Amnioserosa cell constriction but not epidermal actin cable tension autonomously drives dorsal closure

Nature Cell Biology

Volumn 18, Issue 11, 2016, Pages 1161-1172

  Pasakarnis, Laurynas ^a   Frei, Erich ^a   Caussinus, Emmanuel ^a   Affolter, Markus ^b   Brunner, Damian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN II; DROSOPHILA PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ADULT; AMNIOSEROSA CELL; AMNIOSEROSA CELL CONSTRICTION; AMNIOSEROSA TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR PARAMETERS; CONTROLLED STUDY; DIPTERA; DORSAL CLOSURE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENHANCER REGION; EPIDERMAL ACTIN CABLE TENSION; FEMALE; MALE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ACTIN FILAMENT; ANIMAL; CELL MOTION; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; EPIDERMIS; LIGATION; METABOLISM; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTINS; ACTOMYOSIN; ANIMALS; BODY PATTERNING; CELL MOVEMENT; CONSTRICTION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPIDERMIS; MORPHOGENESIS;

EID: 84991696913     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3420     Document Type: Article

References (53)

1. Sandler, A. D. Children with spina bifida: key clinical issues. Pediatr. Clin. North Am. 57, 879-892 (2010).
2. Watkins, S. E., Meyer, R. E., Strauss, R. P. & Aylsworth, A. S. Classification, epidemiology, and genetics of orofacial clefts. Clin. Plast. Surg. 41, 149-163 (2014).
3. Edwards, K. A., Demsky, M., Montague, R. A., Weymouth, N. & Kiehart, D. P. GFPmoesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 191, 103-117 (1997).
4. Young, P. E., Richman, A. M., Ketchum, A. S. & Kiehart, D. P. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29-41 (1993).
5. Franke, J. D., Montague, R. A., Kiehart, D. P. & Carolina, N. Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr. Biol. 15, 2208-2221 (2005).
6. 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. 149, 471-490 (2000).
7. Eltsov, M. et al. Quantitative analysis of cytoskeletal reorganization during epithelial tissue sealing by large-volume electron tomography. Nat. Cell Biol. 17, 605-614 (2015).
8. Hutson, M. S. et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145-149 (2003).
9. Peralta, X. G. et al. Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys. J. 92, 2583-2596 (2007).
10. 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 137, 1331-1342 (2009).
11. David, D. J. V., Tishkina, A. & Harris, T. J. C. The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137, 1645-1655 (2010).
12. Blanchard, G. B., Murugesu, S., Adams, R. J., Martinez-Arias, A. & Gorfinkiel, N. Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137, 2743-2752 (2010).
13. Saravanan, S., Meghana, C. & Narasimha, M. Local, cell-nonautonomous feedback regulation of myosin dynamics patterns transitions in cell behavior: a role for tension and geometry? Mol. Biol. Cell 24, 2350-2361 (2013).
14. Jacinto, A. et al. Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250 (2002).
15. Scuderi, A. & Letsou, A. Amnioserosa is required for dorsal closure in Drosophila. Dev. Dyn. 232, 791-800 (2005).
16. Wada, A., Kato, K., Uwo, M. F., Yonemura, S. & Hayashi, S. Specialized extraembryonic cells connect embryonic and extraembryonic epidermis in response to Dpp during dorsal closure in Drosophila. Dev. Biol. 301, 340-349 (2007).
17. Wells, A. R. et al. Complete canthi removal reveals that forces from the amnioserosa alone are sufficient to drive dorsal closure in Drosophila. Mol. Biol. Cell 25, 3552-3568 (2014).
18. Rodriguez-Diaz, A. et al. Actomyosin purse strings: renewable resources that make morphogenesis robust and resilient. HFSP J. 2, 220-237 (2008).
19. Caussinus, E., Kanca, O. & Affolter, M. Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat. Struct. Mol. Biol. 19, 117-121 (2012).
20. Mizuno, T., Tsutsui, K. & Nishida, Y. Drosophila myosin phosphatase and its role in dorsal closure. Development 129, 1215-1223 (2002).
21. Wodarz, A., Hinz, U., Engelbert, M. & Knust, E. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76 (1995).
22. Manseau, L. et al. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209, 310-322 (1997).
23. Chatterjee, N. & Bohmann, D. A versatile 'C31 based reporter system for measuring AP-1 and NRF2 signaling in Drosophila and in tissue culture. PLoS One 7, e34063 (2012).
24. Fischer, S. C. et al. Contractile and mechanical properties of epithelia with perturbed actomyosin dynamics. PLoS One 9, e95695 (2014).
25. Lee A, T. J. Excessive Myosin activity in mbs mutants causes photoreceptor movement out of the Drosophila eye disc epithelium. Mol. Biol. Cell 15, 3285-3295 (2004).
26. Saias, L. et al. Decrease in cell volume generates contractile forces driving dorsal closure. Dev. Cell 33, 611-621 (2015).
27. Azevedo, D. et al. DRhoGEF2 regulates cellular tension and cell pulsations in the amnioserosa during Drosophila dorsal closure. PLoS One 6, e23964 (2011).
28. Ma, X., Lynch, H. E., Scully, P. C. & Hutson, M. S. Probing embryonic tissue mechanics with laser hole drilling. Phys. Biol. 6, 036004 (2009).
29. Gorfinkiel, N., Blanchard, G. B., Adams, R. J. & Martinez Arias, A. Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136, 1889-1898 (2009).
30. Herranz, H. & Morata, G. The functions of pannier during Drosophila embryogenesis. Development 128, 4837-4846 (2001).
31. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (1993).
32. Glise, B. & Noselli, S. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11, 1738-1747 (1997).
33. Pfeiffer, B. D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl Acad. Sci. USA 105, 9715-9720 (2008).
34. Takaesu, N. T., Johnson, A. N. & Newfeld, S. J. Posterior spiracle specific GAL4 lines: new reagents for developmental biology and respiratory physiology. Genesis 34, 16-18 (2002).
35. Sepp, K. J. & Auld, V. J. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093-1101 (1999).
36. Martín-Blanco, E. et al. Puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12, 557-670 (1998).
37. Jankovics, F. & Brunner, D. Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster. Dev. Cell 11, 375-385 (2006).
38. David, D. J. V., Wang, Q., Feng, J. J. & Harris, T. J. C. Bazooka inhibits aPKC to limit antagonism of actomyosin networks during amnioserosa apical constriction. Development 140, 4719-4729 (2013).
39. Sokolow, A., Toyama, Y., Kiehart, D. P. & Edwards, G. S. Cell ingression and apical shape oscillations during dorsal closure in Drosophila. Biophys. J. 102, 969-979 (2012).
40. Jayasinghe, A. K., Crews, S. M., Mashburn, D. N. & Hutson, M. S. Apical oscillations in amnioserosa cells: basolateral coupling and mechanical autonomy. Biophys. J. 105, 255-265 (2013).
41. Narasimha, M. & Brown, N. H. Novel functions for integrins in epithelial morphogenesis. Curr. Biol. 14, 381-385 (2004).
42. Machado, P. F. et al. Emergent material properties of developing epithelial tissues. BMC Biol. 13, 98 (2015).
43. Lehmann, R. & Nüsslein-Volhard, C. Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47, 141-152 (1986).
44. Franke, J. D., Montague, R. A. & Kiehart, D. P. Nonmuscle myosin II is required for cell proliferation, cell sheet adhesion and wing hair morphology during wing morphogenesis. Dev. Biol. 345, 117-132 (2010).
45. Wang, Q., Feng, J. J. & Pismen, L. M. A cell-level biomechanical model of Drosophila dorsal closure. Biophys. J. 103, 2265-2274 (2012).
46. Martin, A. C., Kaschube, M. & Wieschaus, E. F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499 (2009).
47. Rauzi, M., Lenne, P.-F. & Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114 (2010).
48. Gorfinkiel, N. & Arias, A. M. Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila. J. Cell Sci. 120, 3289-3298 (2007).
49. Kaltschmidt, J. A. et al. Planar polarity and actin dynamics in the epidermis of Drosophila. Nat. Cell Biol. 4, 937-944 (2002).
50. Ducuing, A. & Vincent, S. The actin cable is dispensable in directing dorsal closure dynamics but neutralizes mechanical stress to prevent scarring in the Drosophila embryo. Nat. Cell Biol. http://dx. doi. org/10. 1038/ncb3421 (2016).
51. Igaki, T. et al. Drob-1, a Drosophila member of the Bcl-2/CED-9 family that promotes cell death. Proc. Natl Acad. Sci. USA 97, 662-667 (2000).
52. Rubin, G. M. & Spradling, A. C. Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353 (1982).
53. Abreu-Blanco, M. T., Verboon, J. M. & Parkhurst, S. M. Cell wound repair in Drosophila occurs through three distinct phases of membrane and cytoskeletal remodeling. J. Cell Biol. 193, 455-464 (2011).