The guanine exchange factor vav controls axon growth and guidance during Drosophila development

Journal of Neuroscience

Volumn 30, Issue 6, 2010, Pages 2257-2267

  Malartre, Marianne ^a   Ayaz, Derya ^b   Amador, Fatima Fernandez ^a   Martín Bermudo, Maria Dolores ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

RAC PROTEIN; VAV PROTEIN;

ALLELE; ANIMAL CELL; ARTICLE; BRAIN; BRAIN REGION; CONTROLLED STUDY; CYTOSKELETON; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EYE; LARVAL DEVELOPMENT; LOCOMOTION; MODULATION; MUTANT; NERVE FIBER GROWTH; NONHUMAN; OPTIC LOBE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ANIMALS; AXONS; BODY PATTERNING; CELL DIFFERENTIATION; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; DROSOPHILA; LARVA; MUTATION; NEUROGLIA; PHOTORECEPTOR CELLS, INVERTEBRATE; PROTO-ONCOGENE PROTEINS C-VAV;

EID: 76649109555     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1820-09.2010     Document Type: Article

References (50)

1. Aoki K, Nakamura T, Fujikawa K, Matsuda M (2005) Local phosphatidylinositol 3,4,5-trisphosphate accumulation recruits Vav2 and Vav3 to activate Rac1/Cdc42 and initiate neurite outgrowth in nerve growth factor-stimulated PC12 cells. Mol Biol Cell 16:2207-2217.
2. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, Ito K, Hama C (2000) The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26:119-131.
3. Bateman J, Shu H, Van Vactor D (2000) The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 26:93-106.
4. Betz R, Sandhoff K, Fischer KD, van Echten-Deckert G (2003) Detection and identification of Vav1 protein in primary cultured murine cerebellar neurons and in neuroblastoma cells (SH-SY5Y and Neuro-2a). Neurosci Lett 339:37-40.
5. Boquet I, Hitier R, Dumas M, Chaminade M, Préat T (2000a) Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. J Neurobiol 42:33-48.
6. Boquet I, Boujemaa R, Carlier MF, Préat T (2000b) Ciboulot regulates actin assembly during Drosophila brain metamorphosis. Cell 102:797-808.
7. Boyle M, Nighorn A, Thomas JB (2006) Drosophila Eph receptor guides specific axon branches of mushroom body neurons. Development 133:1845-1854.
8. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
9. Bustelo XR (2000) Regulatory and signaling properties of the Vav family. Mol Cell Biol 20:1461-1477.
10. Chauvet N, Prieto M, Fabre C, Noren NK, Privat A (2003) Distribution of p120 catenin during rat brain development: potential role in regulation of cadherin-mediated adhesion and actin cytoskeleton organization. Mol Cell Neurosci 22:467-486.
11. Clandinin TR, Zipursky SL (2002) Making connections in the fly visual system. Neuron 35:827-841.
12. Couceiro JR, Martín-Bermudo MD, Bustelo XR (2005) Phylogenetic conservation of the regulatory and functional properties of the Vav oncoprotein family. Exp Cell Res 308:364-380.
13. Cowan CW, Shao YR, Sahin M, Shamah SM, Lin MZ, Greer PL, Gao S, Griffith EC, Brugge JS, Greenberg ME (2005) Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 46:205-217.
14. Crowner D, Madden K, Goeke S, Giniger E (2002) Lola regulates midline crossing of CNS axons in Drosophila. Development 129:1317-1325.
15. Dekel I, Russek N, Jones T, Mortin MA, Katzav S (2000) Identification of the Drosophila melanogaster homologue of the mammalian signal transducer protein, Vav. FEBS Lett 472:99-104.
16. Forsthoefel DJ, Liebl EC, Kolodziej PA, Seeger MA (2005) The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132:1983-1994.
17. Fritz JL, VanBerkum MF (2000) Calmodulin and Son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS. Development 127:1991-2000.
18. Fujikawa K, Miletic AV, Alt FW, Faccio R, Brown T, Hoog J, Fredericks J, Nishi S, Mildiner S, Moores SL, Brugge J, Rosen FS, Swat W (2003) Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med 198:1595-1608.
19. Garrity PA, Rao Y, Salecker I, McGlade J, Pawson T, Zipursky SL (1996) Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85:639-650.
20. Garrity PA, Lee CH, Salecker I, Robertson HC, Desai CJ, Zinn K, Zipursky SL (1999) Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22:707-717.
21. Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45-57.
22. Hakeda-Suzuki S, Ng J, Tzu J, Dietzl G, Sun Y, Harms M, Nardine T, Luo L, Dickson BJ (2002) Rac function and regulation during Drosophila development. Nature 416:438-442.
23. Hing H, Xiao J, Harden N, Lim L, Zipursky SL (1999) Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97:853-863.
24. Hornstein I, Mortin MA, Katzav S (2003) DroVav, the Drosophila melanogaster homologue of the mammalian Vav proteins, serves as a signal transducer protein in the Rac and DER pathways. Oncogene 22:6774-6784.
25. Hu H, Li M, Labrador JP, McEwen J, Lai EC, Goodman CS, Bashaw GJ (2005) Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc Natl Acad Sci U S A 102:4613- 4618.
26. Klämbt C, Jacobs JR, Goodman CS (1991) The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64:801-815.
27. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
28. Linseman DA, Loucks FA (2008) Diverse roles of Rho family GTPases in neuronal development, survival, and death. Front Biosci 13:657-676.
29. Mast JD, Prakash S, Chen PL, Clandinin TR (2006) The mechanisms and molecules that connect photoreceptor axons to their targets in Drosophila. Semin Cell Dev Biol 17:42-49.
30. Movilla N, Bustelo XR (1999) Biological and regulatory properties of Vav-3, a new member of the Vav family of oncoproteins. Mol Cell Biol 19:7870-7885.
31. Murata T, Ohnishi H, Okazawa H, Murata Y, Kusakari S, Hayashi Y, Miyashita M, Itoh H, Oldenborg PA, Furuya N, Matozaki T (2006) CD47 promotes neuronal development through Src- and FRG/Vav2-mediated activation of Rac and Cdc42. J Neurosci 26:12397-12407.
32. Newsome TP, Schmidt S, Dietzl G, Keleman K, Asling B, Debant A, Dickson BJ (2000) Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101:283-294.
33. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L (2002) Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
34. Noordermeer JN, Kopczynski CC, Fetter RD, Bland KS, Chen WY, Goodman CS (1998) Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21:991-1001.
35. Pascual A, Huang KL, Neveu J, Préat (2004) Neuroanatomy: brain asymmetry and long-term memory. Nature 427:605-606.
36. Perrimon N (1984) Clonal analysis of dominant female-sterile, germline-dependent mutations in Drosophila melanogaster. Genetics 108:927-939.
37. Poeck B, Fischer S, Gunning D, Zipursky SL, Salecker I (2001) Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29:99-113.
38. Reinke R, Krantz DE, Yen D, Zipursky SL (1988) Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52:291-301.
39. Renn SC, Armstrong JD, Yang M, Wang Z, An X, Kaiser K, Taghert PH (1999) Genetic analysis of the Drosophila ellipsoid body neutrophil: organization and development of the central complex. J Neurobiol 41:189-207.
40. Schmid A, Chiba A, Doe CQ (1999) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653-4689.
41. Schmid RS, Midkiff BR, Kedar VP, Maness PF (2004) Adhesion molecule L1 stimulates neuronal migration through Vav2-Pak1 signaling. Neuroreport 15:2791-2794.
42. Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409-426.
43. Stemerdink C, Jacobs JR (1997) Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos. Development 124:3787-3796.
44. Strauss R (2002) The central complex and the genetic dissection of locomotor behavior. Curr Opin Neurobiol 12:633-638.
45. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852-1861.
46. Suh GS, Poeck B, Chouard T, Oron E, Segal D, Chamovitz DA, Zipursky SL (2002) Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33:35-46.
47. Turner M, Billadeau DD (2002) VAV proteins as signal integrators for multisubunit immune-recognition receptors. Nat Rev Immunol 2:476-486.
48. Wu JS, Luo L (2006) A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nat Protoc 1:2583-2589.
49. Xiong WC, Okano H, Patel NH, Blendy JA, Montell C (1994) repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8:981-994.
50. Yang L, Bashaw GJ (2006) Son of sevenless directly links the Robo receptor to rac activation to control axon repulsion at the midline. Neuron 52:595-607.