol. 2024; 25(8):654-670.

PMID: 38600372 DOI: 10.1038/s41580-024-00719-x.

References

Hetherington S, Gally C, Fritz J, Polanowska J, Reboul J, Schwab Y . PAT-12, a potential anti-nematode target, is a new spectraplakin partner essential for Caenorhabditis elegans hemidesmosome integrity and embryonic morphogenesis. Dev Biol. 2010; 350(2):267-78. DOI: 10.1016/j.ydbio.2010.11.025. View

Zhang D, Grode K, Stewman S, Diaz-Valencia J, Liebling E, Rath U . Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat Cell Biol. 2011; 13(4):361-70. PMC: 3144748. DOI: 10.1038/ncb2206. View

Clark I, Jan L, Jan Y . Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development. 1997; 124(2):461-70. DOI: 10.1242/dev.124.2.461. View

Lee C, Scherr H, Wallingford J . Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development. 2007; 134(7):1431-41. DOI: 10.1242/dev.02828. View

Westermann S, Weber K . Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol. 2003; 4(12):938-47. DOI: 10.1038/nrm1260. View

Bertet C, Sulak L, Lecuit T . Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature. 2004; 429(6992):667-71. DOI: 10.1038/nature02590. View

DAvino P, Takeda T, Capalbo L, Zhang W, Lilley K, Laue E . Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J Cell Sci. 2008; 121(Pt 8):1151-8. DOI: 10.1242/jcs.026716. View

Corrigall D, Walther R, Rodriguez L, Fichelson P, Pichaud F . Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev Cell. 2007; 13(5):730-742. DOI: 10.1016/j.devcel.2007.09.015. View

Martin A, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus E . Integration of contractile forces during tissue invagination. J Cell Biol. 2010; 188(5):735-49. PMC: 2835944. DOI: 10.1083/jcb.200910099. View

10.

Roper K, Brown N . A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol. 2004; 14(2):99-110. View

11.

Lee J, Harland R . Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. Dev Biol. 2007; 311(1):40-52. PMC: 2744900. DOI: 10.1016/j.ydbio.2007.08.010. View

12.

Solon J, Kaya-Copur A, Colombelli J, Brunner D . Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell. 2009; 137(7):1331-42. DOI: 10.1016/j.cell.2009.03.050. View

13.

Bartolini F, Gundersen G . Generation of noncentrosomal microtubule arrays. J Cell Sci. 2006; 119(Pt 20):4155-63. DOI: 10.1242/jcs.03227. View

14.

Bush K, Lynch F, Denittis A, Steinberg A, Lee H, Nagele R . Neural tube formation in the mouse: a morphometric and computerized three-dimensional reconstruction study of the relationship between apical constriction of neuroepithelial cells and the shape of the neuroepithelium. Anat Embryol (Berl). 1990; 181(1):49-58. DOI: 10.1007/BF00189727. View

15.

Pope K, Harris T . Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis in Drosophila. Development. 2008; 135(13):2227-38. DOI: 10.1242/dev.019802. View

16.

Roper K, Brown N . Maintaining epithelial integrity: a function for gigantic spectraplakin isoforms in adherens junctions. J Cell Biol. 2003; 162(7):1305-15. PMC: 2173965. DOI: 10.1083/jcb.200307089. View

17.

Brodu V, Baffet A, Le Droguen P, Casanova J, Guichet A . A developmentally regulated two-step process generates a noncentrosomal microtubule network in Drosophila tracheal cells. Dev Cell. 2010; 18(5):790-801. DOI: 10.1016/j.devcel.2010.03.015. View

18.

Roper K, Gregory S, Brown N . The 'spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J Cell Sci. 2002; 115(Pt 22):4215-25. DOI: 10.1242/jcs.00157. View

19.

Gorfinkiel N, Blanchard G . Dynamics of actomyosin contractile activity during epithelial morphogenesis. Curr Opin Cell Biol. 2011; 23(5):531-9. DOI: 10.1016/j.ceb.2011.06.002. View

20.

David D, Tishkina A, Harris T . The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development. 2010; 137(10):1645-55. DOI: 10.1242/dev.044107. View