The actin cable is dispensable in directing dorsal closure dynamics but neutralizes mechanical stress to prevent scarring in the Drosophila embryo

Nature Cell Biology

Volumn 18, Issue 11, 2016, Pages 1149-1160

  Ducuing, Antoine ^a   Vincent, Stéphane ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYTOSKELETON PROTEIN; ENABLED PROTEIN; UNCLASSIFIED DRUG; Z BAND ALTERNATIVELY SPLICED PDZ MOTIF CONTAINING PROTEIN 52 PROTEIN; ACTIN; DROSOPHILA PROTEIN;

ACTIN CABLE; ARTICLE; CELL FUNCTION; CELL INTERACTION; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; MECHANICAL STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCAR FORMATION; SKIN DEFECT; WOUND HEALING; ACTIN FILAMENT; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; EMBRYOLOGY; EPIDERMIS; EPITHELIUM; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC DEVELOPMENT; EPIDERMIS; EPITHELIUM; STRESS, MECHANICAL; WOUND HEALING;

EID: 84991585606     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3421     Document Type: Article

References (44)

1. Wood, W. et al. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 4, 907-912 (2002).
2. Martin, P. & Parkhurst, S. M. Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034 (2004).
3. Belacortu, Y. & Paricio, N. Drosophila as a model of wound healing and tissue regeneration in vertebrates. Dev. Dyn. 240, 2379-2404 (2011).
4. Brock, J., Midwinter, K., Lewis, J. & Martin, P. Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement for Rho activation. J. Cell Biol. 135, 1097-1107 (1996).
5. Martin, P. & Lewis, J. Actin cables and epidermal movement in embryonic wound healing. Nature 360, 179-183 (1992).
6. Davidson, L. A., Ezin, A. M. & Keller, R. Embryonic wound healing by apical contraction and ingression in Xenopus laevis. Cell Motil. Cytoskeleton 53, 163-176 (2002).
7. Mateus, R. et al. In vivo cell and tissue dynamics underlying zebrafish fin fold regeneration. PLoS ONE 7, e51766 (2012).
8. Bement, W. M., Forscher, P. & Mooseker, M. S. A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol. 121, 565-578 (1993).
9. Danjo, Y. & Gipson, I. K. Actin 'purse string' filaments are anchored by E-cadherinmediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement. J. Cell Sci. 111, 3323-3332 (1998).
10. Jacinto, A., Martinez-Arias, A. & Martin, P. Mechanisms of epithelial fusion and repair. Nat. Cell Biol. 3, E117-E123 (2001).
11. 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).
12. Jacinto, A. et al. Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 10, 1420-1426 (2000).
13. Jacinto, A. et al. Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250 (2002).
14. 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).
15. 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).
16. Rodriguez-Diaz, A. et al. Actomyosin purse strings: renewable resources that make morphogenesis robust and resilient. HFSP J. 2, 220-237 (2008).
17. Hutson, M. S. et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145-149 (2003).
18. Faulkner, G. et al. ZASP: a new Z-band alternatively spliced PDZ-motif protein. J. Cell Biol. 146, 465-475 (1999).
19. Zhou, Q. et al. Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J. Cell Biol. 155, 605-612 (2001).
20. Zhou, Q., Ruiz-Lozano, P., Martone, M. E. & Chen, J. Cypher, a striated musclerestricted PDZ and LIM domain-containing protein, binds to -actinin-2 and protein kinase C. J. Biol. Chem. 274, 19807-19813 (1999).
21. Jani, K. & Schock, F. Zasp is required for the assembly of functional integrin adhesion sites. J. Cell Biol. 179, 1583-1597 (2007).
22. Katzemich, A., Liao, K. A., Czerniecki, S. & Schock, F. Alp/Enigma family proteins cooperate in Z-disc formation and myofibril assembly. PLoS Genet. 9, e1003342 (2013).
23. Ducuing, A., Keeley, C., Mollereau, B. & Vincent, S. A DPP-mediated feed-forward loop canalizes morphogenesis during Drosophila dorsal closure. J. Cell Biol. 208, 239-248 (2015).
24. Stronach, B. Extensive nonmuscle expression and epithelial apicobasal localization of the Drosophila ALP/Enigma family protein, Zasp52. Gene Expr. Patterns 15, 67-79 (2014).
25. Pashmforoush, M. et al. Adult mice deficient in actinin-associated LIM-domain protein reveal a developmental pathway for right ventricular cardiomyopathy. Nat. Med. 7, 591-597 (2001).
26. Arimura, T. et al. A Cypher/ZASP mutation associated with dilated cardiomyopathy alters the binding affinity to protein kinase C. J. Biol. Chem. 279, 6746-6752 (2004).
27. Selcen, D. & Engel, A. G. Mutations in ZASP define a novel form of muscular dystrophy in humans. Ann. Neurol. 57, 269-276 (2005).
28. Vatta, M. et al. Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J. Am. Coll. Cardiol. 42, 2014-2027 (2003).
29. Gettings, M. et al. JNK signalling controls remodelling of the segment boundary through cell reprogramming during Drosophila morphogenesis. PLoS Biol. 8, e1000390 (2010).
30. Katzemich, A., Long, J. Y., Jani, K., Lee, B. R. & Schock, F. Muscle typespecific expression of Zasp52 isoforms in Drosophila. Gene Expr. Patterns 11, 484-490 (2011).
31. Gates, J. et al. Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134, 2027-2039 (2007).
32. Grevengoed, E. E., Loureiro, J. J., Jesse, T. L. & Peifer, M. Abelson kinase regulates epithelial morphogenesis in Drosophila. J. Cell Biol. 155, 1185-1198 (2001).
33. Laplante, C. & Nilson, L. A. Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 133, 3255-3264 (2006).
34. Legoff, L., Rouault, H. & Lecuit, T. A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc. Development 140, 4051-4059 (2013).
35. Peralta, X. G. et al. Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys. J. 92, 2583-2596 (2007).
36. Verma, S. et al. A WAVE2-Arp2/3 actin nucleator apparatus supports junctional tension at the epithelial zonula adherens. Mol. Biol. Cell 23, 4601-4610 (2012).
37. Vincent, S., Perrimon, N. & Axelrod, J. D. Hedgehog and Wingless stabilize but do not induce cell fate during Drosophila dorsal embryonic epidermal patterning. Development 135, 2767-2775 (2008).
38. Pasakarnis, L., Frei, E., Caussinus, E., Affolter, M. & Brunner, D. Amnioserosa cell constriction but not epidermal actin cable tension autonomously drives dorsal closure. Nat. Cell Biol. http://dx. doi. org/10. 1038/ncb3420 (2016).
39. Caussinus, E., Kanca, O. & Affolter, M. Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat. Struct. Mol. Biol. 19, 117-121 (2012).
40. Millard, T. H. & Martin, P. Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135, 621-626 (2008).
41. Abate, A. et al. A mathematical model to study the dynamics of epithelial cellular networks. IEEE/ACM Trans. Comput. Biol. Bioinform. 9, 1607-1620 (2012).
42. Reffay, M. et al. Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat. Cell Biol. 16, 217-223 (2014).
43. Strudwick, X. L. & Cowin, A. J. Cytoskeletal regulation of dermal regeneration. Cells 1, 1313-1327 (2012).
44. Li, J., Zhang, S., Soto, X., Woolner, S. & Amaya, E. ERK and phosphoinositide 3-kinase temporally coordinate different modes of actin-based motility during embryonic wound healing. J. Cell Sci. 126, 5005-5017 (2013).