Skip to main content
SpringerLink
Log in

Functioning of glia and neurodegeneration in Drosophila melanogaster

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

The views on the role of glial tissue have changed greatly since the first studies in the field. The cells once regarded as “cell glue” have been shown to play important roles in development, trophic processes, production of navigation signals for axon growth, electric insulation of neurons, creation of a barrier between the brain and the hemolymph, control of extracellular homeostasis, and physiological functioning of the brain. Researchers all over the world are currently turning to Drosophila melanogaster, a well-characterized model organism in genetics, in order to investigate multiple molecular aspects of neurodegeneration processes, since the modeling of neurodegeneration mechanisms in Drosophila has a number of advantages. Fruit flies with a mutation in the swiss cheese (sws) gene show degeneration of neurons and surface glia cells of the optical lobe, and the protein product of the sws gene is essential for maintaining the functionality and integrity of the fly brain. The present review addresses the role of glial cells in Drosophila brain development and in the functioning of the adult fly brain as well as the pattern of expression of the gene sws and the distribution of the product of this gene in neurons and glia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Gilbert, L, Drosophila is an inclusive model for human diseases, growth and development, Mol. Cell. Endocrinol., 2008, vol. 24, nos. 1–2, pp. 25–31.

    Article  Google Scholar 

  2. Muqit, M.K. and Feany, M.B, Modelling neurodegenerative diseases in Drosophila: a fruitful approach?, Nat. Rev. Neurosci., 2002, vol. 3, no. 3, pp. 237–243.

    Article  CAS  PubMed  Google Scholar 

  3. Chakraborty, R., Vepuri, V., Mhatre, S.D., Paddock, B.E., Miller, S., Michelson, S.J., Delvadia, R., Desai, A., Vinokur, M., Melicharek, D.J., Utreja, S., Khandelwal, P., Ansaloni, S., Goldstein, L.E., Moir, R.D., Lee, J.C., Tabb, L.P., Saunders, A.J., and Marenda, D.R, Characterization of a Drosophila Alzheimer’s disease model: pharmacological rescue of cognitive defects, PLoS One, 2011, vol. 6, no. 6, p. e20799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Gruenewald, C., Botella, J.A., Bayersdorfer, F., Navarro, J.A., and Schneuwly, S., Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster, Free Radic. Biol. Med., 2009, vol. 46, no. 12, pp. 1668–1676.

    Article  CAS  PubMed  Google Scholar 

  5. Moloney, A., Sattelle, D.B., Lomas, D.A., and Crowther, D.C., Alzheimer’s disease: insights from Drosophila melanogaster models, Trends Biochem. Sci., 2010, vol. 35, no. 4, pp. 228–235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Edenfeld, G., Stork, T., and Klambt, C, Neuronglia interaction in the insect nervous system, Curr. Opin. Neurobiol., 2005, vol. 15, no. 1, pp. 34–39.

    Article  CAS  PubMed  Google Scholar 

  7. Edwards, T.N. and Meinertzhagen, I.A, The functional organization of glia in the adult brain of Drosophila and other insects, Prog. Neurobiol., 2010, vol. 90, no. 4, pp. 471–497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Awasaki, T., Lai, S.L., Ito, K., and Lee, T, Organization and postembryonic development of glial cells in the adult central brain of Drosophila, J. Neurosci., 2008, vol. 28, no. 51, pp. 13742–13753.

    Article  CAS  PubMed  Google Scholar 

  9. Tix, S., Eule, E., Fischbach, K.F., and Benzer, S, Glia in the chiasms and medulla of the Drosophila melanogaster optic lobes, Cell Tissue Res., 1997, vol. 289, no. 3, pp. 397–409.

    Article  CAS  PubMed  Google Scholar 

  10. Kretzschmar, D. and Pflugfelder, G.O, Glia in development, function, and neurodegeneration of the adult insect brain, Brain Res. Bull., 2002, vol. 57, no. 1, pp. 121–131.

    CAS  PubMed  Google Scholar 

  11. Bastiani, M.J., Lac, S., and Goodman, C.S, Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of a specific axonal pathway by the pCC neuron, J. Neurosci., 1986, vol. 6, no. 12, pp. 3518–3531.

    Article  CAS  PubMed  Google Scholar 

  12. Braitenberg, V, Patterns of projection in the visual system of the fly. I. Retina-lamina projections, Exp. Brain Res., 1967, vol. 3, no. 3, pp. 271–298.

    Article  CAS  PubMed  Google Scholar 

  13. Andrzejak, J., Glia-related circadian plasticity in the visual system of Diptera, Front. Physiol., 2013, vol. 4, pp. 1–8.

    Google Scholar 

  14. Strausfeld, N.J., Atlas of an Insect Brain, Berlin: Springer, 1976.

    Book  Google Scholar 

  15. Borycz, J., Borycz, J.A., Loubani, M., and Meinertzhagen, I.A, Tan and ebony genes regulate a novel path-way for transmitter metabolism at fly photoreceptor terminals, J. Neurosci., 2002, vol. 22, pp. 10549–10557.

    Article  CAS  PubMed  Google Scholar 

  16. Borycz, J.A., Borycz, J., Kubow, A., Kostyleva, R., and Meinertzhagen, I.A, Histamine compartments of the Drosophila brain with an estimate of the quantum content at the photoreceptor synapse, J. Neurophysiol., 2005, vol. 93, no. 3, pp. 1611–1619.

    Article  CAS  PubMed  Google Scholar 

  17. Greer, C.L., Grygoruk, A., Patton, D.E., Ley, B., Romero-Calderon, R., Chang, H.Y., Houshyar, R., Bainton, R.J., Diantonio, A., and Krantz, D.E., A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine, J. Neurobiol., 2005, vol. 64, pp. 239–258.

    Article  CAS  PubMed  Google Scholar 

  18. Romero-Calderon, R., Uhlenbrock, G., Borycz, J., Simon, A.M., Grygoruk, A., Yee, S.K., Shyer, A., Ackerson, L.C., Meidment, N.T., Meinertzhagen, I.A., Hovemann, B.T., and Krantz, D.E., A glial variant of the vesicular monoamine transporter is required to store histamine in the Drosophila visual system, PLoS Genet., 2008, vol. 4, no. 11, p. e1000245.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Rival, T., Soustelle, L., Stambi, C., Besson, M.T., Iche, M., and Birman, S., Decreasing glutamate buffering capacity ttrigers oxidative stress and neuropile degeneration in the Drosophila brain. Curr. Biol., 2004, vol. 14, no. 7, pp. 599–605.

    Article  CAS  PubMed  Google Scholar 

  20. Lievens, J.C., Rival, T., Iche, M., Chneiweiss, H., and Birman, S, Expanded polyglutamine peptides disrupt EGF receptor signaling and glutamate transporter expression in Drosophila, Hum. Mol. Genet., 2005, vol. 14, no. 5, pp. 713–724.

    Article  CAS  PubMed  Google Scholar 

  21. Pyza, E. and Gorska-Andrzejak, J., Involvement of glial cells in rhythmic size changes in neurons of the housefly’s visual system, J. Neurobiol., 2004, vol. 59, no. 2, pp. 205–215.

    Article  PubMed  Google Scholar 

  22. Lessing, D. and Bonini, N.M, Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants, Nat. Rev. Genet., 2009, vol. 10, pp. 359–370.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hotta, Y. and Benzer, S, Mapping of behaviour in Drosophila mosaics, Nature, 1972, vol. 240, pp. 527–535.

    Article  CAS  PubMed  Google Scholar 

  24. Benzer, S, Behavioral mutants of Drosophila isolated by countercurrent distribution, Proc. Natl. Acad. Sci. U. S. A., 1967, vol. 58, no. 3, pp. 1112–1119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Heisenberg, M. and Bohl, K, Isolation of anatomical brain mutants of Drosophila by histological means, Z. Naturfors. C. Biosci., 1979, vol. 34, nos. 1–2, pp. 143–147.

    Article  Google Scholar 

  26. Coombe, P.E. and Heisenberg, M, The structural brain mutant vacuolar medulla of Drosophila melanogaster with specific behavioral defects and cell degeneration in the adult, J. Neurogenet., 1986, vol. 3, no. 3, pp. 135–158.

    Article  CAS  PubMed  Google Scholar 

  27. Kretzschmar, D, Neurodegenerative mutants in Drosophila: a means to identify genes and mechanisms involved in human disease?, Invert. Neurosci., 2005, vol. 5, no. 3, pp. 97–109.

    Article  CAS  PubMed  Google Scholar 

  28. Kretzschmar, D, Swiss cheese et allii, some of the first neurodegenerative mutants isolated in Drosophila, J. Neurogenet., 2009, vol. 23, nos. 1–2, pp. 34–41.

    CAS  PubMed  Google Scholar 

  29. Kretzschmar, D., Hasan, G., Sharma, G., Heisenberg, M., and Benzer, S, The Swiss cheese mutant causes glial hyperwraping and brain degeneration in Drosophila, J. Neurosci., 1997, vol. 17, no. 19, pp. 7425–7432.

    Article  CAS  PubMed  Google Scholar 

  30. Brand, A.H. and Perrimon, N, Targeted gene expression as a means of altering cell fates and generating dominant phenotypes, Development, 1993, vol. 118, no. 2, pp. 401–415.

    CAS  PubMed  Google Scholar 

  31. Osterwalder, T., Yoon, K.S., White, B.H., and Keshishian, H., A conditional tissue-specific transgene expression system using inducible GAL4, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, no. 2, pp. 12596–12601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Muehlig-Versen, M., Cruz, A.B., Moser, M., Buttner, R., Athenstaedt, K., Glynn, P., and Kretzshmar, D, Loss of Swiss cheese/neuropathy target esterase activity causes disruption of phosphatidylcholine homeostasis and neuronal and glial death in adult Drosophila, J. Neurosci., 2005, vol. 25, no. 11, pp. 2865–2873.

    Article  CAS  Google Scholar 

  33. Dutta, S., Rieche, F., Eckl, N., Duch, C., and Kretzshmar, D, Glial expression of Swiss cheese (SWS), the Drosophila orthologue of neuropathy target esterase (NTE), is required for neuronal ensheathment and function, Dis. Model Mech., 2016, vol. 9, no. 3, pp. 283–294.

    CAS  Google Scholar 

  34. Hasan, G, Molecular cloning of an olfactory gene from Drosophila melanogaster, Proc. Natl. Acad. Sci. U. S. A., 1990, vol. 87, no. 22, pp. 9037–9041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. www.modencode.org.

  36. Johnson, M.K, The delayed neurotoxic effect of some organophosphorus compounds: identification of the phosphorylation site as an esterase, Biochem. J., 1969, vol. 114, no. 4, pp. 711–714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lush, M.J., Li, Y., Read, D.J., Willis, A.C., and Glynn, P, Neuropathy target esterase and a homologous Drosophila neurodegeneration-associated mutant protein contain a novel domain conserved from bacteria to man, Biochem. J., 1998, vol. 332, pp. 1–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lotti, M, The pathogenesis of organophosphate polyneuropathy, Crit. Rev. Toxicol., 1992, vol. 21, no. 6, pp. 465–487.

    Article  CAS  Google Scholar 

  39. Moser, M., Li, Y., Vaupel, K., Kretzshmar, D., Kluge, R., Glynn, P., and Buettner, R, Placental failure and impaired vasculogenesis result in embryonic lethality for neuropathy target esterase-deficient mice, Mol. Cell Biol., 2004, vol. 24, no. 4, pp. 1667–1679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Johnson, M.K, Organophosphates and delayed neuropathy— is NTE alive and well?, Toxicol. Appl. Pharmacol., 1990, vol. 102, no. 3, pp. 385–399.

    Article  CAS  PubMed  Google Scholar 

  41. Glynn, P, Axonal degeneration and neuropathy target esterase, Arh. Hig. Rada. Toksikol., 2007, vol. 58, pp. 355–358.

    Article  CAS  PubMed  Google Scholar 

  42. Glynn, P, Neuropathy target esterase and phospholipid deacylation, Biochim. Biophys. Acta, 2005, vol. 1736, no. 2, pp. 87–93.

    Article  CAS  PubMed  Google Scholar 

  43. Li, Y., Dinsdale, D., and Glynn, P, Protein domains, catalytic activity, and subcellular distribution of neuropathy target esterase in mammalian cells, J. Biol. Chem., 2003, vol. 278, no. 10, pp. 8820–8825.

    CAS  PubMed  Google Scholar 

  44. Akassoglou, K., Malester, B., Xu, J., Tessarollo, L., Rosenbluth, J., and Chao, M.V., Brain-specific deletion of neuropathy target esterase/Swiss cheese results in neurodegeneration, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 14, pp. 75–80.

    Article  Google Scholar 

  45. Zaccheo, O., Dinsdale, D., Meacock, P., and Glynn, P, Neuropathy target esterase and its yeast homologue degrade phosphatidylcholine to glycerophosphocholine in living cells, J. Biol. Chem., 2004, vol. 279, no. 23, pp. 24024–24033.

    Article  CAS  PubMed  Google Scholar 

  46. Cui, Z. and Houweling, M, Phosphatidylcholine and cell death, Biochim. Biophys. Acta, 2002, vol. 1585, nos. 2–3, pp. 87–96.

    Article  CAS  PubMed  Google Scholar 

  47. Fergestad, T., Ganetzky, B., and Palladino, M.J, Neuropathology in Drosophila membrane excitability mutants, Genetics, 2006, vol. 172, no. 2, pp. 1031–1042.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Jackowski, S., Wang, J., and Baburina, I, Activity of the phosphatydylcholine biosynthetic pathway modulates the disruption of fatty acids into glycerolipids in proliferating cells, Biochim. Biophys. Acta, 2000, vol. 1483, no. 3, pp. 301–315.

    Article  CAS  PubMed  Google Scholar 

  49. Klein, J, Membrane breakdown in acute and chronic neurodegeneration: focus on choline-containing phospholipids, J. Neural. Transm., 2000, vol. 107, nos. 8–9, pp. 1027–1063.

    Article  CAS  PubMed  Google Scholar 

  50. Van der Sanden, M.H., Houweling, M, Van Golde, L.M., and Vaandrager, A.B., Inhibition of phosphatidylcholine synthesis induces expression of the endoplasmic reticulum stress and apoptosis-related protein CCAAT/enhancer-binding protein-homologous protein (CHOP/GADD153), Biochem. J., 2003, vol. 369, pp. 643–650.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Du, C., Zhao, Q., Araki, S., Zhang, S., and Miao, J, Apoptosis mediated be phosphatidylcholine-specific phospholipase c is associated with camp,p53 level,and cell-cycle distribution in vascular endothelial cells, Endothelium, 2003, vol. 10, no. 3, pp. 141–147.

    Article  CAS  PubMed  Google Scholar 

  52. Xie, Z., Fang, M., and Bankaitis, V.A, Evidence of intrinsic toxicity of phosphatidylcholine to Sec14pdependent protein transport from the yeast Golgi complex, Mol. Biol. Cell, 2001, vol. 12, no. 4, pp. 1117–1129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. FlyBase: The Drosophila Database, Nucleic Acids Res., 1996, vol. 24, no. 1, pp. 53–56.

  54. Griffiths, I., Klugmann, M., Anderson, T., Yool., D., Thomson, C., Schwab, M.H., Schneider, A., Zimmermann, F., McCulloch, M., Nadon, N., and Nave, K.A, Axonal swellings and degeneration in mice lacking the major proteolipid of myelin, Science, 1998, vol. 280, no. 5369, pp. 1610–1613.

    Article  CAS  PubMed  Google Scholar 

  55. Von Mering, C., Jensen, L.J., Snel, B., Hooper, S.D., Krupp, M., Foglierini, M., Jouffre, N., Huynen, M.A., and Bork, P., STRING: Known and predicted proteinprotein interactions, integrated and transferred across organisms. Nucleic Acids Res., 2005, vol. 33 (database issue), pp. D433–D434.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Ivan Franko National University, Lviv, Ukraine

    I. I. Mohylyak & Ya. I. Chernyk

Authors
  1. I. I. Mohylyak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya. I. Chernyk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ya. I. Chernyk.

Additional information

Original Ukrainian Text © I.I. Mohylyak, Ya.I. Chernyk, 2017, published in Tsitologiya i Genetika, 2017, Vol. 51, No. 3, pp. 66–78.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mohylyak, I.I., Chernyk, Y.I. Functioning of glia and neurodegeneration in Drosophila melanogaster. Cytol. Genet. 51, 202–213 (2017). https://doi.org/10.3103/S0095452717030094

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452717030094

Keywords

Search

Navigation