Skip to main content
Log in

Analog of vertebrate anionic sites in blood-brain interface of larval Drosophila

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The blood-brain barrier ensures brain function in vertebrates and in some invertebrates by maintaining ionic integrity of the extraneuronal bathing fluid. Recent studies have demonstrated that anionic sites on the luminal surface of vascular endothelial cells collaborate with tight junctions to effect this barrier in vertebrates. We characterize these two analogous barrier factors for the first time on Drosophila larva by an electron-dense tracer and cationic gold labeling. Ionic lanthanum entered into but not through the extracellular channels between perineurial cells. Tracer is ultimately excluded from neurons in the ventral ganglion mainly by an extensive series of (pleated sheet) septate junctions between perineurial cells. Continuous junctions, a variant of the septate junction, were not as efficient as the pleated sheet variety in blocking tracer. An anionic domain now is demonstrated in Drosophila central nervous system through the use of cationic colloidal gold in LR White embedment. Anionic domains are specifically stationed in the neural lamella and not noted in the other cell levels of the blood-brain interface. It is proposed that in the central nervous system of the Drosophila larva the array of septate junctions between perineurial cells is the physical barrier, while the anionic domains in neural lamella are a “charge-selective barrier” for cations. All of these results are discussed relative to analogous characteristics of the vertebrate blood-brain barrier.

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

References

  • Abbott NJ, Lane NJ, Bundgaard M (1986) The blood-brain interface in invertebrates. Ann NY Acad Sci 481:20–42

    Google Scholar 

  • Bargiello TA, Saez L, Baylies MK, Gasic G, Young MW, Spray DC (1987) The Drosophila clock gene per affects intercellular junctional communication. Nature 328:686–691

    Google Scholar 

  • Bertolatus JA (1990) Affinity cytochemical labeling of glomerular basement membrane anionic sites using specific biotinylation and colloidal gold probes. J Histochem Cytochem 38:377–384

    Google Scholar 

  • Bush MS, Reid AR, Allt G (1991) Blood-nerve barrier: distribution of anionic sites on the endothelial plasma membrane and basal lamina of dorsal root ganglia. J Neurocytol 20:759–768

    Google Scholar 

  • Chakrabarti S, Ma N, Sima AA (1991) Anionic sites in diabetic basement membranes and their possible role in diffusion barrier abnormalities in the BB-rat. Diabetologia 34:301–306

    Google Scholar 

  • Edwards JS, Swales LS, Bate CM (1991) Development of nonneural elements in the central nervous system of Drosophila. Ann NY Acad Sci 633:615–616

    Google Scholar 

  • Flower NE (1986) Sealing junctions in number of arachnid tissues. Tissue Cell 18:899–913

    Google Scholar 

  • Flower NE, Filshie BK (1975) Junctional structures in the midgut cells of lepidopteran caterpillars. J Cell Sci 17:221–239

    Google Scholar 

  • Forsman CA, Elfvin LG (1987) The ultrastructure of membranes in sympathetic ganglia. Scanning Microsc 1:191–205

    Google Scholar 

  • Fristrom DK (1982) Septate junctions in imaginal disks of Drosophila: a model for the redistribution of septa during cell rearrangement. J Cell Biol 94:77–87

    Google Scholar 

  • 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 9:2402–2411

    Google Scholar 

  • Juang JL, Carlson SD (1992 a) Fine structure and blood-brain properties of the central nervous system of a dipteran maggot. J Comp Neurol 324:343–352

    Google Scholar 

  • Juang JL, Carlson SD (1992 b) A blood-brain barrier without tight junctions in the fly central nervous system in the early postembryonic stage. Cell Tissue Res 270:95–103

    Google Scholar 

  • Kazama T, Oguro K, Sato Y (1989) Effect of enzyme digestion on anionic sites and charge-selective permeability of dermo-epidermal junction. J Invest Dermatol 93:814–817

    Google Scholar 

  • Klämbt C, Goodman CS (1991) Role of midline glia and neurons in the formation of the axon commissures in the central nervous system of the Drosophila embryo. Ann NY Acad Sci 633:142–159

    Google Scholar 

  • Kogaya Y, Nanci A (1992) Post-embedding staining with high-iron diamine-thiocarbohydrazide-silver protein and its application to visualizing sulfated glycoconjugates in cryofixed kidney and cartilage. J Histochem Cytochem 40:1257–1267

    Google Scholar 

  • Lane NJ, Treherne TE (1972) Studies on perineurial junctional complexes and the sites of uptake of microperoxidase and lanthanum in the cockroach central nervous system. Tissue Cell 4:427–436

    Google Scholar 

  • Lane NJ, Treherne JE (1980) Functional organization of arthropod glia. In: Locke M, Smith DS (eds) Insect biology in the future, “VBW 80”. Academic Press, New York, pp 765–795

    Google Scholar 

  • Lawrence PA, Green SM (1975) The anatomy of a compartment border: the intersegmental boundary in Oncopeltus. J Cell Biol 65:373–382

    Google Scholar 

  • Loewenstein WR (1981) Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev 61:829–913

    Google Scholar 

  • Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic Press, San Diego

    Google Scholar 

  • Rounds S, Vaccaro CA (1987) The binding of cationic probes to apical and basal surface of rat lung capillary endothelium and endothelial cells in tissue culture. Am Rev Respir Dis 135:725–730

    Google Scholar 

  • Ruangvoravat CP, Lo CW (1992) Restrictions in gap junctional communication in the Drosophila larval epidermis. Dev Dyn 193:70–82

    Google Scholar 

  • Ryerse JS (1989) Electron microscope immunolocation of gap junctions in Drosophila. Tissue Cell 21:835–839

    Google Scholar 

  • Ryerse JS (1991) Gap junction protein tissue distribution and abundance in the adult brain in Drosophila. Tissue Cell 23:709–718

    Google Scholar 

  • Ryerse JS, Nagel BA (1984) Gap junction distribution in the Drosophila wing disc mutants vg, l(2)gd, l(3)c43hs1, and l(2)gl14. Dev Biol 105:396–403

    Google Scholar 

  • Saint Marie RL, Carlson SD (1985) Interneuronal and glial-neuronal gap junctions in the lamina ganglionaris of the compound eye of the housefly, Musca domestica. Cell Tissue Res 241:43–52

    Google Scholar 

  • Skutelsky E, Roth J (1986) Cationic colloidal gold: a new probe for the detection of anionic cell surfaces by electron microscopy. J Histochem Cytochem 34:693–696

    Google Scholar 

  • Spray DC, Cherbas L, Cherbas P, Morales EA, Carrow GM (1989) Ionic coupling and mitotic synchrony of sibling in a Drosophila cell line. Exp Cell Res 184:509–517

    Google Scholar 

  • Swales LS, Lane NJ (1985 a) Embryonic development of glial cells and their junctions in the locust central nervous system. J Neurosci 5:117–127

    Google Scholar 

  • Swales LS, Lane NJ (1985 b) Unusual structural features and assembly of gap and pleated septate junctions in embryonic cockroach CNS. J Cell Sci 76:269–281

    Google Scholar 

  • Treherne JE (1985) Blood-brain barrier. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 5, Pergamon Press, Oxford, pp 115–137

    Google Scholar 

  • Vorbrodt AW (1987) Demonstration of anionic sites on the luminal and abluminal fronts of endothelial cells with poly-L-lysine-gold complex. J Histochem Cytochem 35:1261–1266

    Google Scholar 

  • Vorbrodt AW, Lossinsky AS, Dobrogowska DH, Wisniewski HM (1990) Sequential appearance of anionic domains in the developing blood-brain barrier. Dev Brain Res 52:31–37

    Google Scholar 

  • Weir MP, Lo CW (1984) Gap-junctional communication compartments in the Drosophila wing imaginal disk. Dev Biol 102:130–146

    Google Scholar 

  • Wood RL, Kuda AM (1980) Formation of junctions in regenerating hydra: septate junctions. J Ultrastruct Res 70:104–117

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Juang, JL., Carlson, S.D. Analog of vertebrate anionic sites in blood-brain interface of larval Drosophila . Cell Tissue Res 277, 87–95 (1994). https://doi.org/10.1007/BF00303084

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00303084

Key words

Navigation