Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure

Developmental Cell

Volumn 33, Issue 5, 2015, Pages 611-621

  Saias, Laure ^a,b   Swoger, Jim ^a,b   D'Angelo, Arturo ^a,b   Hayes, Peran ^a,b   Colombelli, Julien ^c   Sharpe, James ^a,b,d   Salbreux, Guillaume ^e   Solon, Jérôme ^a,b  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^e MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CASPASE; DROSOPHILA PROTEIN; MYOSIN;

ARTICLE; CELL MATURATION; CELL VOLUME; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; FORCE; HEART MUSCLE CONTRACTILE FORCE; HUMAN; MOVEMENT (PHYSIOLOGY); MUSCLE CONTRACTILITY; PRESSURE; PRIORITY JOURNAL; TENSION; ACTIN FILAMENT; ANIMAL; ANIMAL EMBRYO; BIOMECHANICS; CELL SIZE; CYTOLOGY; DROSOPHILA; EMBRYOLOGY; EPITHELIUM CELL; MECHANOTRANSDUCTION; METABOLISM; MORPHOGENESIS; PHOSPHORYLATION; PHYSIOLOGY; SEROSA; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ANIMALS; BIOMECHANICAL PHENOMENA; CASPASES; CELL SIZE; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPITHELIAL CELLS; MECHANOTRANSDUCTION, CELLULAR; MORPHOGENESIS; MYOSINS; PHOSPHORYLATION; SEROUS MEMBRANE;

EID: 84930575028     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.03.016     Document Type: Article

References (46)

1. Bardet P.L., Kolahgar G., Mynett A., Miguel-Aliaga I., Briscoe J., Meier P., Vincent J.P. A fluorescent reporter of caspase activity for live imaging. Proc. Natl. Acad. Sci. USA 2008, 105:13901-13905.
2. Bortner C.D., Cidlowski J.A. Apoptotic volume decrease and the incredible shrinking cell. Cell Death Differ. 2002, 9:1307-1310.
3. Bortner C.D., Cidlowski J.A. Cell shrinkage and monovalent cation fluxes: role in apoptosis. Arch. Biochem. Biophys. 2007, 462:176-188.
4. Brodu V., Casanova J. The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination. Genes Dev. 2006, 20:1817-1828.
5. Corrigall D., Walther R.F., Rodriguez L., Fichelson P., Pichaud F. Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev. Cell 2007, 13:730-742.
6. David D.J., Wang Q., Feng J.J., Harris T.J. Bazooka inhibits aPKC to limit antagonism of actomyosin networks during amnioserosa apical constriction. Development 2013, 140:4719-4729.
7. Farhadifar R., Röper J.C., Aigouy B., Eaton S., Jülicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 2007, 17:2095-2104.
8. Fischer S.C., Blanchard G.B., Duque J., Adams R.J., Arias A.M., Guest S.D., Gorfinkiel N. Contractile and mechanical properties of epithelia with perturbed actomyosin dynamics. PLoS ONE 2014, 9:e95695.
9. Förster D., Luschnig S. Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat. Cell Biol. 2012, 14:526-534.
10. Franke J.D., Montague R.A., Kiehart D.P. Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr. Biol. 2005, 15:2208-2221.
11. Gorfinkiel N., Blanchard G.B., Adams R.J., Martinez Arias A. Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 2009, 136:1889-1898.
12. Hannezo E., Prost J., Joanny J.F. Theory of epithelial sheet morphology in three dimensions. Proc. Natl. Acad. Sci. USA 2014, 111:27-32.
13. Hernández-Enríquez B., Arellano R.O., Morán J. Role for ionic fluxes on cell death and apoptotic volume decrease in cultured cerebellar granule neurons. Neuroscience 2010, 167:298-311.
14. Hočevar Brezavšček A., Rauzi M., Leptin M., Ziherl P. A model ofepithelial invagination driven by collective mechanics of identical cells. Biophys. J. 2012, 103:1069-1077.
15. Huisken J., Swoger J., Del Bene F., Wittbrodt J., Stelzer E.H. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 2004, 305:1007-1009.
16. Hutson M.S., Tokutake Y., Chang M.S., Bloor J.W., Venakides S., Kiehart D.P., Edwards G.S. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 2003, 300:145-149.
17. Jablonski E.M., Webb A.N., McConnell N.A., Riley M.C., Hughes F.M. Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am. J. Physiol. Cell Physiol. 2004, 286:C975-C985.
18. Jacinto A., Woolner S., Martin P. Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell 2002, 3:9-19.
19. Kiehart D.P., Galbraith C.G., Edwards K.A., Rickoll W.L., Montague R.A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J.Cell Biol. 2000, 149:471-490.
20. Lannan E., Vandergaast R., Friesen P.D. Baculovirus caspase inhibitors P49 and P35 block virus-induced apoptosis downstream of effector caspase DrICE activation in Drosophila melanogaster cells. J.Virol. 2007, 81:9319-9330.
21. Layton A.T., Toyama Y., Yang G.Q., Edwards G.S., Kiehart D.P., Venakides S. Drosophila morphogenesis: tissue force laws and the modeling of dorsal closure. HFSP J. 2009, 3:441-460.
22. Lebreton G., Casanova J. Specification of leading and trailing cell features during collective migration in the Drosophila trachea. J.Cell Sci. 2014, 127:465-474.
23. Li F., Huang Q., Chen J., Peng Y., Roop D.R., Bedford J.S., Li C.Y. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci. Signal. 2010, 3:ra13.
24. Llimargas M., Casanova J. Apical constriction and invagination: a very self-reliant couple. Dev. Biol. 2010, 344:4-6.
25. Maeno E., Ishizaki Y., Kanaseki T., Hazama A., Okada Y. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. USA 2000, 97:9487-9492.
26. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
27. Muliyil S., Krishnakumar P., Narasimha M. Spatial, temporal and molecular hierarchies in the link between death, delamination and dorsal closure. Development 2011, 138:3043-3054.
28. Núñez R., Sancho-Martínez S.M., Novoa J.M., López-Hernández F.J. Apoptotic volume decrease as a geometric determinant for cell dismantling into apoptotic bodies. Cell Death Differ. 2010, 17:1665-1671.
29. Porter A.G., Jänicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
30. Reed B.H., Wilk R., Schöck F., Lipshitz H.D. Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis. Curr. Biol. 2004, 14:372-380.
31. Rodriguez-Diaz A., Toyama Y., Abravanel D.L., Wiemann J.M., Wells A.R., Tulu U.S., Edwards G.S., Kiehart D.P. Actomyosin purse strings: renewable resources that make morphogenesis robust and resilient. HFSP J. 2008, 2:220-237.
32. Roth K.A., D'Sa C. Apoptosis and brain development. Ment. Retard. Dev. Disabil. Res. Rev. 2001, 7:261-266.
33. Royou A., Sullivan W., Karess R. Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J.Cell Biol. 2002, 158:127-137.
34. Salbreux G., Charras G., Paluch E. Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol. 2012, 22:536-545.
35. Sawyer J.M., Harrell J.R., Shemer G., Sullivan-Brown J., Roh-Johnson M., Goldstein B. Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 2010, 341:5-19.
36. Shen W., Chen X., Cormier O., Cheng D.C., Reed B., Harden N. Modulation of morphogenesis by Egfr during dorsal closure in Drosophila. PLoS ONE 2013, 8:e60180.
37. 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, 137:1331-1342.
38. Stewart M.P., Helenius J., Toyoda Y., Ramanathan S.P., Muller D.J., Hyman A.A. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469:226-230.
39. Swoger J., Muzzopappa M., Lopez-Schier H., Sharpe J. 4D retrospective lineage tracing using SPIM for zebrafish organogenesis studies. J.Biophotonics 2011, 4:122-134.
40. Toyama Y., Peralta X.G., Wells A.R., Kiehart D.P., Edwards G.S. Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 2008, 321:1683-1686.
41. Verveer P.J., Swoger J., Pampaloni F., Greger K., Marcello M., Stelzer E.H. High-resolution three-dimensional imaging of large specimens with light sheet-based microscopy. Nat. Methods 2007, 4:311-313.
42. Vu C.C., Bortner C.D., Cidlowski J.A. Differential involvement of initiator caspases in apoptotic volume decrease and potassium efflux during Fas- and UV-induced cell death. J.Biol. Chem. 2001, 276:37602-37611.
43. Wang Y.C., Khan Z., Kaschube M., Wieschaus E.F. Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 2012, 484:390-393.
44. Wood W., Jacinto A., Grose R., Woolner S., Gale J., Wilson C., Martin P. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 2002, 4:907-912.
45. Yu S.P., Choi D.W. Ions, cell volume, and apoptosis. Proc. Natl. Acad. Sci. USA 2000, 97:9360-9362.
46. Zuzarte-Luis V., Hurle J.M. Programmed cell death in the embryonic vertebrate limb. Semin. Cell Dev. Biol. 2005, 16:261-269.