Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Drosophila central brain formation requires Robo proteins

  • 213 Accesses

  • 9 Citations

Abstract

The Robo proteins have been extensively studied in the Drosophila embryonic ventral nerve cord, in which their expression level controls the midline crossing and optic lobe formation, but nothing is known about their activities during adult central brain formation. We have analyzed how Robo guidance cues influence central complex (CX) and mushroom body (MB) formation. Mutations of robo2 and robo3 confer a series of strong MB and CX defects. We found that the Robo2 and Robo3 proteins are expressed in two structures of the developing CX, the fan-shaped body (FB) and the noduli (NO), and by fibers across the central neuropile. We conclude that the Robo2 and Robo3 receptors play postembryonic roles during central brain formation.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Battye R, Stevens A, Perry RL, Jacobs JR (2001) Repellent signaling by Slit requires the leucine-rich repeats. J Neurosci 21:4290–4298

  2. Boquet I, Hitier R, Dumas M, Chaminade M, Preat T (2000) Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. J Neurobiol 42:33–48

  3. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38–51

  4. Davis RL (1993) Mushroom bodies and Drosophila learning. Neuron 11:1–14

  5. Godenschwege TA, Simpson JH, Shan X, Bashaw GJ, Goodman CS, Murphey RK (2002) Ectopic expression in the giant fiber system of Drosophila reveals distinct roles for roundabout (Robo), Robo2, and Robo3 in dendritic guidance and synaptic connectivity. J Neurosci 22(8):3117–3129

  6. Hanesch U, Fischbarch KF, Heisenberg M (1989) Neural architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 457:343–366

  7. Heisenberg M (1998) What do the mushroom bodies do for the insect brain? An introduction. Learn Mem 5:1–10

  8. Heisenberg M, Boehl K (1979) Isolation of anatomical brain mutants of Drosophila by histological means. Z Naturforsch B 34c:143–147

  9. Isabel I, Pascual A, Preat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304:1024–1027

  10. Jacobs JR (2000) The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog Neurobiol 62:475–508

  11. Kaprielian Z, Runko E, Imondi R (2001) Axon guidance at the midline choice point. Dev Dyn 221:154–181

  12. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G (1998) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92:205–215

  13. Kurusu M, Awasaki T, Masuda-Nakagawa LM, Kawauchi H, Ito K, Furukubo-Tokunaga K (2002) Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 129:409–419

  14. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065–4076

  15. Noveen A, Daniel A, Hartenstein V (2000) Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 127:3475–3488

  16. Pascual A, Preat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115–1117

  17. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson BJ (2000a) Crossing the midline. Roles and regulation of Robo receptors. Neuron 28:767–777

  18. Rajagopalan S, Vivancos V, Nicolas E, Dickson BJ (2000b) Selecting a longitudinal pathway. Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103:1033–1045

  19. Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409–426

  20. Simpson JH, Bland KS, Fetter RD, Goodman CS (2000a) Short-range and long-range guidance by Slit and its Robo receptors. A combinatorial code of Robo receptors controls lateral position. Cell 103:1019–1032

  21. Simpson JH, Kidd T, Bland KS, Goodman CS (2000b) Short-range and long-range guidance by Slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 28:753–766

  22. Strausfeld NJ, Sinakevitch I, Vilinsky I (2003) The mushroom bodies of Drosophila melanogaster: an immunocytological and Golgi study of Kenyon cell organization in the calyces and lobes. Microsc Res Tech 62(2):151–169

  23. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13(5):1852–1861

  24. Tayler TD, Robichaux MB, Garrity PA (2004) Compartmentalization of visual centers in the Drosophila brain requires Slit and Robo proteins. Development 131(23):5935–5945

  25. Truman JW, Taylor BJ, Awad TA (1993) Formation of the adult nervous system. In: The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 1245–1276

  26. Wang J, Zugates CT, Liang IH, Lee CH, Lee T (2002) Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33:559–571

Download references

Acknowledgements

We thank B.J. Dickson for providing Robo2 and Robo3 antibodies and robo2 and robo3 fly stocks; R.L. Davis for the anti-DCO antibody; S. Brown and C. Talbot for confocal microscopy expertise; and G. Isabel, G. Didelot, and A. Pascual for their fruitful comments on the manuscript. This work was supported by research grants from the Association pour la Recherche contre le Cancer, the Ligue contre le Cancer, and the Human Frontier Science Program.

Author information

Correspondence to Emmanuelle Nicolas.

Additional information

Communicated by P. Simpson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nicolas, E., Preat, T. Drosophila central brain formation requires Robo proteins. Dev Genes Evol 215, 530–536 (2005). https://doi.org/10.1007/s00427-005-0009-8

Download citation

Keywords

  • Brain
  • Mushroom body
  • Drosophila
  • Metamorphosis
  • Robo