Development and organization of glial cells in Drosophila melanogaster

International Journal of Developmental Biology

Volumn 40, Issue 5, 1996, Pages 917-927

  Giangrande, Angela ^a,b  

^a CNRS   (France)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Drosophila melanogaster; glial cells; glide gcm; gliogenesis; neural development

Indexed keywords

ANIMAL CELL; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; EMBRYO; GLIA CELL; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL DIFFERENTIATION; CLONE CELLS; DROSOPHILA MELANOGASTER; MUTATION; NEUROGLIA; NEURONS; WING;

ANIMALIA; DROSOPHILA MELANOGASTER; INVERTEBRATA; MELANOGASTER; VERTEBRATA;

EID: 0029994179     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (84)

1. ANDERSON, D.J. (1995). A molecular switch for the neuron-glia developmental decision Neuron 15: 1219-1222.
2. ANDERSON, M.G., PERKINS, G L., CHITTIK, P., SHRIGLEY, R J and JOHNSON, W.A. (1995). drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes Dev. 9: 123-137.
3. AULD, V.J., FETTER, R.D., BROADIE, K. and GOODMAN, C.S. (1995). Gliotactin, a novel transmembrane protein on peripheral glia is required to form the blood-nerve barrier in Drosophila. Cell 81: 757-767.
4. BARRES, B.A. (1991) Glial ion channels Curr. Opin. Neurobiol. 1: 354-359.
5. BARRES, B.A. and RAFF, M.C. (1994). Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12: 935-942.
6. BARRES, B.A., HART, I.K., COLES, H.S.R, BURNE, J.F., VOYVODIC, J.T., RICHARDSON, W.D. and RAFF, M C. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70: 31-46.
7. BARRES, B.A., SCHMID, R., SENDTNER, M. and RAFF, M.C. (1993). Multiple extracellular signals are required for long term oligodendrocyte survival. Development 118. 283-295.
8. BODMER, R., CARRETTO, R. and JAN, Y.N. (1989). Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages Neuron 3: 21-32.
9. BOSSING, T., YECHNAU, G.M. and DOE, C.Q. (1996). huckebein is required for glial development and axon pathfinding in the neuroblast 1-1 and neuroblast 2-2 lineages in the Drosophila central nervous system. Mech. Dev 55: 53-64.
10. BRAND, A. and PERRIMON, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
11. BREWSTER, R. and BODMER, R. (1995). Origin and specification of type II sensory neurons in Drosophila. Development 121: 2923-2936.
12. BUCHANAN, R.L. and BENZER, S. (1993). Defective glia in the Drosophila brain degeneration mutant drop-dead Neuron 10: 839-850.
13. BUNGE, R P. (1993). Expanding roles for the Schwann cell: ensheathment, myelination, trophism and regeneration. Curr. Opin. Neurobiol. 3: 805-809.
14. CAMPBELL, G., GÖRING, H., LIN, T., SPANA, E. ANDERSON, S , DOE, C.Q. and TOMLINSON, A. (1994). RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120: 2957-2966.
15. CAMPOS-ORTEGA, J.A. (1994). Cellular interactions in the developing nervous system of Drosophila. Cell 77: 969-975.
16. CHOI, K-W. and BENZER, S (1994) Migration of glia along photoreceptor axons in the developing Drosophila eye Neuron 12: 423-431.
17. CONDRON, B.G. and ZINN, K. (1994). The grasshopper median neuroblast is a multipotent progenitor cell that generates glia and neurons in distinct temporal phases. J. Neurosci. 14: 5766-5777.
18. CONDRON, B.G. and ZINN, K. (1995). Activation of cAMP-dependent protein kinase A triggers a glial-to-neuronal cell-fate switch in an insect neuroblast lineage. Curr. Biol 5: 51-61
19. CONDRON, B.G., PATEL, N.H. and ZINN, K. (1994). engrailed controls glial/ neuronal cell fate decision at the midline of the central nervous system. Neuron 13. 541-554.
20. DOE, C.Q., CHU-LA-GRAFF, Q , WRIGHT, D.M. and SCOTT, M.P. (1991). The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65: 451-464.
21. EBENS, A.J., GARREN, H., CHEYETTE, B.N.R. and ZIPURSKY, L. (1993). The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74: 15-27
22. EDWARDS, J.S., SWALES, L.S. and BATE, C.M. (1993) The differentiation between neuroglia and connective sheath in insect ganglia revisited, the neural lamella and penneural sheath cells are absent in a mesodermless mutant of Drosophila. J. Comp. Neurol 333: 301-308
23. ENDO, Y. and TSURUGI, K. (1988). The RNA N-glycosidase activity of ricin A-chain. The characteristics of the enzymatic activity of ricin A-chain with ribosomes and ribosomal RNA. J. Biol. Chem. 263. 8735-8739.
24. FREDIEU, J.R. and MAHOWALD, A.P (1989). Glial interactions with neurons during Drosophila embryogenesis. Development 106: 739-748.
25. GIANGRANDE, A. (1994). Glia in the fly wing are clonally related to epithelial cells and use the nerve as a pathway for migration. Development 120: 523-534.
26. GIANGRANDE, A. (1995). Proneural genes influence gliogenesis in fly. Development 121: 429-438.
27. GIANGRANDE, A. and PALKA, J. (1990). Genes involved in the development of the peripheral nervous system of Drosophila. Semin. Cell Biol. 1: 197-209.
28. GIANGRANDE, A., MURRAY, M.A. and PALKA, P. (1993). Development and organization of glial cells in the Peripheral Nervous System of Drosophila melanogaster Development 117: 895-904.
29. GINIGER, E., WELLIS, W , JAN, L.Y. and JAN, Y.N (1993). Tracing neurons with a kinesin-B-galactosidase fusion protein. Roux Arch. Dev. Biol. 202: 112-122.
30. GOLIC, K.G. and LINDQUIST, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59: 499-509.
31. HALTER, D.A., URBAN, J., RICKERT, C., NER, S.S., ITO, K., TRAVERS, A.A. and TECHNAU, G.M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121: 317-332.
32. HARTENSTEIN, A.Y., RUGENDORFF, A., TEPASS, U. and HARTENSTEIN, V. (1992). The function of the neurogenic genes during epithelial development in the Drosophila embryo Development 116: 1203-1220.
33. HENDERSON, C.E., PHILLIPS, H.S., POLLOCK, R A., DAVIES, A.M., LEMEULLE, C., ARMANINI, M., SIMPSON, L.C., MOFFET, B., VANDLEN, R.A., KOLIATOS, V.E. and ROSENTHAL, A. (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266: 1062-1064.
34. HIDALGO, A., URBAN, J. and BRAND, A. (1995). Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 121: 3703-3712.
35. HOSOYA, T., TAKIZAWA, K., NITTA, K. and HOTTA, Y. (1995). glial cell missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82: 1025-1036.
36. ITO K., URBAN J. and TECHNAU G.M. (1995). Distribution, classification and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord Roux Arch. Dev. Biol. 204: 284-307.
37. JACOBS, J.R. and GOODMAN, C S (1989). Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J. Neurosci. 9: 2402-2411.
38. JACOBS, J.R., HIROMI, Y., PATEL, N.H. and GOODMAN, C.S. (1989). Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker. Neuron 2: 1625-1631.
39. JESSEN, K.R. and MIRSKY, R (1992). Schwann cells: early lineage, regulation of proliferation and control of myelin formation. Curr. Opin. Neurobiol. 2: 575-581
40. JESSEN, K.R., BRENNAN, A., MORGAN, L , MIRSKY, R., KENT, A., HASHIMOTO, Y. and GAVRILOVIC, J. (1994) The Schwann cell precursor and its fate a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12: 509-527.
41. JONES, B.W., FETTER, R.D., TEAR, G. and GOODMAN, C S. (1995) glial cell missing: a genetic switch that controls glial versus neuronal fate. Cell 82: 1013-1023.
42. KARIM, F.D , URNESS, L.D., THUMMEL, C.S , KLEMSZ, M.J., MCKERCHER, S.R., CELADA, A., VAN BEVEREN, C., MAKI, R.A., GUNTHER, C.V., NYE, J.A. and GRAVES, B.J. (1990). The ETS-domain: a new DNA binding motif that recognizes a purine rich core DNA sequence. Genes Dev. 4: 1451-1453.
43. KEIL, T A. and STEINBRECHT, R.A (1986). Mechanosensitive and olfactory sensilla of insects. In Insect Ultrastructure, Vol. 2 (Eds. R.C. King and H. Akai). Plenum Press, New York, pp 477-516.
44. KLAES, A., MENNE, T , STOLLEWERK, A., SCHOLZ, H. and KLÄMBT, C. (1994). The ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78: 149-160.
45. KLAMBT, C. (1993). The Drosophila gene pointed encodes two ets-like proteins which are involved in the development of the midline glial cells. Development 117. 163-176.
46. KLAMBT, C. and GOODMAN, C.S. (1991). The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4: 205-213.
47. KLÄMBT, C., GLAZER, L and SHILO, B-Z. (1992). breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev. 6: 1668-1678.
48. KLÄMBT, C., JACOBS, J.R. and GOODMAN, C.S. (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.
49. LE DOUARIN, N.M., DUPIN, E and ZILLER, C. (1994). Genetic and epigenetic control in neural crest development. Curr. Opin. Genet. Dev. 4: 685-695.
50. LEMKE, G.E. and BROCKES, J.P. (1984). Identification and purification of glial growth factor. J. Neurosci 4: 75-83.
51. MARCHIONNI, M.A., GOODEARL, A.D.J., CHEN, M.S , BERMINGHAM-McDONOGH, O., KIRK, C., HENDRICKS, M., DANEHY, F., MISUMI, D., SUDHALTER, J., KOBAYASHI, K., WROBLESKI, D., LYNCH, C., BALDASSARRE., M., HILES, I., DAVIS, J.B., HSUAN, J.J., TOTTY, N.F., OTSU, M., MCBURNEY, R.N., WATERFIELD., M.D., STROOBANT, P. and GWYNNE, D. (1993) Glial growth factors are alternatively spliced rebB2 ligands expressed in the nervous system. Nature 362: 312-318.
52. MASU, Y., WOLF, E., HOLTMANN, B., SENDTNER, M., BREM , G. and THOENEN, H. (1993). Disruption of the CNTF gene results in motor neuron degeneration. Nature 365: 27-32.
53. McCONNELL, S.K. (1991). The generation of neuronal diversity in the central nervous system. Annu. Rev. Neurosci. 14: 269-300.
54. MEYER, M.R., REDDY, G.R. and EDWARDS, J S. (1987). Immunological probes reveal spatial and developmental diversity in insect neuroglia. J. Neurosci. 7: 512-521.
55. MILLER, R H. (1996). Oligodendrocyte origins. Trends Neurosci. 19: 92-96.
56. MLODZIK, M. and HIROMI, Y. (1992). Enhancer trap model in Drosophila: its application to neurobiology. Methods Neurosci. 9: 397-414.
57. MURRAY, M.A., SCHUBIGER, M. and PALKA, J. (1984). Neuron differentiation and axon growth in the developing wing of Drosophila melanogaster. Dev. Biol. 104: 259-273.
58. NELSON, H B and LAUGHON, A. (1993). Drosophila glial architecture and development: analysis using a collection of new cell-specific markers. Roux Arch Dev Biol. 202: 341-354
59. NELSON, H.B and LAUGHON, A (1994). Drosophila glial development is regulated by genes involved in the control of neuronal cell fate. Roux Arch. Dev. Biol. 204: 118-125.
60. O'KANE, C.J. and GEHRING, W.J. (1987). Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84. 9123-9127.
61. PFRIEGER, F.W. and BARRES, B.A. (1995). What the fly's glia tell the fly's brain. Cell 83: 671-674.
62. POULSON, D.F. (1950). Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster. In Biology of Drosophila (Ed. M Demerec). J. Wiley and Sons, Inc, New York, pp 168-274,.
63. RAFF, M.C., BARRES, B.A., BURNE, J F., COLES, H.S., ISHIZAKI, Y. and JACOBSON, M.D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262: 695-699.
64. REYNOLDS, M.L. and WOOLF, C.J. (1993). Reciprocal Schwann cell-neuron interactions Curr. Opin. Neurobiol. 2: 683-693.
65. RITCHIE, J.M. (1992). Voltage-gated ion channels in Schwann cells and glia. Trends Neurosci. 15. 345-351.
66. RUBIN, G.M. and SPRADLING, A.C. (1982). Genetic transformation of Drosophila with transposable element vectors Science 218: 348-353.
67. SAINT MARIE, R L. and CARLSON, S.D. (1983). The fine structure of neuroglia in the lamina ganglionaris of the housefly, Musca domestica L. J. Neurocytol. 12: 213-241.
68. SAINT MARIE, R.L., CARLSON, S.D. and CHI, C. (1982). The glial cells of insects. In Insect Ultrastructure, Vol. 2 (Eds. C.R. King and H. Akai). Plenum Press, New York and London, pp. 435-475.
69. SENDTNER M, HOLTMAN, B., KOLBECK, R., THOENEN, H. and BARDE, Y.A. (1992). Brain derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360: 757-759.
70. SHAH, N.M., MARCHIONNI, M.A., ISAACS, I., STROOBANT, P. and ANDERSON, D. (1994). Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77: 349-360.
71. SMITH, P.J.S., SHEPHERD, D. and EDWARDS, J.S. (1991). Neural repair and glial proliferation: parallel with gliogenesis in insects. BioEssays 13: 65-72.
72. SONNENFELD, M.J. and JACOBS, J.R. (1995). Apoptosis of the midline glia during Drosophila embryogenesis: a correlation with axon contact. Development 121: 569-578
73. STEMPLE, D.L. and ANDERSON, D.J. (1993). Lineage diversification of the neural crest: in vitro investigation. Dev. Biol. 159: 12-23.
74. STRAUSFELD, N.J (1976). Atlas of an Insect Brain. Springer-Verlag, Berlin
75. STRUHL, G. and BASLER, K. (1993). Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
76. UDOLPH, G., PROKOP, A., BOSSING, T. and TECHNAU, G.M. (1993). A common precursor for glia and neuron in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 118: 765-775.
77. VAESSIN, H., GRELL, E., WOLFF, E., BIER, E., JAN, L Y. and JAN, Y.N. (1991). prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67: 941-953.
78. VINCENT, S., VONESCH, J.L. and GIANGRANDE, A. (1996). glide directs glial fate commitment and cell fate switch between neurones and glia. Development 122: 131-139.
79. WEIGEL, D. JURGENS, G., KLINGER, M. and JÄCKLE, H. (1990). Two gap genes mediate maternal terminal pattern information in Drosophila Science 248: 495-498.
80. WIGGLESWORTH, V.B. (1959) The histology of the nervous system of an insect Rhodnius prolixus (Hemiptera) I. The central ganglia. Quart. J. Microsc. Sci. 100. 299-313.
81. WILSON, C., PEARSON, R.K., BELLEN, H. J., O'KANE, C.J., GROSSNIKLAUS, U and GEHRING, W.J. (1989). P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev 3: 1301-1313.
82. WINBERG, M. L., PEREZ, S.E. and STELLER, H. (1992). Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster. Development 115: 903-911.
83. XIONG, W-C. and MONTELL, C. (1995). Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron 14: 581-590.
84. XIONG, W-C., OKANO, H., PATEL, N.H., BLENDY, J.A. and MONTELL, C. (1994). repo codes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8: 981-994.