Modulation of Morphogenesis by Egfr during Dorsal Closure in Drosophila

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Shen, Weiping ^a,c   Chen, Xi ^a   Cormier, Olga ^b   Cheng, David Chung Pei ^a   Reed, Bruce ^b   Harden, Nicholas ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DECAPENTAPLEGIC PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN ACK; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMNIOSEROSA; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SHAPE; CONTROLLED STUDY; DORSAL CLOSURE; DPP GENE; DROSOPHILA; EGFR GENE; EMBRYO; EMBRYO (ANATOMY); EMBRYO DEVELOPMENT; ENDOCYTOSIS; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; INSECT DEVELOPMENT; INTRACELLULAR SIGNALING; MORPHOGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; ZIP GENE;

ALLELES; ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; ENDOCYTOSIS; EPIDERMIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MORPHOGENESIS; MYOSIN HEAVY CHAINS; PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84875997986     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060180     Document Type: Article

References (121)

1. Harden N, (2002) Signaling pathways directing the movement and fusion of epithelial sheets: lessons from dorsal closure in Drosophila. Differentiation 70: 181-203.
2. Reed BH, Wilk R, Schock F, Lipshitz HD, (2004) Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis. Curr Biol 14: 372-380.
3. Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS, (2008) Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321: 1683-1686.
4. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA, (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149: 471-490.
5. Heisenberg CP, (2009) Dorsal closure in Drosophila: cells cannot get out of the tight spot. Bioessays 31: 1284-1287.
6. Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, et al. (2000) Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr Biol 10: 1420-1426.
7. Jacinto A, Wood W, Woolner S, Hiley C, Turner L, et al. (2002) Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr Biol 12: 1245-1250.
8. Riesgo-Escovar JR, Hafen E, (1997) Common and distinct roles of DFos and DJun during Drosophila development. Science 278: 669-672.
9. Zeitlinger J, Kockel L, Peverali FA, Jackson DB, Mlodzik M, et al. (1997) Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophila fos mutants. EMBO J 16: 7393-7401.
10. Wada A, Kato K, Uwo MF, Yonemura S, Hayashi S, (2007) Specialized extraembryonic cells connect embryonic and extraembryonic epidermis in response to Dpp during dorsal closure in Drosophila. Dev Biol 301: 340-349.
11. Ricos MG, Harden N, Sem KP, Lim L, Chia W, (1999) Dcdc42 acts in TGF-β signaling during Drosophila morphogenesis: distinct roles for the Drac1/JNK and Dcdc42/TGF-β cascades in cytoskeletal regulation. J Cell Sci 112: 1225-1235.
12. Young PE, Richman AM, Ketchum AS, Kiehart DP, (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7: 29-41.
13. Glise B, Noselli S, (1997) Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev 11: 1738-1747.
14. Jackson PD, Hoffmann FM, (1994) Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression. Dev Dyn 199: 28-44.
15. St Johnston RD, Gelbart WM, (1987) Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6: 2785-2791.
16. Sluss HK, Davis RJ, (1997) Embryonic morphogenesis signaling pathway mediated by JNK targets the transcription factor JUN and the TGF-β homologue decapentaplegic. J Cell Biochem 67: 1-12.
17. Riesgo-Escovar JR, Hafen E, (1997) Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev 11: 1717-1727.
18. Hou XS, Goldstein ES, Perrimon N, (1997) Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev 11: 1728-1737.
19. Childs SR, Wrana JL, Arora K, Attisano L, O'Connor MB, et al. (1993) Identification of a Drosophila activin receptor. Proc Natl Acad Sci U S A 90: 9475-9479.
20. Affolter M, Nellen D, Nussbaumer U, Basler K, (1994) Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF β homologs during Drosophila embryogenesis. Development 120: 3105-3117.
21. Penton A, Chen Y, Staehling-Hampton K, Wrana JL, Attisano L, et al. (1994) Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a Decapentaplegic receptor. Cell 78: 239-250.
22. Letsou A, Arora K, Wrana JL, Simin K, Twombly V, et al. (1995) Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF β receptor family. Cell 80: 899-908.
23. Ruberte E, Marty T, Nellen D, Affolter M, Basler K, (1995) An absolute requirement for both the type II and type I receptors, Punt and Thick veins, for Dpp signaling in vivo. Cell 80: 889-897.
24. Arquier N, Perrin L, Manfruelli P, Semeriva M, (2001) The Drosophila tumor suppressor gene lethal(2)giant larvae is required for the emission of the Decapentaplegic signal. Development 128: 2209-2220.
25. Fernandez BG, Arias AM, Jacinto A, (2007) Dpp signalling orchestrates dorsal closure by regulating cell shape changes both in the amnioserosa and in the epidermis. Mech Dev 124: 884-897.
26. Zahedi B, Shen W, Xu X, Chen X, Mahey M, et al. (2008) Leading edge-secreted Dpp cooperates with ACK-dependent signaling from the amnioserosa to regulate myosin levels during dorsal closure. Dev Dyn 237: 2936-2946.
27. Franke JD, Montague RA, Kiehart DP, (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15: 2208-2221.
28. Hopper NA, Lee J, Sternberg PW, (2000) ARK-1 inhibits EGFR signaling in C. elegans. Mol Cell 6: 65-75.
29. Lin Q, Lo CG, Cerione RA, Yang W (2002) The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J Biol Chem 277: 10134-10138. Epub 12002 Jan 10117.
30. Shen F, Lin Q, Gu Y, Childress C, Yang W, (2007) Activated Cdc42-associated kinase 1 is a component of EGF receptor signaling complex and regulates EGF receptor degradation. Mol Biol Cell 18: 732-742.
31. Lin Q, Wang J, Childress C, Sudol M, Carey DJ, et al. (2010) HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Mol Cell Biol 30: 1541-1554.
32. Grovdal LM, Johannessen LE, Rodland MS, Madshus IH, Stang E, (2008) Dysregulation of Ack1 inhibits down-regulation of the EGF receptor. Exp Cell Res 314: 1292-1300.
33. Schweitzer R, Shilo BZ, (1997) A thousand and one roles for the Drosophila EGF receptor. Trends Genet 13: 191-196.
34. Shilo BZ, (2003) Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res 284: 140-149.
35. Clifford R, Schupbach T, (1992) The torpedo (DER) receptor tyrosine kinase is required at multiple times during Drosophila embryogenesis. Development 115: 853-872.
36. Clifford RJ, Schupbach T, (1989) Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics 123: 771-787.
37. Nusslein-Volhard C, Wieschaus E, Kluding H, (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster I. Zygotic loci on the second chromosome. Roux's Arch Dev Biol 193: 267-282.
38. Royzman I, Whittaker AJ, Orr-Weaver TL, (1997) Mutations in Drosophila DP and E2F distinguish G1-S progression from an associated transcriptional program. Genes Dev 11: 1999-2011.
39. Perkins LA, Johnson MR, Melnick MB, Perrimon N, (1996) The nonreceptor protein tyrosine phosphatase corkscrew functions in multiple receptor tyrosine kinase pathways in Drosophila. Dev Biol 180: 63-81.
40. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
41. Hinz U, Giebel B, Campos-Ortega JA, (1994) The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76: 77-87.
42. Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, et al. (1997) GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209: 310-322.
43. Gabay L, Seger R, Shilo BZ, (1997) MAP kinase in situ activation atlas during Drosophila embryogenesis. Development 124: 3535-3541.
44. Gabay L, Seger R, Shilo BZ, (1997) In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277: 1103-1106.
45. Oda H, Tsukita S, (2001) Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J Cell Sci 114: 493-501.
46. Byars CL, Bates KL, Letsou A, (1999) The dorsal-open group gene raw is required for restricted DJNK signaling during closure. Development 126: 4913-4923.
47. Wei HC, Sanny J, Shu H, Baillie DL, Brill JA, et al. (2003) The Sac1 lipid phosphatase regulates cell shape change and the JNK cascade during dorsal closure in Drosophila. Curr Biol 13: 1882-1887.
48. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, et al. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12: 557-570.
49. Yagi Y, Hayashi S, (1997) Role of the Drosophila EGF receptor in determination of the dorsoventral domains of escargot expression during primary neurogenesis. Genes Cells 2: 41-53.
50. Chen CK, Kuhnlein RP, Eulenberg KG, Vincent S, Affolter M, et al. (1998) The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development. Development 125: 4959-4968.
51. Dobens LL, Peterson JS, Treisman J, Raftery LA, (2000) Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary. Development 127: 745-754.
52. Kumar JP, Moses K, (2001) The EGF receptor and notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development. Development 128: 2689-2697.
53. Chen Y, Schupbach T, (2006) The role of brinker in eggshell patterning. Mech Dev 123: 395-406.
54. Carneiro K, Fontenele M, Negreiros E, Lopes E, Bier E, et al. (2006) Graded maternal short gastrulation protein contributes to embryonic dorsal-ventral patterning by delayed induction. Dev Biol 296: 203-218.
55. Shravage BV, Altmann G, Technau M, Roth S, (2007) The role of Dpp and its inhibitors during eggshell patterning in Drosophila. Development 134: 2261-2271.
56. Yan SJ, Zartman JJ, Zhang M, Scott A, Shvartsman SY, et al. (2009) Bistability coordinates activation of the EGFR and DPP pathways in Drosophila vein differentiation. Mol Syst Biol 5: 278.
57. Liu M, Lim TM, Cai Y, (2010) The Drosophila female germline stem cell lineage acts to spatially restrict DPP function within the niche. Sci Signal 3: ra57.
58. Szuts D, Bienz M, (2000) An autoregulatory function of Dfos during Drosophila endoderm induction. Mech Dev 98: 71-76.
59. Kopp A, Blackman RK, Duncan I, (1999) Wingless, decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila. Development 126: 3495-3507.
60. Wappner P, Gabay L, Shilo BZ, (1997) Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124: 4707-4716.
61. Peri F, Roth S, (2000) Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development 127: 841-850.
62. Deng WM, Bownes M, (1997) Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development 124: 4639-4647.
63. de Celis JF, (1997) Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development 124: 1007-1018.
64. Carmena A, Gisselbrecht S, Harrison J, Jimenez F, Michelson AM, (1998) Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev 12: 3910-3922.
65. Martin-Blanco E, Roch F, Noll E, Baonza A, Duffy JB, et al. (1999) A temporal switch in DER signaling controls the specification and differentiation of veins and interveins in the Drosophila wing. Development 126: 5739-5747.
66. Jordan KC, Clegg NJ, Blasi JA, Morimoto AM, Sen J, et al. (2000) The homeobox gene mirror links EGF signalling to embryonic dorso-ventral axis formation through notch activation. Nat Genet 24: 429-433.
67. Dequier E, Souid S, Pal M, Maroy P, Lepesant JA, et al. (2001) Top-DER- and Dpp-dependent requirements for the Drosophila fos/kayak gene in follicular epithelium morphogenesis. Mech Dev 106: 47-60.
68. Shirai T, Maehara A, Kiritooshi N, Matsuzaki F, Handa H, et al. (2003) Differential requirement of EGFR signaling for the expression of defective proventriculus gene in the Drosophila endoderm and ectoderm. Biochem Biophys Res Commun 311: 473-477.
69. Motola S, Neuman-Silberberg FS, (2004) spoonbill, a new Drosophila female-sterile mutation, interferes with chromosome organization and dorsal-ventral patterning of the egg. Dev Dyn 230: 535-545.
70. de Navascues J, Modolell J, (2007) tailup, a LIM-HD gene, and Iro-C cooperate in Drosophila dorsal mesothorax specification. Development 134: 1779-1788.
71. O'Keefe DD, Prober DA, Moyle PS, Rickoll WL, Edgar BA, (2007) Egfr/Ras signaling regulates DE-cadherin/Shotgun localization to control vein morphogenesis in the Drosophila wing. Dev Biol 311: 25-39.
72. Yakoby N, Lembong J, Schupbach T, Shvartsman SY, (2008) Drosophila eggshell is patterned by sequential action of feedforward and feedback loops. Development 135: 343-351.
73. Kim SY, Jung KI, Kim SH, Jeon SH, (2008) Dpp represses eagle expression at short-range, but can repress its expression at a long-range via EGFR signal repression. Mol Cells 26: 576-582.
74. Chang T, Shy D, Hartenstein V, (2003) Antagonistic relationship between Dpp and EGFR signaling in Drosophila head patterning. Dev Biol 263: 103-113.
75. Crozatier M, Glise B, Vincent A, (2002) Connecting Hh, Dpp and EGF signalling in patterning of the Drosophila wing; the pivotal role of collier/knot in the AP organiser. Development 129: 4261-4269.
76. Kubota K, Goto S, Eto K, Hayashi S, (2000) EGF receptor attenuates Dpp signaling and helps to distinguish the wing and leg cell fates in Drosophila. Development 127: 3769-3776.
77. Letizia A, Barrio R, Campuzano S, (2007) Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning. Development 134: 1337-1346.
78. Sotillos S, De Celis JF, (2005) Interactions between the Notch, EGFR, and decapentaplegic signaling pathways regulate vein differentiation during Drosophila pupal wing development. Dev Dyn 232: 738-752.
79. Szuts D, Eresh S, Bienz M, (1998) Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction. Genes Dev 12: 2022-2035.
80. von Ohlen T, Doe CQ, (2000) Convergence of Dorsal, Dpp, and Egfr signaling pathways subdivides the Drosophila neuroectoderm into three dorsal-ventral columns. Dev Biol 224: 362-372.
81. Wahlstrom G, Norokorpi HL, Heino TI, (2006) Drosophila alpha-actinin in ovarian follicle cells is regulated by EGFR and Dpp signalling and required for cytoskeletal remodelling. Mech Dev 123: 801-818.
82. Kretzschmar M, Doody J, Massague J, (1997) Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 389: 618-622.
83. Radke K, Johnson K, Guo R, Davidson A, Ambrosio L, (2001) Drosophila-raf acts to elaborate dorsoventral pattern in the ectoderm of developing embryos. Genetics 159: 1031-1044.
84. Lamka ML, Lipshitz HD, (1999) Role of the amnioserosa in germ band retraction of the Drosophila melanogaster embryo. Dev Biol 214: 102-112.
85. Reed BH, Wilk R, Lipshitz HD, (2001) Downregulation of Jun kinase signaling in the amnioserosa is essential for dorsal closure of the Drosophila embryo. Curr Biol 11: 1098-1108.
86. Stronach BE, Perrimon N, (2001) Investigation of leading edge formation at the interface of amnioserosa and dorsal ectoderm in the Drosophila embryo. Development 128: 2905-2913.
87. Conder R, Yu H, Ricos M, Hing H, Chia W, et al. (2004) dPak is required for integrity of the leading edge cytoskeleton during Drosophila dorsal closure but does not signal through the JNK cascade. Dev Biol 276: 378-390.
88. Scuderi A, Letsou A, (2005) Amnioserosa is required for dorsal closure in Drosophila. Dev Dyn 232: 791-800.
89. Lada K, Gorfinkiel N, Martinez Arias A, (2012) Interactions between the amnioserosa and the epidermis revealed by the function of the u-shaped gene. Biol Open 1: 353-361.
90. Schweitzer R, Shaharabany M, Seger R, Shilo BZ, (1995) Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev 9: 1518-1529.
91. Goentoro LA, Reeves GT, Kowal CP, Martinelli L, Schupbach T, et al. (2006) Quantifying the Gurken morphogen gradient in Drosophila oogenesis. Dev Cell 11: 263-272.
92. Lee T, Feig L, Montell DJ, (1996) Two distinct roles for Ras in a developmentally regulated cell migration. Development 122: 409-418.
93. Frank LH, Rushlow C, (1996) A group of genes required for maintenance of the amnioserosa tissue in Drosophila. Development 122: 1343-1352.
94. Goldman-Levi R, Miller C, Greenberg G, Gabai E, Zak NB, (1996) Cellular pathways acting along the germband and in the amnioserosa may participate in germband retraction of the Drosophila melanogaster embryo. Int J Dev Biol 40: 1043-1051.
95. Mohseni N, McMillan SC, Chaudhary R, Mok J, Reed BH, (2009) Autophagy promotes caspase-dependent cell death during Drosophila development. Autophagy 5: 329-338.
96. Kurada P, White K, (1998) Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95: 319-329.
97. Bardet PL, Kolahgar G, Mynett A, Miguel-Aliaga I, Briscoe J, et al. (2008) A fluorescent reporter of caspase activity for live imaging. Proc Natl Acad Sci U S A 105: 13901-13905.
98. Cormier O, Mohseni N, Voytyuk I, Reed BH, (2012) Autophagy can promote but is not required for epithelial cell extrusion in the amnioserosa of the Drosophila embryo. Autophagy 8: 252-264.
99. Clem RJ, Fechheimer M, Miller LK, (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388-1390.
100. Eden ER, White IJ, Futter CE, (2009) Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. Biochem Soc Trans 37: 173-177.
101. Sem KP, Zahedi B, Tan I, Deak M, Lim L, et al. (2002) ACK family tyrosine kinase activity is a component of Dcdc42 Signaling during dorsal closure in Drosophila melanogaster. Mol Cell Biol 22: 3685-3697.
102. Morel V, Arias AM, (2004) Armadillo/beta-catenin-dependent Wnt signalling is required for the polarisation of epidermal cells during dorsal closure in Drosophila. Development 131: 3273-3283.
103. McEwen DG, Cox RT, Peifer M, (2000) The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning. Development 127: 3607-3617.
104. Nagaraj R, Banerjee U, (2009) Regulation of Notch and Wingless signalling by phyllopod, a transcriptional target of the EGFR pathway. EMBO J 28: 337-346.
105. Dumstrei K, Nassif C, Abboud G, Aryai A, Hartenstein V, (1998) EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125: 3417-3426.
106. Dumstrei K, Wang F, Shy D, Tepass U, Hartenstein V, (2002) Interaction between EGFR signaling and DE-cadherin during nervous system morphogenesis. Development 129: 3983-3994.
107. VanHook A, Letsou A, (2008) Head involution in Drosophila: genetic and morphogenetic connections to dorsal closure. Dev Dyn 237: 28-38.
108. Schoenherr JA, Drennan JM, Martinez JS, Chikka MR, Hall MC, et al. (2012) Drosophila activated Cdc42 kinase has an anti-apoptotic function. PLoS Genet 8: e1002725.
109. Mateus AM, Gorfinkiel N, Schamberg S, Martinez Arias A, (2011) Endocytic and recycling endosomes modulate cell shape changes and tissue behaviour during morphogenesis in Drosophila. PLoS One 6: e18729.
110. Freeman M, (2000) Feedback control of intercellular signalling in development. Nature 408: 313-319.
111. Segatto S, Anastasi S, Alema S, (2011) Regulation of epidermal growth factor signalling by inducible feedback inhibitors. J Cell Sci 124: 1785-1793.
112. Wood W, Jacinto A, Grose R, Woolner S, Gale J, et al. (2002) Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4: 907-912.
113. Martin P, Parkhurst SM, (2004) Parallels between tissue repair and embryo morphogenesis. Development 131: 3021-3034.
114. Campos I, Geiger JA, Santos AC, Carlos V, Jacinto A, (2010) Genetic screen in Drosophila melanogaster uncovers a novel set of genes required for embryonic epithelial repair. Genetics 184: 129-140.
115. Geiger JA, Carvalho L, Campos I, Santos AC, Jacinto A, (2011) Hole-in-one mutant phenotypes link EGFR/ERK signaling to epithelial tissue repair in Drosophila. PLoS One 6: e28349.
116. Ashburner M (1989) Drosophila: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
117. Harden N, Lee J, Loh HY, Ong YM, Tan I, et al. (1996) A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol Cell Biol 16: 1896-1908.
118. Harden N, Ricos M, Ong YM, Chia W, Lim L, (1999) Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 112: 273-284.
119. Van Vactor D, Kopczynski C (1999) Anatomical Techniques for Analysis of Nervous System Development in the Drosophila Embryo. In: Richter J, editor. A Comparative Methods Approach to the Study of Oocytes and Embryos. New York: Oxford University Press. 490-513.
120. Lecuyer E, Parthasarathy N, Krause HM (2007) Fluorescent in situ Hybridization Protocols in Drosophila Embryos and Tissues. In: Dahmann C, editor. Drosophila: Methods and Protocols. Totowa, NJ: Humana Press.
121. Reed BH, McMillan SC, Chaudhary R (2009) The preparation of Drosophila embryos for live-imaging using the hanging drop protocol. J Vis Exp.