Skip to main content
Log in

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

  • Original Article
  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

%NAP :

Percent neuromere antero-posterior

%NML :

Percent neuromere medio-lateral

%NVD :

Percent neuromere ventro-dorsal

ac :

Anterior commissure

act :

Cell body fibre tracts to the anterior commissure

aCC :

anterior corner cell AEL After egg laying

A-SPG :

A subperineurial glial cell

B-SPG :

B subperineurial glial cell

cbf :

Cell body fibres

CBG :

Cell body glia (glial cell)

CG :

Channel glia (glial cell)

CNS :

Central nervous system D Dorsal

DAB :

3,3′-diaminobenzidine

DLSPG :

Dorsal lateral subperineurial glial cell

dn :

Dorsal nerve (transverse nerve)

DV :

channel Dorsoventral channel

D-CG :

Dorsal channel glial cell

D-IG :

Dorsal interface glial cell (cluster)

D-MG :

Dorsal midline glial cell (cluster)

DRG Dorsal :

roofglia

EG :

Exit glia (glial cell)

FETi :

Fast extensor tibiae

GDA :

glutardialdehyde

GFAP :

Glial fibrillary acid protein

GIGI :

Glial glia

IG :

Interface glia (glial cell)

ISNG :

Intersegmental nerve root glia (glial cell)

ISNR :

Intersegmental nerve root

L :

Lateral

L1 :

First instar larvae just after hatching

D-SPG :

Lateral dorsal subperineurial glial cell

LG :

longitudinal glia (glial cell)

LV-SPG :

Lateral ventral subperineurial glial cell

L-CBG :

Lateral cell body glial cell

L-IG :

Lateral interface glial cell (cluster)

L-ISNG :

Lateral intersegmental nerve root glial cell

L-SNG :

Lateral segmental nerve root glial cell

M :

medial

MD-SPG :

Medial dorsal subperineurial glial cell

MG :

midline glia (glial cell) (cluster)

MM :

medialmost

MM-CBG :

medialmost cell body glial cell

MNB :

Median neuroblast

MV-SPG :

Medial ventral subperineurial glial cell

m-cbf :

Cell body fibre tracts from the midline neurons

M-CBG :

Medial cell body glial cell

M-CG :

Medial channel glial cell (cluster)

M-ISNG :

Medial intersegmental nerve root glial cell

M-SNG :

Medial segmental nerve root glial cell

NG :

Nerve root glia (glial cell)

nho:

Neurohemal organ

NPG :

Neuropilar glia (glial cell)

PBS :

phosphate-buffered saline

PBT :

PBS with Triton-X

pc :

Posterior commissure

pct :

Cell body fibre tracts to the posterior commissure

PEM :

PIPES-EGTA-Mg S04 buffer

PG :

Peripheral glia (glial cell)

PNG :

Perineurial glia (glial cell)

RT :

room temperature

SaGl :

Satellite glia

SBC :

Segment boundary cell

SNG :

Segmental nerve root glia (glial cell)

SNR :

Segmental nerve root

SPG :

Subperineurial glia (glial cell)

TpGl :

Transport glia

TrGl :

tracheal glia

V :

Ventral

VL-CBG :

Ventral lateral cell body glial cell

VI-SPG :

Ventral lateral subperineurial glial cell

VNC :

Ventral nerve cord

vt :

Vertical cell body fibre tracts to the dorsal neuropile

VUM :

Ventral unpaired median

V-CG :

Ventral channel glial cell

V-IG :

Ventral interface glial cell

V-MG :

Ventral midline glial cell (cluster)

References

  • Abrams JM, White K, Fessler LL Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 117:29–43

    PubMed  Google Scholar 

  • Bastiani MJ, Goodman CS (1986) Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways. J Neurosci 6:3542–3551

    PubMed  Google Scholar 

  • Bauer V (1904) Zur inneren Metamorphose des Zentralnervensystems der Insekten. Zool Jahrb Abt Anat Ontog Tiere 20:123–150

    Google Scholar 

  • Bodmer R, Jan YN (1987) Morphological differentiation of the embryonic peripheral neurons inDrosophila. Roux's Arch Dev Biol 196:69–77

    Google Scholar 

  • Bossing T, Technau GM (1994) The fate of the CNS midline progenitors inDrosophila as revealed by a new method for single cell labelling. Development 120:1895–1906

    PubMed  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    PubMed  Google Scholar 

  • Buchanan RL, Benzer S (1993) Defective glia in theDrosophila brain degeneration mutantdrop-dead. Neuron 10:839–850

    PubMed  Google Scholar 

  • 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 120:2957–2966

    PubMed  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985) The embryonic development ofDrosophila melanogaster. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Cantera R (1993) Glial cells in adult and developing prothoracic ganglion of the hawk mothManduca sexta. Cell Tissue Res 272:93–108

    Google Scholar 

  • Carlson SD, SaintMarie RL (1990) Structure and function of insect glia. Annu Rev Entomol 35:597–621

    Google Scholar 

  • Choi K-W Benzer S (1994) Migration of glia along photoreceptor axons in the developingDrosophila eye. Neuron 12:423–431

    PubMed  Google Scholar 

  • Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in theDrosophila central nervous system. Development 116:855–863

    PubMed  Google Scholar 

  • Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP (1991) The prospero gene specifies cell fates in theDrosophila central nervous system. Cell 65:451–464

    PubMed  Google Scholar 

  • Ebens AJ, Garren H, Cheyette BNR, Zipursky SL (1993) TheDrosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15–27

    PubMed  Google Scholar 

  • 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 333:301–308

    PubMed  Google Scholar 

  • Eng LF, DeArmond SJ (1982) Immunocytochemical studies of astrocytes in normal development and disease. Adv Cell Neurobiol 3:145–171

    Google Scholar 

  • Fredieu JR, Mahowald AP (1989) Glial interactions with neurons duringDrosophila embryogenesis. Development 106:739–748

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Giangrande A, Murray MA, Palka J (1993) Development and organization of glial cells in the peripheral nervous system ofDrosophila melanogaster. Development 117:895–904

    PubMed  Google Scholar 

  • Giniger E, Jan LY, Jan YN (1993) Specifying the path of the intersegmental nerve of theDrosophila embryo: a role forDelta and Notch. Development 117:431–440

    PubMed  Google Scholar 

  • 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 1131–1206

    Google Scholar 

  • 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 120:2143–2152

    PubMed  Google Scholar 

  • Gray GE, Sanes JR (1992) Lineage of radial glia in the chicken optic tectum. Development 114:271–283

    PubMed  Google Scholar 

  • 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 press

  • 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 13:179–184

    PubMed  Google Scholar 

  • Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane vonDrosophila melanogaster (Meigen). Z Wiss Zool Alit A 139:559–663

    Google Scholar 

  • Hoyle G (1986) Glial cells of an insect ganglion. J Comp Neurol 246:85–103

    PubMed  Google Scholar 

  • Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain ofDrosophila melanogaster. Dev Biol 149:134–148

    PubMed  Google Scholar 

  • Jacobs JR (1993) Perturbed glial scaffold formation precedes axon tract malformation inDrosophila mutants. J Neurobiol 24:611–626

    PubMed  Google Scholar 

  • 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 9:2402–2411

    PubMed  Google Scholar 

  • Jacobs JR, Goodman CS (1989b) Embryonic development of axon pathways in theDrosophila CNS. II. Behaviour of pioneer growth cones. J Neurosci 9:2412–2422

    PubMed  Google Scholar 

  • 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 2:1625–1631

    PubMed  Google Scholar 

  • Klämbt C, Goodman CS (1991) The diversity and pattern of glia during axon pathway formation in theDrosophila embryo. Glia 4:205–213

    PubMed  Google Scholar 

  • 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 64:801–815

    PubMed  Google Scholar 

  • 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 62:389–414

    PubMed  Google Scholar 

  • Menne TV, Klämbt C (1994) The formation of commissures in theDrosophila CNS depends on the midline cells and on the Notch gene. Development 120:123–133

    PubMed  Google Scholar 

  • Meyer MR, Reddy GR, Edwards JS (1987) Immunological probes reveal spatial and developmental diversity in insect neuroglia. J Neurosci 7:512–521

    PubMed  Google Scholar 

  • 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 67:1157–1167

    PubMed  Google Scholar 

  • 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 267:343–356

    PubMed  Google Scholar 

  • Nelson HB, Laughon A (1993)Drosophila glial architecture and development: analysis using a collection of new cell-specific markers. Roux's Arch Dev Biol 202:341–354

    Google Scholar 

  • 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 162:197–217

    Google Scholar 

  • 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 58:955–968

    PubMed  Google Scholar 

  • Prokop A, Technau GM (1991) The origin of postembryonic neuroblasts in the ventral nerve cord ofDrosophila melanogaster. Development 111:79–88

    PubMed  Google Scholar 

  • 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 33–57

    Google Scholar 

  • 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 204:54–61

    Google Scholar 

  • 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 13:1–168

    Google Scholar 

  • 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 118:461–470

    PubMed  Google Scholar 

  • 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 55:1047–1059

    PubMed  Google Scholar 

  • Scharrer BC (1939) The differentiation between neuroglia and connective tissue sheath in the cockroachPeriplaneta americana. J Comp Neurol 70:77–88

    Google Scholar 

  • 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 10:409–426

    PubMed  Google Scholar 

  • 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 185:1–22

    PubMed  Google Scholar 

  • 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 135:449–459

    PubMed  Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Tepass U, Hartenstein V (1994) The development of cellular junctions in theDrosophila embryo. Dev Biol 161:563–596

    PubMed  Google Scholar 

  • Tolbert LP, Oland LA (1989) A role for glia in the development of organized neuropilar structures. Trends Neurosci 12:70–75

    PubMed  Google Scholar 

  • Tolbert LP, Oland LA (1990) Glial cells form bounderies for developing insect olfactory glomeruli. Exp Neurol 109:19–28

    PubMed  Google Scholar 

  • Truman JW Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system ofDrosophila melanogaster. Dev Biol 125:145–157

    PubMed  Google Scholar 

  • 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 118:765–775

    PubMed  Google Scholar 

  • White K, Kankel DR (1978) Patterns of cell division and cell movement in the formation of the imaginal nervous system inDrosophila melanogaster. Dev Biol 65:296–321

    PubMed  Google Scholar 

  • Wigglesworth VB (1959) The histology of the nervous system of an insect,Rhodnius prolixus (Hemiptera). II. The central ganglia. Quart J Micr Sci 100:299–313

    Google Scholar 

  • Winberg ML, Perez SE, Steller H (1992) Generation and early differentiation of glial cells in the first optic ganglion ofDrosophila melanogaster. Development 115:903–911

    PubMed  Google Scholar 

  • 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 8:981–994

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ito, K., Urban, J. & Technau, G.M. Distribution, classification, and development ofDrosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch Dev Biol 204, 284–307 (1995). https://doi.org/10.1007/BF02179499

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02179499

Key words

Navigation