Key Interactions Between Neurons and Glial Cells During Neural Development in Insects

Annual Review of Entomology

Volumn 48, Issue , 2003, Pages 89-110

  Oland, Lynne A ^a   Tolbert, Leslie P ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Axon guidance; Embryogenesis; Intercellular interactions; Metamorphosis

Indexed keywords

INSECT; NERVOUS SYSTEM; NEUROLOGY;

HEXAPODA; INSECTA; VERTEBRATA;

ANIMAL; BRAIN; CELL COMMUNICATION; CYTOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; INNERVATION; INSECT; NERVE CELL; NERVOUS SYSTEM; OPTIC LOBE; PERIPHERAL NERVE; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; SENSE ORGAN;

ANIMALS; BRAIN; CELL COMMUNICATION; INSECTS; NERVOUS SYSTEM; NEUROGLIA; NEURONS; OPTIC LOBE; PERIPHERAL NERVES; SENSE ORGANS;

EID: 0037209123     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ento.48.091801.112654     Document Type: Review

References (119)

1. Auld V. 1999. Glia as mediators of growth cone guidance: studies from insect nervous systems. Cell Mol. Life Sci. 55:1377-85
2. Bastiani MJ, du Lac S, Goodman CS. 1986. Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of a specific axonal pathway by the pCC neuron. J. Neurosci. 6:3518-31
3. Bastiani MJ, Goodman CS. 1986. Guidance of neuronal growth cones in the grasshopper embryo III. Recognition of specific glial pathways. J. Neurosci. 6:3542-51
4. Battye R, Adrienne S, Jacobs JR. 1999. Axon repulsion from the midline of the Drosophila CNS requires slit function. Development 126:2475-81
5. Baumgartner S, Littleton J, Broadie K, Bhat M, Harbecke R, et al. 1996. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87:1059-68
6. Bier E, Jan L, Jan Y. 1990. rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4:190-203
7. Booth G, Kinrade E, Hidalgo A. 2000. Glia maintain follower neuron survival during Drosophila CNS development. Development 127:237-44
8. Boyan G, Therianos S, Williams J, Reichert H. 1995. Axogenesis in the embryonic brain of the grasshopper Schistocerca gregaria: an identified cell analysis of early brain development. Development 121:75-86
9. Brose D, Bland K, Wang K, Arnott D, Henzel W, et al. 1999. Slit proteins bind robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795-806
10. Brose K, Tessier-Lavigne M. 2000. Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10:95-102
11. Brunner A, Twardzik T, Schneuwly S. 1994. The Drosophila giant lens gene plays a dual role in eye and optic lobe development: inhibition of differentiation of ommatidial cells and interference in photoreceptor axon guidance. Mech. Dev. 48:175-85
12. Buchanan R, Benzer S. 1993. Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10:839-50
13. Burek M, Oppenheim R. 1999. Cellular interactions that regulate programmed cell death in the developing vertebrate nervous system. Cell Death Dis. Nerv. Syst. 1:145-80
14. Campbell G, Göring H, Lin T, Spana E, Andersson S, et al. 1994. RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120:2957-66
15. Campos A, Lee K, Steller H. 1995. Establishment of neuronal connectivity during development of the Drosophila larval visual system. J. Neurobiol. 28:313-29
16. Choi K-W, Benzer S. 1994. Migration of glia along photoreceptor axons in the developing Drosophila eye. Neuron 12:423-31
17. Clyne P, Warr C, Freeman M, Lessing D, Kim J, Carlson J. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-38
18. Condron B. 1999. Spatially discrete FGF-mediated signalling directs glial morphogenesis. Development 126:4635-41
19. Crews S, Thomas J, Goodman C. 1988. The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52:143-51
20. Doe C, Chu-Lagraff Q, Wright D, Scott M. 1991. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65:451-64
21. Dong R, Jacobs J. 1997. Origin and differentiation of supernumerary midline glia in Drosophila embryos deficient for apoptosis. Dev. Biol. 190:165-77
22. Ebens A, Garren H, Cheyette B, Zipursky S. 1993. The Drosophila anachronism locus: A glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15-27
23. Edwards JS. 1969. Postembryonic development and regeneration of the insect nervous system. Adv. Insect Physiol. 6:97-137
24. Edwards JS, Tolbert LP. 1998. Insect neuroglia. In Microscopic Anatomy of the Invertebrates, ed. M Locke, 11B:449-66. New York: Wiley
25. Giangrande A. 1996. Development and organization of glial cells in Drosophila melanogaster. Int. J. Dev. Biol. 40:917-27
26. Gibson NJ, Rossler W, Nighorn AJ, Oland LA, Hildebrand JG, Tolbert LP. 2001. Neuron-glia communication via nitric oxide is essential in establishing antennal-lobe structure in Manduca sexta. Dev. Biol. 240:326-39
27. Giesen K, Hummel T, Stollewerk A, Harrison S, Travers A, Klambt C. 1997. Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes. Development 124:2307-11
28. Gisselbrecht S, Skeath J, Doe C, Michelson A. 1996. heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. Genes Dev. 10:3003-17
29. Granderath S, Klambt C. 1999. Glia development in the embryonic CNS of Drosophila. Curr. Opin. Neurobiol. 9:531-36
30. Gymer A, Edwards J. 1967. The development of insect nervous system. I. An analysis of postembryonic growth in the terminal ganglion of Acheta domesticus. J. Morphol. 123:191-97
31. Halter D, Urban J, Rickert C. 1995. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121:317-32
32. Harris R, Sabatelli L, Seeger M. 1996. Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila netrin/UNC-6 homologs. Neuron 17:217-28
33. Hartenstein V, Nassif C, Lekven A. 1998. Embryonic development of the Drosophila brain. II. Pattern of glial cells. J. Comp. Neurol. 402:32-47
34. Hidalgo A, Booth G. 2000. Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127:393-402
35. Hidalgo A, Urban J, Brand A. 1995. Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 121:3703-12
36. Higgins MR, Gibson NJ, Eckholdt PA, Nighorn A, Copenhaver P, et al. 2002. Different isoforms of fasciclin II are expressed by a subset of developing olfactory receptor neurons and by olfactory-nerve glial cells during formation of glomeruli in the moth Manduca sexta. Dev. Biol. 244:134-54
37. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20:595-631
38. Hosoya T, Takiwaza K, Nitta K, Hotta Y. 1995. glial cells missing: a binary switch between neuronal and glial differentiation in Drosophila. Cell 82:1025-36
39. Huang Z, Kunes S. 1998. Signals transmitted along retinal axons in Drosophila: hedgehog signal reception and the cell circuitry of lamina cartridge assembly. Development 125:3753-64
40. Hummel T, Attix S, Gunning D, Zipursky S. 2002. Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33:193-203
41. Hummel T, Krukkert K, Roos J, Davis G, Klambt C. 2000. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26:357-70
42. Hummel T, Schimmelpfeng K, Klämbt C. 1999. Commissure formation in the embryonic CNS of Drosophila. I. Identification of gene function. Dev. Biol. 208:381-98
43. Hummel T, Schimmelpfeng K, Klämbt C. 1999. Commissure formation in the embryonic CNS of Drosophila. II. Function of the different midline cells. Development 126:771-79
44. Ito D, Urban J, Technau G. 1995. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch. Dev. Biol. 204:284-307
45. Jacobs JR. 2000. The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog. Neurobiol. 62:475-508
46. Jacobs JR, Goodman CS. 1989. Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J. Neurosci. 9:2402-11
47. Jacobs JR, Hiromi Y, Patel M, Goodman CS. 1989. Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker. Neuron 2:1625-31
48. Jhaveri D, Rodrigues V. 2002. Sensory neurons of the Atonal lineage pioneer the formation of glomeruli within the adult Drosophila olfactory lobe. Development 129:1251-60
49. Jhaveri D, Sen A, Rodrigues V. 2000. Mechanism underlying olfactory neuronal connectivity in Drosophila - the Atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. Dev. Biol. 226:73-87
50. Jones B. 2001. Glial cell development in the Drosophila embryo. BioEssays 23:877-87
51. Jones B, Fetter R, Tear G, Goodman CS. 1995. glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82:1013-23
52. Kidd T, Bland KS, Goodman CS. 1999. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96:785-94
53. Kinrade E, Brates T, Tear G, Hidalgo A. 2001. Roundabout signaling, cell contact and trophic support confine longitudinal glia and axons in the Drosophila CNS. Development 128:207-16
54. Klaes A, Menne T, Stollewerk A, Scholz H, Klämbt C. 1994. The ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78:149-60
55. Klämbt C, Goodman CS. 1991. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4:205-13
56. Klämbt C, Jacobs J, Goodman C. 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 64:801-15
57. Klämbt D, Hummel T, Menne T, Sadlowski E, Scholz H, Stollewerk A. 1996. Development and function of embryonic central nervous system glial cells in Drosophila. Dev. Genet. 18:40-49
58. Kolodziej P, Timpe L, Mitchell K, Fried S, Goodman C, et al. 1996. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87:197-204
59. Kretzschmar D, Hasan G, Sharma S, Heisenberg M, Benzer S. 1997. The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J. Neurosci. 17:7425-32
60. Kretzschmar D, Pflugfelder G. 2002. Glia in development, function, and neurodegeneration of the adult insect brain. Brain Res. Bull. 57(1):121-31
61. Kunes S, Wilson C, Steller H. 1993. Independent guidance of retinal axons in the developing visual system of Drosophila. J. Neurosci. 13:752-67
62. Lanoue B, Jacobs J. 1999. rhomboid function in the midline of the Drosophila CNS. Dev. Genet. 25:321-30
63. Leiserson W, Harkins E, Keshishian H. 2000. Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 28:793-806
64. Lemke G. 2001. Glial control of neural development. Annu. Rev. Neurosci. 24:87-105
65. Martin KA, Poeck B, Roth H, Ebens AJ, Ballard LC, Zipursky SL. 1995. Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14:229-40
66. Mitchell K, Doyle J, Serafini T, Kennedy T, Tessier-Lavigne M, et al. 1996. Genetic analysis of netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17:203-15
67. Mombaerts P. 1996. Targeting olfaction. Curr. Opin. Neurobiol. 6:481-86
68. Nassif C, Noveen A, Hartenstein V. 1998. Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. J. Comp. Neurol. 402:10-31
69. Noordermeer J, Kopczynski C, Fetter R, Bland K, Chen W, Goodman C. 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
70. Oland LA, Pott WM, Higgins MR, Tolbert LP. 1998. Targeted ingrowth and axon-glial relationships of olfactory receptor axons in the primary olfactory pathway of an insect. J. Comp. Neurol. 398:119-38
71. Oland LA, Tolbert LP. 1996. Multiple factors shape the development of olfactory glomeruli: insights from an insect model system. J. Neurobiol. 30:92-109
72. Oland LA, Tolbert LP, Mossman KL. 1988. Radiation-induced reduction of the glial population during development disrupts the formation of olfactory glomeruli in an insect. J. Neurosci. 8:353-67
73. Perez SE, Steller H. 1996. Migration of glial cells into retinal axon target field in Drosophila melanogaster. J. Neurobiol. 30:359-73
74. Pflugfelder GO, Heisenberg M. 1995. Optomotor-blind of Drosophila melanogaster: a neurogenetic approach to optic lobe development and optomotor behaviour. Comp. Biochem. Physiol. A 110:185-202
75. Pfreiger FW, Barres B. 1995. What the fly's glia tell the fly's brain. Cell 83:671-74
76. Pielage J, Klämbt C. 2001. Glial cells aid axonal target selection. Trends Neurosci. 24:432-33
77. Poeck B, Fischer S, Gunning D, Zipursky L, Salecker I. 2001. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29:99-113
78. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson B. 2000. Crossing the midline: roles and regulation of robo receptors. Neuron 28:767-77
79. Rajagopalan S, Vivancos V, Nicolas E, Dickson B. 2000. Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103:1033-45
80. Rangarajan R, Courvoisier H, Gaul U. 2001. Dpp and Hedgehog mediate neuron-glia interactions in Drosophila eye development by promoting the proliferation and motility of subretinal glia. Mech. Dev. 108:93-103
81. Rangarajan R, Gong Q, Gaul U. 1999. Migration and function of glia in the developing Drosophila eye. Development 126:3285-92
82. Reddy GV, Rodrigues V. 1999. A glial cell arises from an additional division within the mechanosensory lineage during development of the microchaete on the Drosophila notum. Development 126:4617-22
83. Reichert H, Boyan G. 1997. Building a brain: developmental insights in insects. Trends Neurosci. 20:258
84. Rospars J. 1988. Structure and development of the insect antennodeutocerebral system. Int. J. Insect Morphol. Embryol. 17:243-94
85. Rössler W, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP. 1999. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J. Neurosci. 19:9865-77
86. Rössler W, Randolph PW, Tolbert LP, Hildebrand JG. 1999. Axons of olfactory receptor cells of trans-sexually grafted antennae induce development of sexually dimorphic glomeruli in Manduca sexta. J. Neurobiol. 38:521-41
87. Rothberg J, Jacobs J, Goodman C, Artavanis-Tsakonas S. 1990. slit: An extracellular protein necessary for the development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4:2169-87
88. Salecker I, Boeckh J. 1995. Embryonic development of the antennal lobes of a hemimetabolous insect, the cockroach Periplaneta americana: light and electron microscopic observations. J. Comp. Neurol. 352:33-54
89. Salecker I, Boeckh J. 1996. Influence of receptor axons on the formation of olfactory glomeruli in a hemimetabolous insect, the cockroach Periplaneta americana. J. Comp. Neurol. 370:262-79
90. Sawamoto K, Okabe M, Tanimura T, Hayashi S, Mikoshiba K, Okano H. 1996. argos is required for projection of photoreceptor axons during optic lobe development in Drosophila. Dev. Dyn. 205:162-71
91. Schafer R. 1973. Postembryonic development in the antenna of the cockroach, Leucophaea maderae: growth, regeneration, and the development of the adult pattern of sensory organs. J. Exp. Zool. 183:353-64
92. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM. 1997. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189:186-204
93. Seeger M, Tear G, Ferres-Marco D, Goodman C. 1993. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409-26
94. Selzer R, Schaller-Selzer L. 1987. Structure and function of luminal neurons in the early embryonic antenna of the American cockroach, Periplaneta americana. Dev. Biol. 122:363-72
95. Sepp K, Schulte J, Auld V. 2000. Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30:122-33
96. Sepp K, Schulte J, Auld V. 2001. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol. 238:47-63
97. Sharrow M, Tiemeyer M. 2001. Gliolectin-mediated carbohydrate binding at the Drosophila midline ensures the fidelity of axon pathfinding. Development 128:4585-95
98. Shepherd D. 2000. Glial dependent survival of neurons in Drosophila. BioEssays 22:407-9
99. Shigenaga A, Kimura K, Kobayakawa Y, Tsujimoto Y, Tanimura T. 1997. Cell ablation by ectopic expression of cell death genes, ced-3 and Ice, in Drosophila. Dev. Growth Differ. 39:429-36
100. Shishido E, Ono N, Kojima T, Saigo K. 1997. Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 124:2119-28
101. Silver J, Lorenz S, Wahlsten D, Coughlin J. 1982. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J. Comp. Neurol. 210:10-29
102. Sonnenfeld MJ, Jacobs JR. 1994. Mesectodermal cell fate analysis in Drosophila midline mutants. Mech. Dev. 46:3-13
103. Sonnenfeld MJ, Jacobs JR. 1995. Apoptosis of the midline glia during Drosophila embryogenesis: a correlation with axon contact. Development 121:569-78
104. Sorensen KA, Davis NT, Hildebrand JG. 1990. Postembryonic neurogenesis in the brain of Manduca sexta. Soc. Neurosci. 16:1147 (Abstr.)
105. Stocker R. 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275:3-26
106. Strausfeld NJ. 1976. Atlas of the Fly Brain. Berlin: Springer
107. Suh GS, Poeck B, Chouard T, Oron E, Segal D, et al. 2002. Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33:35-46
108. Tear G, Harris R, Sutaria S, Kilomanski K, Goodman C, Seeger M. 1996. commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16:501-14
109. Therianos S, Leuzinger S, Hirth F, Goodman C, Reichert H. 1995. Embryonic development of the Drosophila brain: formation of commissural and descending pathways. Development 121:3849-60
110. Tissot M, Gendre N, Hawken A, Störtkuhl KF, Stocker RF. 1997. Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J. Neurobiol. 32:281-97
111. Tix S, Eckhart E, Fischbach K-F, Benzer S. 1997. Glia in the chiasms and medulla of the Drosophila melanogaster optic lobes. Cell Tissue Res. 289:397-409
112. Treherne JE, Schofield PK. 1981. Mechanisms of ionic homeostasis in the central nervous system of an insect. J. Exp. Biol. 95:61-73
113. Tucker ES, Oland LA, Tolbert LP. 2000. In vitro study of interactions between olfactory receptor growth cones and glial cells of axonal sorting zone. Soc. Neurosci. 26:1611 (Abstr.)
114. Udolph G, Prokop A, Bossing T, Technau GM. 1993. A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 118:765-75
115. Wigglesworth VB. 1959. The histology of the nervous system of an insect, Rhodnius prolixus (Hemiptera). II. The central ganglia. Q. J. Microsc. Sci. 100:299-13
116. Winberg ML, Perez SE, Steller H. 1992. Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster. Development 115:903-11
117. Xiong W, Montell C. 1995. Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron 14:581-90
118. 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. 8:981-94
119. Zhou L, Schnitzler A, Agapite J, Schwartz L, Steller H, Nambu J. 1997. 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. USA 94:5131-36