JNK signalling influences intracellular trafficking during Drosophila morphogenesis through regulation of the novel target gene Rab30

Developmental Biology

Volumn 331, Issue 2, 2009, Pages 250-260

  Thomas, Chloe ^a   Rousset, Raphaël ^a   Noselli, Stéphane ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Dorsal closure; Drosophila; Head involution; Intracellular trafficking; Jun N terminal kinase; Morphogenesis; Rab GTPase; Thorax closure

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; RAB PROTEIN; RAB30 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; GENETIC TRANSCRIPTION; HEAD; IMMUNOFLUORESCENCE; INTRACELLULAR TRANSPORT; INVOLUTION; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; THORAX; TRANS GOLGI NETWORK; UPREGULATION;

EID: 67549103673     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.05.001     Document Type: Article

References (50)

1. Agnés F., Suzanne M., and Noselli S. The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126 (1999) 5453-5462
2. Bloor J.W., and Kiehart D.P. Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129 (2002) 3173-3183
3. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
4. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., and Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70 (1992) 715-728
5. Chen D., Guo J., Miki T., Tachibana M., and Gahl W.A. Molecular cloning of two novel rab genes from human melanocytes. Gene 174 (1996) 129-134
6. de Leeuw H.P.J.C., Koster P.M., Calafat J., Janssen H., van Zonneveld A.-J., van Mourik J.A., and Voorberg J. Small GTP-binding proteins in human endothelial cells. B. J. Haematol. 103 (1998) 15-19
7. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., and Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448 (2007) 151-156
8. Friggi-Grelin F., Rabouille C., and Therond P. The cis-Golgi Drosophila GMAP has a role in anterograde transport and Golgi organization in vivo, similar to its mammalian ortholog in tissue culture cells. Eur. J. Cell Biol. 85 (2006) 1155-1166
9. Genova J.L., Jong S., Camp J.T., and Fehon R.G. Functional analysis of cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev. Biol. 221 (2000) 181-194
10. Glise B., and Noselli S. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11 (1997) 1738-1747
11. Glise B., Bourbon H., and Noselli S. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83 (1995) 451-461
12. Gorvel J.P., Chavrier P., Zerial M., and Gruenberg J. Rab5 controls early endosome fusion in vitro. Cell 64 (1991) 915-925
13. Grigoriev I., Splinter D., Keijzer N., Wulf P.S., Demmers J., Ohtsuka T., Modesti M., Maly I.V., Grosveld F., Hoogenraad C.C., and Akhmanova A. Rab6 regulates transport and targeting of exocytotic carriers. Dev. Cell 13 (2007) 305-314
14. Haas A.K., Yoshimura S., Stephens D.J., Preisinger G., Fuchs E., and Barr F.A. Analysis of GFPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J. Cell Sci. 120 (2007) 2997-3010
15. Hutson M.S., Tokutake Y., Chang M.S., Bloor J.W., Venakides S., Kiehart D.P., and Edwards G.S. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300 (2003) 145-149
16. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., and Speed T.P. Summaries of Affymetric GeneChip probe level data. Nucleic Acids Rev. 31 (2003) e15
17. Jankovics F., and Brunner D. Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster. Dev. Cell 11 (2006) 1-11
18. Jasper H., Benes V., Schwager C., Sauer S., Clauder-Münster S., Ansorge W., and Bohmann D. The genomic response of the Drosophila embryo to JNK signaling. Dev. Cell 1 (2001) 579-586
19. Kennerdell J.R., and Carthew R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled2 act in the wingless pathway. Cell 95 (1998) 1017-1026
20. Kiehart D.P., Galbraith C.G., Edwards K.A., Rickoll W.L., and Montague R.A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149 (2000) 471-490
21. Lui R., Woolner S., Johndrow J.E., Metzger D., Flores A., and Parkhurst S.M. Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135 (2008) 53-63
22. McLauchlan H., Newell J., Morrice N., Osborne A., West M., and Smythe E. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8 (1998) 34-45
23. Martin P., and Parkhurst S.M. Parallels between tissue repair and embryo morphogenesis. Development 131 (2004) 3021-3034
24. Martin P., and Wood W. Epithelial fusions in the embryo. Curr. Opin. Cell Biol. 14 (2002) 569-574
25. Martín-Blanco E., Gampel A., Ring J., Virdee K., Kirov N., Tolkovsky A.M., and Martínez-Arias A. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12 (1998) 557-570
26. Martín-Blanco E., Pastor-Pareja J.C., and García-Bellido A. JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7888-7893
27. Misquetta L., and Paterson B.M. Targeted disruption of gene function in Drosophila by RNA interference. In: Sullivan W., et al. (Eds). Drosophila Protocols (2000), Cold Spring Harbor Laboratory Press
28. Pastor-Pareja J.C., Grawe F., Martín-Blanco E., and García-Bellido A. Invasive cell behaviour during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev. Cell 7 (2004) 387-399
29. Pereira-Leal J.B., and Seabra M.C. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313 (2001) 889-901
30. Reichhart J.M., Liqoxyqakis P., Naitza S., Woerfel G., Imler J.L., and Gubb D. Splice-activated UAS hairpin vector gives complete RNAi knockout of single or double target transcripts in Drosophila melanogaster. Genesis 34 (2002) 160-164
31. Riesgo-Escovar J.R., Jenni M., Fritz A., and Hafen E. 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 (1996) 2759-2768
32. Ring J.M., and Martínez-Arias A. puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Dev. Suppl. (1993) 251-259
33. Rousset R., Almeida L., and Noselli S. Drosophila morphogenesis: the Newtonian revolution. Curr. Biol. 13 (2003) R494-R495
34. Satoh A.K., O'Tousa J.E., Ozaki K., and Ready D.F. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132 (2005) 1487-1497
35. Seabra M.C., and Wasmeier C. Controlling the location and activation of Rab GTPases. Curr. Opin. Cell Biol. 16 (2004) 451-457
36. Sherwood N.T., Sun Q., Xue M., Zhang B., and Zinn K. Drosophila Spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2 (2004) e429
37. Sinka R., Gillingham A.K., Kondylis V., and Munro S. Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins. J. Cell Biol. 183 (2008) 607-615
38. Sluss H.K., Han Z., Barrett T., Davis R.J., and Ip Y.T. A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10 (1996) 2745-2758
39. Sönnichsen B., de Renzisa S., Nielsena E., Rietdorfb J., and Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149 (2000) 901-913
40. Stronach B., and Perrimon N. Activation of the JNK pathway during dorsal closure in Drosophila requires the mixed lineage kinase, Slipper. Genes Dev. 16 (2002) 377-387
41. Tepass U., Gruszynski-DeFeo E., Haag T.A., Omatyar L., Török T., and Hartenstein V. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10 (1996) 672-685
42. Uemura T., Oda H., Kraut R., Hayashi S., Kataoka Y., and Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10 (1996) 659-671
43. Ullrich O., Reinsch S., Urbé M., Zerial M., and Parton R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135 (1996) 913-924
44. VanHook A., and Letsou A. Head involution in Drosophila: genetic and morphogenetic connections to dorsal closure. Dev. Dyn. 237 (2008) 28-38
45. Wieschaus E., and Nusslein-Volhard C. Looking at embryos. In: Roberts D.M. (Ed). Drosophila: A Practical Approach (1986), IRL Press Ltd, Oxford 199-227
46. Wilke M., Johannes L., Galli T., Mayau V., Goud B., and Salamero J. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151 (2000) 1207-1220
47. Xia Y., and Karin M. The control of cell motility and epithelial morphogenesis by JNK kinases. Trends Cell Biol. 14 (2004) 94-101
48. Zeitlinger J., and Bohmann D. Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126 (1999) 3947-3956
49. Zerial M., and McBride H. Rab proteins as membrane organisers. Nat. Rev. Mol. Cell Biol. 2 (2001) 107-117
50. Zhang J., Schulze K.L., Hiesinger P.R., Suyama K., Wang S., Fish M., Acar M., Hoskins R.A., Bellen H.J., and Scott M.P. Thirty-one flavors of Drosophila rab proteins. Genetics 176 (2007) 1307-1322