Drosophila cortex and neuropile glia influence secondary axon tract growth, pathfinding, and fasciculation in the developing larval brain

Developmental Biology

Volumn 334, Issue 2, 2009, Pages 355-368

  Spindler, Shana R ^a   Ortiz, Irma ^a   Fung, Siaumin ^a   Takashima, Shigeo ^a   Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; Drosophila; Glia; Lineage

Indexed keywords

BRAIN PROTEIN; NIRVANA2 PROTEIN; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; ELECTRON MICROSCOPY; GLIA; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LARVA; NERVE FIBER GROWTH; NEUROBLAST; NEUROPIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

EID: 70349296750     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.07.035     Document Type: Article

References (52)

1. Ashburner M. A Laboratory Handbook (1989), Cold Spring Harbor Laboratory Press
2. Bach E.A., Ekas L.A., Ayala-Camargo A., Flaherty M.S., Lee H., Perrimon N., and Baeg G.H. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns 7 (2007) 323-331
3. Bainton R.J., Tsai L.T., Schwabe T., DeSalvo M., Gaul U., and Heberlein U. moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123 (2005) 145-156
4. Bastiani M.J., and Goodman C.S. Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways. J. Neurosci. 6 (1986) 3542-3551
5. Baumann P.M., Oland L.A., and Tolbert L.P. Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta. J. Comp. Neurol. 373 (1996) 118-128
6. Bernardoni R., Vivancos V., and Giangrande A. glide/gcm is expressed and required in the scavenger cell lineage. Dev. Biol. 191 (1997) 118-130
7. Chen W., and Hing H. The L1-CAM, Neuroglian, functions in glial cells for Drosophila antennal lobe development. Dev. Neurobiol. 68 (2008) 1029-1045
8. Dumstrei K., Wang F., and Hartenstein V. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J. Neurosci. 23 (2003) 3325-3335
9. Ebens A.J., Garren H., Cheyette B.N., and Zipursky S.L. The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74 (1993) 15-27
10. Goodman C.S., and D. C. Embryonic Development of the Drosophila Central Nervous System (1993), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
11. Gorczyca M.G., Phillis R.W., and Budnik V. The role of tinman, a mesodermal cell fate gene, in axon pathfinding during the development of the transverse nerve in Drosophila. Development 120 (1994) 2143-2152
12. Hartenstein V., Nassif C., and Lekven A. Embryonic development of the Drosophila brain. II. Pattern of glial cells. J. Comp. Neurol. 402 (1998) 32-47
13. Hidalgo A., and Booth G.E. Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127 (2000) 393-402
14. Hidalgo A., Urban J., and Brand A.H. Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 121 (1995) 3703-3712
15. Hitier R., Simon A.F., Savarit F., and Preat T. no-bridge and linotte act jointly at the interhemispheric junction to build up the adult central brain of Drosophila melanogaster. Mech. Dev. 99 (2000) 93-100
16. Hortsch M., Patel N.H., Bieber A.J., Traquina Z.R., and Goodman C.S. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 110 (1990) 1327-1340
17. Hoyle G., Williams M., and Phillips C. Functional morphology of insect neuronal cell-surface/glial contacts: the trophospongium. J. Comp. Neurol. 246 (1986) 113-128
18. Ito K., and Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev. Biol. 149 (1992) 134-148
19. Ito K., Awano W., Suzuki K., Hiromi Y., and Yamamoto D. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124 (1997) 761-771
20. Jacobs J.R. Perturbed glial scaffold formation precedes axon tract malformation in Drosophila mutants. J. Neurobiol. 24 (1993) 611-626
21. Jacobs J.R., and Goodman C.S. Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J. Neurosci. 9 (1989) 2402-2411
22. Jefferis G.S., Vyas R.M., Berdnik D., Ramaekers A., Stocker R.F., Tanaka N.K., Ito K., and Luo L. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131 (2004) 117-130
23. Kidd T., Bland K.S., and Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96 (1999) 785-794
24. Klambt C., and Goodman C.S. Role of the midline glia and neurons in the formation of the axon commissures in the central nervous system of the Drosophila embryo. Ann. N.Y. Acad. Sci. 633 (1991) 142-159
25. Klambt C., Hummel T., Menne T., Sadlowski E., Scholz H., and Stollewerk A. Development and function of embryonic central nervous system glial cells in Drosophila. Dev. Genet. 18 (1996) 40-49
26. Kumar S., and Doumanis J. The fly caspases. Cell Death Differ. 7 (2000) 1039-1044
27. Lai S.L., Awasaki T., Ito K., and Lee T. Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135 (2008) 2883-2893
28. Laissue P.P., and Vosshall L.B. The olfactory sensory map in Drosophila. Adv. Exp. Med. Biol. 628 (2008) 102-114
29. Laissue P.P., Reiter C., Hiesinger P.R., Halter S., Fischbach K.F., and Stocker R.F. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405 (1999) 543-552
30. Nassif C., Noveen A., and Hartenstein V. Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. J. Comp. Neurol. 402 (1998) 10-31
31. Nassif C., Noveen A., and Hartenstein V. Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J. Comp. Neurol. 455 (2003) 417-434
32. Oland L.A., Biebelhausen J.P., and Tolbert L.P. Glial investment of the adult and developing antennal lobe of Drosophila. J. Comp. Neurol. 509 (2008) 526-550
33. Pereanu W., and Hartenstein V. Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 26 (2006) 5534-5553
34. Pereanu W., Shy D., and Hartenstein V. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev. Biol. 283 (2005) 191-203
35. Pereanu W., Spindler S., Cruz L., and Hartenstein V. Tracheal development in the Drosophila brain is constrained by glial cells. Dev. Biol. 302 (2007) 169-180
36. Pereanu W., Spindler S., Im E., Buu N., and Hartenstein V. The emergence of patterned movement during late embryogenesis of Drosophila. Dev. Neurobiol. 67 (2007) 1669-1685
37. Rossler W., Oland L.A., Higgins M.R., Hildebrand J.G., and Tolbert L.P. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J. Neurosci. 19 (1999) 9865-9877
38. Schwabe T., Bainton R.J., Fetter R.D., Heberlein U., and Gaul U. GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123 (2005) 133-144
39. Sepp K.J., Schulte J., and Auld V.J. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol. 238 (2001) 47-63
40. Sonnenfeld M.J., and Jacobs J.R. Apoptosis of the midline glia during Drosophila embryogenesis: a correlation with axon contact. Development 121 (1995) 569-578
41. Stork T., Engelen D., Krudewig A., Silies M., Bainton R.J., and Klambt C. Organization and function of the blood-brain barrier in Drosophila. J. Neurosci. 28 (2008) 587-597
42. Stork T., Thomas S., Rodrigues F., Silies M., Naffin E., Wenderdel S., and Klambt C. Drosophila Neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to Wrapper. Development 136 (2009) 1251-1261
43. Sun B., Xu P., and Salvaterra P.M. Dynamic visualization of nervous system in live Drosophila. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10438-10443
44. Takizawa K., and Hotta Y. Pathfinding analysis in a glia-less gcm mutant in Drosophila. Dev. Genes Evol. 211 (2001) 30-36
45. Tayler T.D., and Garrity P.A. Axon targeting in the Drosophila visual system. Curr. Opin. Neurobiol. 13 (2003) 90-95
46. Urbach R., Schnabel R., and Technau G.M. The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130 (2003) 3589-3606
47. Wheeler S.R., Banerjee S., Blauth K., Rogers S.L., Bhat M.A., and Crews S.T. Neurexin IV and wrapper interactions mediate Drosophila midline glial migration and axonal ensheathment. Development 136 (2009) 1147-1157
48. Yoshida S., Soustelle L., Giangrande A., Umetsu D., Murakami S., Yasugi T., Awasaki T., Ito K., Sato M., and Tabata T. DPP signaling controls development of the lamina glia required for retinal axon targeting in the visual system of Drosophila. Development 132 (2005) 4587-4598
49. Younossi-Hartenstein A., Nassif C., Green P., and Hartenstein V. Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 370 (1996) 313-329
50. Younossi-Hartenstein A., Salvaterra P.M., and Hartenstein V. Early development of the Drosophila brain: IV. Larval neuropile compartments defined by glial septa. J. Comp. Neurol. 455 (2003) 435-450
51. Younossi-Hartenstein A., Nguyen B., Shy D., and Hartenstein V. Embryonic origin of the Drosophila brain neuropile. J. Comp. Neurol. 497 (2006) 981-998
52. Zhou L., Schnitzler A., Agapite J., Schwartz L.M., Steller H., and Nambu J.R. Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 5131-5136