Roux's archives of developmental biology

, Volume 204, Issue 5, pp 284–307 | Cite as

Distribution, classification, and development ofDrosophila glial cells in the late embryonic and early larval ventral nerve cord

  • Kei Ito
  • Joachim Urban
  • Gerhard Martin Technau
Original Article


To facilitate the investigation of glial development inDrosophila, we present a detailed description of theDrosophila glial cells in the ventral nerve cord. A GAL4 enhancer-trap screen for glial-specific expression was performed. Using UAS-lacZ and UAS-kinesin-lacZ as reporter constructs, we describe the distribution and morphology of the identified glial cells in the fully differentiated ventral nerve cord of first-instar larvae just after hatching. The three-dimensional structure of the glial network was reconstructed using a computer. Using the strains with consistent GAL4 expression during late embryogenesis, we traced back the development of the identified cells to provide a glial map at embryonic stage 16. We identify typically 60 (54–64) glial cells per abdominal neuromere both in embryos and early larvae. They are divided into six subtypes under three categories: surface-associated glia (16–18 subperineurial glial cells and 6–8 channel glial cells), cortex-associated glia (6–8 cell body glial cells), and neuropile-associated glia (8–10 nerve root glial cells, 14–16 interface glial cells, and 3–4 midline glial cells). The proposed glial classification system is discussed in comparison with previous insect glial classifications.

Key words

Drosophila Central nervous system Glia GAL4 enhancer trap Classification 



Percent neuromere antero-posterior


Percent neuromere medio-lateral


Percent neuromere ventro-dorsal


Anterior commissure


Cell body fibre tracts to the anterior commissure


anterior corner cell AEL After egg laying


A subperineurial glial cell


B subperineurial glial cell


Cell body fibres


Cell body glia (glial cell)


Channel glia (glial cell)


Central nervous system D Dorsal




Dorsal lateral subperineurial glial cell


Dorsal nerve (transverse nerve)


channel Dorsoventral channel


Dorsal channel glial cell


Dorsal interface glial cell (cluster)


Dorsal midline glial cell (cluster)

DRG Dorsal



Exit glia (glial cell)


Fast extensor tibiae




Glial fibrillary acid protein


Glial glia


Interface glia (glial cell)


Intersegmental nerve root glia (glial cell)


Intersegmental nerve root




First instar larvae just after hatching


Lateral dorsal subperineurial glial cell


longitudinal glia (glial cell)


Lateral ventral subperineurial glial cell


Lateral cell body glial cell


Lateral interface glial cell (cluster)


Lateral intersegmental nerve root glial cell


Lateral segmental nerve root glial cell




Medial dorsal subperineurial glial cell


midline glia (glial cell) (cluster)




medialmost cell body glial cell


Median neuroblast


Medial ventral subperineurial glial cell


Cell body fibre tracts from the midline neurons


Medial cell body glial cell


Medial channel glial cell (cluster)


Medial intersegmental nerve root glial cell


Medial segmental nerve root glial cell


Nerve root glia (glial cell)


Neurohemal organ


Neuropilar glia (glial cell)


phosphate-buffered saline


PBS with Triton-X


Posterior commissure


Cell body fibre tracts to the posterior commissure


PIPES-EGTA-Mg S04 buffer


Peripheral glia (glial cell)


Perineurial glia (glial cell)


room temperature


Satellite glia


Segment boundary cell


Segmental nerve root glia (glial cell)


Segmental nerve root


Subperineurial glia (glial cell)


Transport glia


tracheal glia




Ventral lateral cell body glial cell


Ventral lateral subperineurial glial cell


Ventral nerve cord


Vertical cell body fibre tracts to the dorsal neuropile


Ventral unpaired median


Ventral channel glial cell


Ventral interface glial cell


Ventral midline glial cell (cluster)


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrams JM, White K, Fessler LL Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 117:29–43PubMedGoogle Scholar
  2. Bastiani MJ, Goodman CS (1986) Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways. J Neurosci 6:3542–3551PubMedGoogle Scholar
  3. Bauer V (1904) Zur inneren Metamorphose des Zentralnervensystems der Insekten. Zool Jahrb Abt Anat Ontog Tiere 20:123–150Google Scholar
  4. Bodmer R, Jan YN (1987) Morphological differentiation of the embryonic peripheral neurons inDrosophila. Roux's Arch Dev Biol 196:69–77Google Scholar
  5. Bossing T, Technau GM (1994) The fate of the CNS midline progenitors inDrosophila as revealed by a new method for single cell labelling. Development 120:1895–1906PubMedGoogle Scholar
  6. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415PubMedGoogle Scholar
  7. Buchanan RL, Benzer S (1993) Defective glia in theDrosophila brain degeneration mutantdrop-dead. Neuron 10:839–850PubMedGoogle Scholar
  8. Campbell G, Göring H, Lin T, Spana E, Andersson S, Doe CQ, Tomlinson A (1994) RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability inDrosophila. Development 120:2957–2966PubMedGoogle Scholar
  9. Campos-Ortega JA, Hartenstein V (1985) The embryonic development ofDrosophila melanogaster. Springer, Berlin Heidelberg New YorkGoogle Scholar
  10. Cantera R (1993) Glial cells in adult and developing prothoracic ganglion of the hawk mothManduca sexta. Cell Tissue Res 272:93–108Google Scholar
  11. Carlson SD, SaintMarie RL (1990) Structure and function of insect glia. Annu Rev Entomol 35:597–621Google Scholar
  12. Choi K-W Benzer S (1994) Migration of glia along photoreceptor axons in the developingDrosophila eye. Neuron 12:423–431PubMedGoogle Scholar
  13. Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in theDrosophila central nervous system. Development 116:855–863PubMedGoogle Scholar
  14. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP (1991) The prospero gene specifies cell fates in theDrosophila central nervous system. Cell 65:451–464PubMedGoogle Scholar
  15. Ebens AJ, Garren H, Cheyette BNR, Zipursky SL (1993) TheDrosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15–27PubMedGoogle Scholar
  16. Edwards JS, Swales LS, Bate M (1993) The differentiation between neuroglia and connective tissue sheath in insect ganglia revisited: the neural lamella and perineurial sheath cells are absent in a mesodermless mutant ofDrosophila. J Comp Neurol 333:301–308PubMedGoogle Scholar
  17. Eng LF, DeArmond SJ (1982) Immunocytochemical studies of astrocytes in normal development and disease. Adv Cell Neurobiol 3:145–171Google Scholar
  18. Fredieu JR, Mahowald AP (1989) Glial interactions with neurons duringDrosophila embryogenesis. Development 106:739–748PubMedGoogle Scholar
  19. Giangrande A (1994) Glia in the fly wing are clonally related to epithelial cells and use the nerve as a pathway for migration. Development 120:523–534Google Scholar
  20. Giangrande A, Murray MA, Palka J (1993) Development and organization of glial cells in the peripheral nervous system ofDrosophila melanogaster. Development 117:895–904PubMedGoogle Scholar
  21. Giniger E, Jan LY, Jan YN (1993) Specifying the path of the intersegmental nerve of theDrosophila embryo: a role forDelta and Notch. Development 117:431–440PubMedGoogle Scholar
  22. Goodman CS, Doe CQ (1993) Embryonic development of theDrosophila central nervous system. In: Bate M, Martinez-Arias A (eds) The development ofDrosophila melanogaster, vol II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 1131–1206Google Scholar
  23. Gorczyca MG, Phillis RW Budnik V (1994) The role oftinman, a mesodermal cell fate gene, in axon pathfinding during the development of the transverse nerve inDrosophila. Development 120:2143–2152PubMedGoogle Scholar
  24. Gray GE, Sanes JR (1992) Lineage of radial glia in the chicken optic tectum. Development 114:271–283PubMedGoogle Scholar
  25. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technan GM (1995) The homeobox generepo is required for the differentiation and maintenance of glia function in the embryonic nervous system ofDrosophila melanogaster. Development in pressGoogle Scholar
  26. Hatten ME (1990) Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13:179–184PubMedGoogle Scholar
  27. Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane vonDrosophila melanogaster (Meigen). Z Wiss Zool Alit A 139:559–663Google Scholar
  28. Hoyle G (1986) Glial cells of an insect ganglion. J Comp Neurol 246:85–103PubMedGoogle Scholar
  29. Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain ofDrosophila melanogaster. Dev Biol 149:134–148PubMedGoogle Scholar
  30. Jacobs JR (1993) Perturbed glial scaffold formation precedes axon tract malformation inDrosophila mutants. J Neurobiol 24:611–626PubMedGoogle Scholar
  31. Jacobs JR, Goodman CS (1989a) Embryonic development of axon pathways in theDrosophila CNS. I. A glial scaffold appears before the first growth cones. J Neurosci 9:2402–2411PubMedGoogle Scholar
  32. Jacobs JR, Goodman CS (1989b) Embryonic development of axon pathways in theDrosophila CNS. II. Behaviour of pioneer growth cones. J Neurosci 9:2412–2422PubMedGoogle Scholar
  33. Jacobs JR, Hiromi Y, Patel NH, Goodman CS (1989) Lineage, migration, and morphogenesis of longitudinal glia in theDrosophila CNS as revealed by a molecular lineage marker. Neuron 2:1625–1631PubMedGoogle Scholar
  34. Klämbt C, Goodman CS (1991) The diversity and pattern of glia during axon pathway formation in theDrosophila embryo. Glia 4:205–213PubMedGoogle Scholar
  35. Klämbt C, Jacobs JR, Goodman CS (1991) The midline of theDrosphila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64:801–815PubMedGoogle Scholar
  36. Lane NJ, Swales LS (1978) Changes in the blood-brain barrier of the central nervous system in the blowfly during development, with special reference to the formation and disaggregation of gap and tight junctions. 1. Larval development. Dev Biol 62:389–414PubMedGoogle Scholar
  37. Menne TV, Klämbt C (1994) The formation of commissures in theDrosophila CNS depends on the midline cells and on the Notch gene. Development 120:123–133PubMedGoogle Scholar
  38. Meyer MR, Reddy GR, Edwards JS (1987) Immunological probes reveal spatial and developmental diversity in insect neuroglia. J Neurosci 7:512–521PubMedGoogle Scholar
  39. Nambu JR, Lewis JO, Wharton KA, Crews ST (1991) TheDrosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67:1157–1167PubMedGoogle Scholar
  40. Nässel DR, Ohlsson LG, Cantera R (1988) Metamorphosis of identified neurons innervating thoracic neurohemal organs in the blowfly: Transformation of cholecystokioninlike immunoreactive neurons. J Comp Neurol 267:343–356PubMedGoogle Scholar
  41. Nelson HB, Laughon A (1993)Drosophila glial architecture and development: analysis using a collection of new cell-specific markers. Roux's Arch Dev Biol 202:341–354Google Scholar
  42. Nordlander RH, Edwards JS (1969) Postembryonic brain development in the monarch butterflyDanaus plexippus plexippus, L.: I. Cellular events during brain morphogenesis. Roux's Arch Dev Biol 162:197–217Google Scholar
  43. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Komberg TB, Goodman CS (1989) Expression ofengrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968PubMedGoogle Scholar
  44. Prokop A, Technau GM (1991) The origin of postembryonic neuroblasts in the ventral nerve cord ofDrosophila melanogaster. Development 111:79–88PubMedGoogle Scholar
  45. Prokop A, Technau GM (1993) Cell transplantation. In: Hartley DA (ed) Cellular interactions in development: a practical approach. Oxford University Press, Oxford New York Tokyo, pp 33–57Google Scholar
  46. Prokop A, Technau GM (1994) BrdU incorporation reveals DNA replication in non dividing glial cells in the larval abdominal CNS ofDrosophila. Roux's Arch Dev Biol 204:54–61Google Scholar
  47. Ramon y Cajal S, Sánchez y Sánchez D (1915) Contribuction al conocrimiento de los centros nerviosos de los insectos. Parte 1. Retina y centros opticos. Trab Lab Invertebr Biol Univ Madrid 13:1–168Google Scholar
  48. Robertson HM, Preston CR, Phillis RW Johnson-Schlitz D, Benz WK, Engels WR (1988) A stable genomic source of P element transposase inDrosophila melanogaster. Genetics 118:461–470PubMedGoogle Scholar
  49. Rothberg MJ, Hartley DA, Walther Z, Artavanis Tsakonas S (1988)slit: An EGF-homologous locus ofD. melanogaster involved in the development of the embryonic central nervous system. Cell 55:1047–1059PubMedGoogle Scholar
  50. Scharrer BC (1939) The differentiation between neuroglia and connective tissue sheath in the cockroachPeriplaneta americana. J Comp Neurol 70:77–88Google Scholar
  51. Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance inDrosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409–426PubMedGoogle Scholar
  52. Singer M, Norlander RH, Egar M (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blueprint hypothesis of neural pathway patterning. J Comp Neurol 185:1–22PubMedGoogle Scholar
  53. Sohal RS, Sharma SP, Couch EF (1972) Fine structure of the neural sheath, glia and neurons in the brain of the housefly,Musca domestica. Z Zellforsch 135:449–459PubMedGoogle Scholar
  54. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  55. Tepass U, Hartenstein V (1994) The development of cellular junctions in theDrosophila embryo. Dev Biol 161:563–596PubMedGoogle Scholar
  56. Tolbert LP, Oland LA (1989) A role for glia in the development of organized neuropilar structures. Trends Neurosci 12:70–75PubMedGoogle Scholar
  57. Tolbert LP, Oland LA (1990) Glial cells form bounderies for developing insect olfactory glomeruli. Exp Neurol 109:19–28PubMedGoogle Scholar
  58. Truman JW Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system ofDrosophila melanogaster. Dev Biol 125:145–157PubMedGoogle Scholar
  59. Udolph G, Prokop A, Bossing T, Technau GM (1993) A common precursor for glia and neurons in the embryonic CNS ofDrosophila gives rise to segment-specific lineage variants. Development 118:765–775PubMedGoogle Scholar
  60. White K, Kankel DR (1978) Patterns of cell division and cell movement in the formation of the imaginal nervous system inDrosophila melanogaster. Dev Biol 65:296–321PubMedGoogle Scholar
  61. Wigglesworth VB (1959) The histology of the nervous system of an insect,Rhodnius prolixus (Hemiptera). II. The central ganglia. Quart J Micr Sci 100:299–313Google Scholar
  62. Winberg ML, Perez SE, Steller H (1992) Generation and early differentiation of glial cells in the first optic ganglion ofDrosophila melanogaster. Development 115:903–911PubMedGoogle Scholar
  63. Xiong W Okano H, Patel NH, Blendy JA, Montell C (1994)repo encodes a glial-specific homeo domain protein required in theDrosophila nervous system. Gene Dev 8:981–994PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Kei Ito
    • 1
  • Joachim Urban
    • 1
  • Gerhard Martin Technau
    • 1
  1. 1.Institut für Genetik, Universität MainzMainzGermany

Personalised recommendations