Signaling pathways directing the movement and fusion of epithelial sheets: Lessons from dorsal closure in Drosophila

Differentiation

Volumn 70, Issue 4-5, 2002, Pages 181-203

  Harden, Nicholas ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Cytoskeleton; Dorsal closure; Drosophila; Epithelial morphogenesis; Signal transduction

Indexed keywords

GUANOSINE TRIPHOSPHATASE; LYMPHOTOXIN; PROTEIN C JUN; RHO KINASE; DROSOPHILA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA;

AMINO TERMINAL SEQUENCE; CELL ACTIVATION; CELL FUSION; CELL INTERACTION; CELL JUNCTION; CELL MIGRATION; CELL MOTION; CELL SHAPE; CELL SPREADING; CELL STRUCTURE; DROSOPHILA; EPITHELIUM; EPITHELIUM CELL; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WOUND HEALING; ANIMAL; ANIMAL EMBRYO; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; PRENATAL DEVELOPMENT;

HEXAPODA; METAZOA;

ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPITHELIAL CELLS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP PHOSPHOHYDROLASES; INTERCELLULAR JUNCTIONS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 0036599061     PISSN: 03014681     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-0436.2002.700408.x     Document Type: Review

References (184)

1. Abram, C.L. and Courtneidge, S.A. (2000) Src family tyrosine kinases and growth factor signaling. Exp Cell Res 254:1-13.
2. Affolter, M., Nellen, D., Nussbaumer, U. and 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.
3. Affolter, M., Marty, T., Vigano, M.A. and Jazwinska, A. (2001) Nuclear interpretation of Dpp signaling in Drosophila. EMBO J 20:3298-3305.
4. Agnès, F., Suzanne, M. and Noselli, S. (1999) The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126:5453-5462.
5. Amano, M., Mukai, H., Ono, Y., Chihara, K., Matsui, T., Hamajima, Y., Okawa, K., Iwamatsu, A. and Kaibuchi, K. (1996) Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science 271:648-650.
6. Arora, K., Dai, H., Kazuko, S.G., Jamal, J., O'Connor, M.B., Letsou, A. and Warrior, R. (1995) The Drosophila schnurri gene acts in the Dpp/TGF β signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81:781-790.
7. Arquier, N., Perrin, L., Manfruelli, P. and Sémériva, M. (2001) The Drosophila tumor suppressor gene lethal(2)giant larvae is required for the emission of the Decapentaplegic signal. Development 128:2209-2220.
8. Artavanis-Tsakonas, S., Matsuno, K. and Fortini, M.E. (1995) Notch signaling. Science 268:225-232.
9. Bard, J. (1990) Morphogenesis: The Cellular and Molecular Processes of Developmental Anatomy, first edn. Cambridge University Press, Cambridge, U.K.
10. Baumgartner, S., Littleton, J.T., Broadie, K., Bhat, M.A., Harbecke, R., Lengyel, J.A., Chiquet-Ehrismann, R., Prokop, A. and Bellen, H.J. (1996) A Drosophila Neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87:1059-1068.
11. Ben-Yaacov, S., Le Borgne, R., Abramson, I., Schweisguth, F. and Schejter, E.D (2001) Wasp, the Drosophila Wiskott-Aldrich syndrome gene homologue, is required for cell fate decisions mediated by Notch signaling. J Cell Biol 152:1-13.
12. Bennett, R.L. and Hoffmann, F.M. (1992) Increased levels of the Drosophila Abelson tyrosine kinase in nerves and muscles: sub-cellular localization and mutant phenotypes imply a role in cell-cell interactions. Development 116:953-966.
13. Bilder, D., Li, M. and Perrimon, N. (2000) Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289:113-116.
14. Bilder, D. and Perrimon, N. (2000) Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676-680.
15. Bishop, A.L. and Hall, A. (2000) Rho GTPases and their effector proteins. Biochem J 348(Pt 2):241-255.
16. Blake, K.J., Myette, G. and Jack, J. (1998) The products of ribbon and raw are necessary for proper cell shape and cellular localization of nonmuscle myosin in Drosophila. Dev Biol 203:177-188.
17. Blake, K.J., Myette, G. and Jack, J. (1999) ribbon, raw, and zipper have distinct functions in reshaping the Drosophila cytoskeleton. Dev Genes Evol 209:555-559.
18. Bock, B.C., Vacratsis, P.O., Qamirani, E. and Gallo, K.A. (2000) Cdc42-induced activation of the mixed-lineage kinase SPRK in vivo. Requirement of the Cdc42/Rac interactive binding motif and changes in phosphorylation. J Biol Chem 275:14231-14241.
19. Boutros, M. and Mlodzik, M. (1999) Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech Dev 83:27-37.
20. Bradley, P.L. and Andrew, D.J. (2001) ribbon encodes a novel BTB/ POZ protein required for directed cell migration in Drosophila melanogaster. Development 128:3001-3015.
21. Brennan, K., Baylies, M. and Martinez Arias, A. (1999a) Repression by Notch is required before Wingless signalling during muscle progenitor cell development in Drosophila. Curr Biol 9:707-710.
22. Brennan, K., Tateson, R., Lieber, T., Couso, J.P., Zecchini, V. and Martinez Arias, A. (1999b) The abruptex mutations of Notch disrupt the establishment of proneural clusters in Drosophila. Dev Biol 216:230-242.
23. Bresnick, A.R. (1999) Molecular mechanisms of nonmuscle myosin-II regulation. Curr Opin Cell Biol 11:26-33.
24. Brown, N.H. (1994) Null mutations in the αPS2 and βPS integrin subunit genes have distinct phenotypes. Development 120:1221-1231.
25. Brown, N.H., Gregory, S.L. and Martin-Bermudo, M.D. (2000) Integrins as mediators of morphogenesis in Drosophila. Dev Biol 223:1-16.
26. Brummel, T.J., Twombly, V., Marques, G., Wrana, J.L., Newfeld, S.J., Attisano, L., Massague, J., O'Connor, M.B. and Gelbart, WM. (1994) Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78:251-261.
27. Burbelo, P.D., Drechsel, D. and Hall, A. (1995) A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem 270:29071-29074.
28. Byars, C.L., Bates, K.L. and Letsou, A. (1999) The dorsal-open group gene raw is required for restricted DJNK signaling during closure. Development 126:4913-4923.
29. Campos-Ortega, J.A. and Hartenstein, V. (1985) The Embryonic Development of Drosophila melanogaster. Springer-Verlag, Berlin.
30. Chávez, V.M., Marqués, G., Delbecque, J.P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J.E. and O'Connor, M.B. (2000) The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 127:4115-4126.
31. Chen, H.W., Marinissen, M.J., Oh, S.W., Chen, X., Melnick, M., Perrimon, N., Gutkind, J.S. and Hou, S.X. (2002) CKA, a novel multidomain protein, regulates the JUN N-terminal kinase signal transduction pathway in Drosophila. Mol Cell Biol 22:1792-1803.
32. Chen, Y., Riese, M.J., Killinger, M.A. and Hoffmann, F.M. (1998) A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 125:1759-1768.
33. Childs, S.R., Wrana, J.L., Arora, K., Attisano, L., O'Connor, M.B. and Massagué, J. (1993) Identification of a Drosophila activin receptor. Proc Natl Acad Sci USA 90:9475-9479.
34. Cooley, L., Verheyen, E. and Ayers, K. (1992) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69:173-184.
35. Coso, O.A., Chiariello, M., Yu, J.C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, J.S. (1995) The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137-1146.
36. Dai, H., Hogan, C., Gopalakrishnan, B., Torres-Vazquez, J., Nguyen, M., Park, S., Raftery, L.A., Warrior, R. and Arora, K. (2000) The zinc finger protein Schnurri acts as a Smad partner in mediating the transcriptional response to Decapentaplegic. Dev Biol 227:373-387.
37. Dan, I., Watanabe, N.M. and Kusumi, A. (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11:220-230.
38. Dong, L.Q., Landa, L.R., Wick, M.J., Zhu, L., Mukai, H., Ono, Y. and Liu, F. (2000) Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc Natl Acad Sci USA 97:5089-5094.
39. Erickson, M.R., Galletta, B.J. and Abmayr, S.M. (1997) Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J Cell Biol 138:589-603.
40. Fehon, R.G., Johansen, K., Rebay, I. and Artavanis-Tsakonas, S. (1991) Complex cellular and subcellular regulation of Notch expression during embryonic and imaginal development of Drosophila: implications for Notch function. J Cell Biol 113:657-669.
41. Fehon, R.G., Dawson, I.A. and Artavanis-Tsakonas, S. (1994) A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120:545-557.
42. Fernandez, R., Tabarini, D., Azpiazu, N., Frasch, M. and Schlessinger, J. (1995) The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J 14:3373-3384.
43. Fernandez, R., Takahashi, F., Liu, Z., Steward, R., Stein, D. and Stanley, E.R. (2000) The Drosophila Shark tyrosine kinase is required for embryonic dorsal closure. Genes Dev 14:604-614.
44. Frank, L.H. and Rushlow, C. (1996) A group of genes required for maintenance of the amnioserosa tissue in Drosophila. Development 122:1343-1352.
45. Genova, J.L., Jong, S., Camp, J.T. and Fehon, R.G. (2000) Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev Biol 221:181-194.
46. Glise, B., Bourbon, H. and Noselli, S. (1995) hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83:451-461.
47. Glise, B. and Noselli, S. (1997) Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev 11:1738-1747.
48. Goberdhan, D.C.I. and Wilson, C. (1998) JNK, cytoskeletal regulator and stress response kinase? A Drosophila perspective. Bioessays 20:1009-1019.
49. Goldstein, L.S. and Gunawardena, S. (2000) Flying through the Drosophila cytoskeletal genome. J Cell Biol 150:F63-F68.
50. Grevengoed, E.E., Loureiro, J.J., Jesse, T.L. and Peifer, M. (2001) Abelson kinase regulates epithelial morphogenesis in Drosophila. J Cell Biol 155:1185-1197.
51. Grieder, N.C., Nellen, D., Burke, R., Basler, K. and Affolter, M. (1995) schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 81:791-800.
52. Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L. and Dickson, B.J. (2002) Rac function and regulation during Drosophila development. Nature 416:438-442.
53. Halsell, S.R., Chu, B.I. and Kiehart, D.P. (2000) Genetic analysis demonstrates a direct link between Rho signaling and nonmuscle myosin function during Drosophila morphogenesis. Genetics 155:1253-1265.
54. Harden, N., Loh, H.Y., Chia, W. and Lim, L. (1995) A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila. Development 121:903-914.
55. Harden, N., Lee, J., Loh, H.Y., Ong, Y.M., Tan, I., Leung, T., Manser, E. and Lim, L. (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.
56. Harden, N., Ricos, M., Ong, Y.M., Chia, W. and 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.
57. Harden, N., Ricos, M., Yee, K., Sanny, J., Langmann, C., Yu, H., Chia, W. and Lim, L. (2002) Drac1 and Crumbs participate in amnioserosa morphogenesis during dorsal closure in Drosophila. J Cell Sci 115:2119-2129.
58. Harris, B.Z. and Lim, W.A. (2001) Mechanism and role of PDZ omains in signaling complex assembly. J Cell Sci 114:3219-3231.
59. Heitzler, P., Haenlin, M., Ramain, P., Calleja, M. and Simpson, P. (1996) A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics 143:1271-1286.
60. Herranz, H. and Morata, G. (2001) The functions of pannier during Drosophila embryogenesis. Development 128:4837-4846.
61. Hing, H., Xiao, J., Harden, N., Lim, L. and Zipursky, S.L. (1999) Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97:853-863.
62. Hou, X.S., Goldstein, E.S. and 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.
63. Hudson, J.B., Podos, S.D., Keith, K., Simpson, S.L. and Ferguson, E.L. (1998) The Drosophila Medea gene is required downstream of Dpp and encodes a functional homolog of human Smad4. Development 125:1407-1420.
64. Jacinto, A., Wood, W., Balayo, T., Turmaine, M., Martinez-Arias, A. and Martin, P. (2000) Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr Biol 10:1420-1426.
65. Jacinto, A. and Martin, P. (2001) Morphogenesis: unravelling the cell biology of hole closure. Curr Biol 11:R705-R707.
66. Jacinto, A., Martinez-Arias, A. and Martin, P. (2001) Mechanisms of epithelial fusion and repair. Nat Cell Biol 3:E117-E123.
67. Jackson, P.D. and Hoffmann, F.M. (1994) Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression. Dev Dyn 199:28-44.
68. Jasper, H., Benes, V., Schwager, C., Sauer, S., Clauder-Münster, S., Ansorge, W. and Bohmann, D. (2001) The genomic response of the Drosophila embryo to JNK signaling. Dev Cell 1:579-586.
69. Jürgens, G., Wieschaus, E., Nüsslein-Volhard, C. and Kluding, H. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster II. Zygotic loci on the third chromosome. Roux's Arch Dev Biol 193:283-295.
70. Kiehart, D.P. (1999) Wound healing: The power of the purse string. Curr Biol 9:R602-R605.
71. Kiehart, D.P., Galbraith, C.G., Edwards, K.A., Rickoll, W.L. and Montague, R.A. (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471-490.
72. Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T and Matsuda, M. (1998a) Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev 12:3331-3336.
73. Kiyokawa, E., Hashimoto, Y., Kurata, T., Sugimura, H. and Matsuda, M. (1998b) Evidence that DOCK180 up-regulates signals from the CrkII-p130(Cas) complex. J Biol Chem 273:24479-24484.
74. Knust, E. (1996) Drosophila morphogenesis: follow-my-leader in epithelia. Curr Biol 6:379-381.
75. Knust, E. (1997) Drosophila morphogenesis: movements behind the edge. Curr Biol 7:R558-R561.
76. Kockel, L., Zeitlinger, J., Staszewski, L.M., Mlodzik, M. and Bohmann, D. (1997) Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev 11:1748-1758.
77. Kockel, L., Homsy, J.G. and Bohmann, D. (2001) Drosophila AP-1: lessons from an invertebrate. Oncogene 20:2347-2364.
78. Kozma, R., Ahmed, S., Best, A. and Lim, L. (1995) The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 15:1942-1952.
79. Kuriyama, M., Harada, N., Kuroda, S., Yamamoto, T., Nakafuku, M., Iwamatsu, A., Yamamoto, D., Prasad, R., Croce, C., Canaani, E. and Kaibuchi, K. (1996) Identification of AF-6 and Canoe as putative targets for Ras. J Biol Chem 271:607-610.
80. Lamb, R.S., Ward, R.E., Schweizer, L. and Fehon, R.G. (1998) Drosophila Coracle, a member of the protein 4.1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol Biol Cell 9:3505-3519.
81. Lamka, M.L. and Lipshitz, H.D (1999) Role of the amnioserosa in germ band retraction of the Drosophila melanogaster embryo. Dev Biol 214:102-112.
82. Lanier, L.M. and Gertler, F.B. (2000) From Ab1 to actin: Ab1 tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10:80-87.
83. Lawrence, N., Langdon, T., Brennan, K. and Martinez Arias, A. (2001) Notch signaling targets the Wingless responsiveness of a Ubx visceral mesoderm enhancer in Drosophila. Curr Biol 11:375-385.
84. Letsou, A., Arora, K., Wrana, J.L., Simin, K., Twombly, V., Jamal, J., Staehling-Hampton, K., Hoffmann, F.M., Gelbart, W.M., Massague, J. and O'Connor, M.B. (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.
85. Lu, Y. and Settleman, J. (1999) The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev 13:1168-1180.
86. Magie, C.R., Meyer, M.R., Gorsuch, M.S. and Parkhurst, S.M. (1999) Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126:5353-5364.
87. Manfruelli, P., Arquier, N., Hanratty, W.P. and Sémériva, M. (1996) The tumor suppressor gene, lethal(2)giant larvae (1(2)g1), is required for cell shape change of epithelial cells during Drosophila development. Development 122:2283-2294.
88. Martín-Blanco, E. (1997) Regulation of cell differentiation by the Drosophila Jun kinase cascade. Curr Opin Genet Dev 7:666-671.
89. Martín-Blanco, E., Gampel, A., Ring, J., Virdee, K., Kirov, N., Tolkovsky, A.M. and Martinez-Arias, A. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12:557-570.
90. Martín-Blanco, E., Pastor-Pareja, J.C. and Garcia-Bellido, A. (2000) JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc Natl Acad Sci USA 97:7888-7893.
91. Martinez-Arias, A. (1993) Development and patterning of the larval epidermis of Drosophila. In: Bate, M. and Martinez-Arias, M. (eds) The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
92. Matsuo, T., Takahashi, K., Kondo, S., Kaibuchi, K. and Yamamoto, D. (1997) Regulation of cone cell formation by Canoe and Ras in the developing Drosophila eye. Development 124:2671-2680.
93. McEwen, D.G., Cox, R.T. and Peifer, M. (2000) The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning. Development 127:3607-3617.
94. Mihaly, J., Kockel, L., Gaengel, K., Weber, U., Bohmann, D. and Mlodzik, M. (2001) The role of the Drosophila TAK homologue dTAK during development. Mech Dev 102:67-79.
95. Minden, A., Lin, A., Claret, F.X., Abo, A. and Karin, M. (1995) Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
96. Miyamoto, H., Nihonmatsu, I., Kondo, S., Ueda, R., Togashi, S., Hirata, K., Ikegami, Y. and Yamamoto, D. (1995) canoe encodes a novel protein containing a GLGF/DHR motif and functions with Notch and scabrous in common developmental pathways in Drosophila. Genes Dev 9:612-625.
97. Mizuno, T., Amano, M., Kaibuchi, K. and Nishida, Y. (1999) Identification and characterization of Drosophila homolog of Rho-kinase. Gene 238:437-444.
98. Mizuno, T., Tsutsui, K. and Nishida, Y. (2002) Drosophila myosin phosphatase and its role in dorsal closure. Development 129:1215-1223.
99. Morisato, D. and Anderson, K.V. (1995) Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet 29:371-399.
100. Mueller, B.K. (1999) Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci 22:351-388.
101. Nellen, D., Affolter, M. and Basler, K. (1994) Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78:225-237.
102. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B.J. and Luo, L. (2002) Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
103. Nobes, C.D. and Hall, A. (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
104. Nolan, K.M., Barrett, K., Lu, Y., Hu, K.Q., Vincent, S. and Settleman, J. (1998) Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes., Genes Dev 12:3337-3342.
105. Noselli, S. (1998) JNK signaling and morphogenesis in Drosophila. Trends Genet 14:33-38.
106. Noselli, S. and Agnès, F. (1999) Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr Opin Genet Dev 9:466-472.
107. Ntwasa, M., Aapies, S., Schiffmann, D.A. and Gay, N.J. (2001) Drosophila embryos lacking N-myristoyltransferase have multiple developmental defects. Exp Cell Res 262:134-144.
108. Nüsslein-Volhard, C., Wieschaus, E. and 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.
109. Ohshiro, T., Yagami, T., Zhang, C. and Matsuzaki, F. (2000) Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature 408:593-596.
110. Peng, C.Y., Manning, L., Albertson, R. and Doe, C.Q. (2000) The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408:596-600.
111. Penton, A., Chen, Y., Staehling-Hampton, K., Wrana, J.L., Attisano, L., Szidonya, J., Cassill, J.A., Massague, J. and Hoffmann, EM. (1994) Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a Decapentaplegic receptor. Cell 78:239-250.
112. Perrimon, N. (1988) The maternal effect of lethal(1)discs-large-1: a recessive oncogene of Drosophila melanogaster. Dev Biol 127:392-407.
113. Perrimon, N., Engstrom, L. and Mahowald, A.P. (1989) Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121:333-352.
114. Pirone, D.M., Carter, D.E. and Burbelo, P.D. (2001) Evolutionary expansion of CRIB-containing Cdc42 effector proteins. Trends Genet 17:370-373.
115. Raabe, T. (2000) The Sevenless signaling pathway: variations of a common theme. Biochim Biophys Acta 1496:151-163.
116. Rämet, M., Lanot, R., Zachary, D. and Manfruelli, P. (2002) JNK Signaling Pathway Is Required for Efficient Wound Healing in Drosophila. Dev Biol 241:145-156.
117. Raymond, K., Bergeret, E., Dagher, M.C., Breton, R., Griffin-Shea, R. and Fauvarque, M.O. (2001) The Rac GTPase-activating protein RotundRacGAP interferes with Drac1 and Dcdc42 signalling in Drosophila melanogaster. J Biol Chem 276:35909-35916.
118. Rebay, I. and Rubin, G.M. (1995) Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81:857-866.
119. Reed, B.H., Wilk, R. and Lipshitz, H.D. (2001) Downregulation of Jun kinase signaling in the amnioserosa is essential for dorsal closure of the Drosophila embryo. Curr Biol 11:1098-1108.
120. Ricos, M.G., Harden, N., Sem, K.P., Lim, L. and Chia, W. (1999) Dcdc42 acts in TGF-β signaling during Drosophila morphogenesis: distinct roles for the Dracl/JNK and Dcdc42/TGF-β cascades in cytoskeletal regulation. J Cell Sci 112:1225-1235.
121. Riesgo-Escovar, J.R., Jenni, M., Fritz, A. and Hafen, E. (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10:2759-2768.
122. Riesgo-Escovar, J.R. and Hafen, E. (1997a) 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.
123. Riesgo-Escovar, J.R. and Hafen, E. (1997b) Common and distinct roles of DFos and DJun during Drosophila development. Science 278:669-672.
124. Ring, J.M. and Martinez Arias, A. (1993)puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Development (Suppl):251-259.
125. Roy, P.J., Zheng, H., Warren, C.E. and Culotti, J.G. (2000) mab-20 encodes Semaphorin-2a and is required to prevent ectopic cell contacts during epidermal morphogenesis in Caenorhabditis elegans. Development 127:755-767.
126. Ruberte, E., Marty, T., Nellen, D., Affolter, M. and 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.
127. Rugendorff, A., Younossi-Hartenstein, A. and Hartenstein, V. (1994) Embryonic origin and differentiation of the Drosophila heart. Roux's Arch Dev Biol 203:266-280.
128. Sawamoto, K., Winge, P., Koyama, S., Hirota, Y., Yamada, C., Miyao, S., Yoshikawa, S., Jin, M.H., Kikuchi, A. and Okano, H. (1999) The Drosophila Ra1 GTPase regulates developmental cell shape changes through the Jun NH(2) -terminal kinase pathway. J Cell Biol 146:361-372.
129. Shirakabe, K., Yamaguchi, K., Shibuya, H., Irie, K., Matsuda, S., Moriguchi, T., Gotoh, Y., Matsumoto, K. and Nishida, E. (1997) TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J Biol Chem 272:8141-8144.
130. Simin, K., Bates, E.A., Horner, M.A. and Letsou, A. (1998) Genetic analysis of punt, a type II Dpp receptor that functions throughout the Drosophila melanogaster life cycle. Genetics 148:801-813.
131. Simske, J.S. and Hardin, J. (2001) Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. Bioessays 23:12-23.
132. Sluss, H.K., Han, Z., Barrett, T., Davis, R.J. and Ip, Y.T. (1996) A INK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev 10:2745-2758.
133. Sluss, H.K. and Davis, R.J. (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.
134. Small, J.V., Rottner, K. and Kaverina, I. (1999) Functional design in the actin cytoskeleton. Curr Opin Cell Biol 11:54-60.
135. Snow, P.M., Bieber, A.J. and Goodman, C.S. (1989) Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell 59:313-323.
136. St. Johnston, R.D. and Gelbart, W.M. (1987) Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6:2785-2791.
137. Staehling-Hampton, K., Laughon, A.S. and Hoffmann, F.M. (1995) A Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development 121:3393-3403.
138. Stark, K.A., Yee, G.H., Roote, C.E., Williams, E.L., Zusman, S. and Hynes, R.O. (1997) A novel alpha integrin subunit associates with βPS and functions in tissue morphogenesis and movement during Drosophila development. Development 124:4583-4594.
139. Strand, D., Jakobs, R., Merdes, G., Neumann, B., Kalmes, A., Heid, H.W., Husmann, I. and Mechler, B.M. (1994a) The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J Cell Biol 127:1361-1373.
140. Strand, D., Raska, I. and Mechler, B.M. (1994b) The Drosophila lethal(2)giant larvae tumor suppressor protein is a component of the cytoskeleton. J Cell Biol 127:1345-1360.
141. Strecker, TR., Li, P., McGhee, S.A., Ham, D., Smith, S.K., Schreck, J.A., Youn, S.J. and Kon, P.S-H. (1995) The effects of the glucocorticoid, dexamethasone, on the development of the Drosophila embryo. Roux's Arch Dev Biol 204:359-368.
142. Stronach, B.E. and Perrimon, N. (2001) Investigation of leading edge formation at the interface of amnioserosa and dorsal ectoderm in the Drosophila embryo. Development 128:2905-2913.
143. Stronach, B. and Perrimon, N. (2002) Activation of the JNK pathway during dorsal closure in Drosophila requires the mixed lineage kinase, slipper. Genes Dev 16:377-387.
144. Strutt, D.I., Weber, U. and Mlodzik, M. (1997) The role of RhoA in tissue polarity and Frizzled signalling. Nature 387:292-295.
145. Su, Y.C., Han, J., Xu, S., Cobb, M. and Skolnik, E.Y. (1997) NIK is a new Ste20-related kinase that binds NCK and MEKK1 and activates the SAPK/JNK cascade via a conserved regulatory domain. EMBO J 16:1279-1290.
146. Su, Y.C., Treisman, J.E. and Skolnik, E.Y. (1998) The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev 12:2371-2380.
147. Su, Y.C., Maurel-Zaffran, C., Treisman, J.E. and Skolnik, E.Y. (2000) The Ste20 kinase Misshapen regulates both photoreceptor axon targeting and dorsal closure, acting downstream of distinct signals. Mol Cell Biol 20:4736-4744.
148. Sugimura, I., Adachi-Yamada, T., Nishi, Y. and Nishida, Y. (2000) A Drosophila Winged-helix nude (Whn)-like transcription factor with essential functions throughout development. Dev Growth Differ 42:237-248.
149. Takahashi, K., Matsuo, T., Katsube, T., Ueda, R. and Yamamoto, D (1998) Direct binding between two PDZ domain proteins Canoe and ZO-1 and their roles in regulation of the jun N-terminal kinase pathway in Drosophila morphogenesis. Mech Dev 78:97-111.
150. Takahisa, M., Togashi, S., Suzuki, T., Kobayashi, M., Murayama, A., Kondo, K., Miyake, T. and Ueda, R. (1996) The Drosophila tamou gene, a component of the activating pathway of extramacrochaetae expression, encodes a protein homologous to mammalian cell-cell junction-associated protein ZO-1. Genes Dev 10:1783-1795.
151. Takatsu, Y., Nakamura, M., Stapleton, M., Danos, M.C, Matsumoto, K., O'Connor, M.B., Shibuya, H. and Ueno, N. (2000) TAK1 participates in c-Jun N-terminal kinase signaling during Drosophila development. Mol Cell Biol 20:3015-3026.
152. Takenawa, T. and Miki, H. (2001) WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114:1801-1809.
153. Tal, T., Vaizel-Ohayon, D. and Schejter, E.D. (2002) Conserved interactions with cytoskeletal but not signaling elements are an essential aspect of Drosophila Wasp function. Dev Biol 243:260-271.
154. Tateno, M., Nishida, Y. and Adachi-Yamada, T. (2000) Regulation of JNK by Src during Drosophila development. Science 287:324-327.
155. Tepass, U., Theres, C. and Knust, E. (1990) crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61:787-799.
156. Tepass, U. and Hartenstein, V. (1994) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563-596.
157. Tepass, U., Gruszynski-DeFeo, E., Haag, T.A., Omatyar, L., Torok, T. and Hartenstein, V. (1996) shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10:672-685.
158. Tepass, U., Tanentzapf, G., Ward, R. and Fehon, R. (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747-784.
159. Teramoto, H., Coso, O.A., Miyata, H., Igishi, T., Miki, T. and Gutkind, J.S. (1996) Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J Biol Chem 271:27225-27228.
160. Udagawa, Y., Hanai, J., Tada, K., Grieder, N.C., Momoeda, M., Taketani, Y., Affolter, M., Kawabata, M. and Miyazono, K. (2000) Schnurri interacts with Mad in a Dpp-dependent manner. Genes Cells 5:359-369.
161. Uemura, T., Oda, H., Kraut, R., Hayashi, S., Kotaoka, Y. and Takeichi, M. (1996) Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 10:659-671.
162. Van Aelst, L. and D'Souza-Schorey, C. (1997) Rho GTPases and signaling networks. Genes Dev 11:2295-2322.
163. Vasioukhin, V. and Fuchs, E. (2001) Actin dynamics and cell-cell adhesion in epithelia. Curr Opin Cell Biol 13:76-84.
164. Vidal, S., Khush, R.S., Leulier, F., Tzou, P., Nakamura, M. and Lemaitre, B. (2001) Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/ NF-κB-dependent innate immune responses. Genes Dev 15:1900-1912.
165. Ward, R.E., Lamb, R.S. and Fehon, R.G. (1998) A conserved functional domain of Drosophila Coracle is required for localization at the septate junction and has membrane-organizing activity. J Cell Biol 140:1463-1473.
166. Watanabe, G., Saito, Y., Madaule, P., Ishizaki, T., Fujisawa, K., Morii, N., Mukai, H., Ono, Y., Kakizuka, A. and Narumiya, S. (1996) Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho. Science 271:645-648.
167. Wear, M.A., Schafer, D.A. and Cooper, J.A. (2000) Actin dynamics: assembly and disassembly of actin networks. Curr Biol 10:R891-R895.
168. Wei, X. and Ellis, H.M. (2001) Localization of the Drosophila MAGUK protein Polychaetoid is controlled by alternative splicing. Mech Dev 100:217-231.
169. Widmann, C., Gibson, S., Jarpe, M.B. and Johnson, G.L. (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180.
170. Wieschaus, E., Nüsslein-Volhard, C. and Jürgens, G. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster III. Zygotic loci on the X-chromosome and the fourth chromosome. Roux's Arch Dev Biol 193:296-307.
171. Winter, C.G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J.D. and Luo, L. (2001) Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105:81-91.
172. Wodarz, A., Hinz, U., Engelbert, M. and Knust, E. (1995) Expression of Crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82:67-76.
173. Wodarz, A. and Nusse, R. (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14:59-88.
174. Wolthuis, R.M. and Bos, J.L. (1999) Ras caught in another affair: the exchange factors for Ra1. Curr Opin Genet Dev 9:112-117.
175. Woods, D.F. and Bryant, P.J. (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451-464.
176. Woods, D.F. and Bryant, P.J. (1993) Apical junctions and cell signalling in epithelia. J Cell Sci 17(Suppl):171-181.
177. Woods, D.F., Hough, C., Peel, D., Callaini, G. and Bryant, P.J. (1996) Dig protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134:1469-1482.
178. Woods, D.F., Wu, J.W and Bryant, R.J. (1997) Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Dev Genet 20:111-118.
179. Young, P.E., Richman, A.M., Ketchum, A.S. and Kiehart, D.P. (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7:29-41.
180. Zallen, J.A., Cohen, Y., Hudson, A.M., Cooley, L., Wieschaus, E. and Schetjer, E.D. (2002) SCAR is a primary regulator of Arp2/ 3-dependent morphological events in Drosophila. J Cell Biol 156:689-701.
181. Zecchini, V., Brennan, K. and Martinez-Arias, A. (1999) An activity of Notch regulates JNK signalling and affects dorsal closure in Drosophila. Curr Biol 9:460-469.
182. Zeitlinger, J., Kockel, L., Peverali, F.A., Jackson, D.B., Mlodzik, M. and Bohmann, D. (1997) Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophila fos mutants. EMBO J 16:7393-7401.
183. Zeitlinger, J. and Bohmann, D. (1999) Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126:3947-3956.
184. Zohn, I.M., Campbell, S.L., Khosravi-Far, R., Rossman, K.L. and Der, C.J. (1998) Rho family proteins and Ras transformation: the RHOad less traveled gets congested. Oncogene 17:1415-1438.