Skip to main content
SpringerLink
Log in

Rab11 is required for embryonic nervous system development in Drosophila

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

Abstract

In eukaryotes, membrane trafficking is regulated by the small monomeric GTPases of Rab protein family. Rab11, an evolutionary conserved, ubiquitously expressed subfamily of the Rab GTPases, has been implicated in the regulation of vesicular trafficking through the recycling of endosomes. To dissect out the role of this protein during embryonic nervous system development, we have studied the expression pattern of Rab11 in the ventral nerve cord during neuronal differentiation in the Drosophila embryo. When the dominant-negative or constitutively-active mutant DRab11 proteins are expressed in neurons, or when homozygous mutant Rab11 embryos are analyzed, defects are found in the developing central nervous system, along with disorganization and misrouting of embryonic axons. Our results provide the first in vivo evidence that Rab11 is involved in the development of the nervous system during Drosophila embryogenesis.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Abdelilah-Seyfried S, Chan YM, Zeng C, Justice NJ, Younger-Shepherd S, Sharp LE, Barbel S, Meadows SA, Jan LY, Jan YN (2000) A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 155:733–752

    PubMed  CAS  Google Scholar 

  • Alone DP, Tiwari AK, Mandal L, Li M, Mechler BM, Roy JK (2005) Rab11 is required during Drosophila eye development. Int J Dev Biol 49:873–879

    Article  PubMed  CAS  Google Scholar 

  • Bogard N, Lan L, Xu J, Cohen RS (2007) Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development 134:3413–3418

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanoaster. Springer, New York

    Google Scholar 

  • Dollar G, Struckhoff E, Michaud J, Cohen RS (2002) Rab11 polarization of the Drosophila oocyte: a novel link between membrane trafficking, microtubule, and oskar mRNA localization and translation. Development 129:517–526

    PubMed  CAS  Google Scholar 

  • Emery G, Hutterer A, Berdnik D, Mayer B, Wirtz-Peitz F, Gaitan MG, Knoblich JA (2005) Asymmetric Rab11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122:763–773

    Article  PubMed  CAS  Google Scholar 

  • Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci USA 79:7929–7933

    Article  PubMed  CAS  Google Scholar 

  • Giansanti MG, Belloni G, Gatti M (2007) Rab11 is required for membrane trafficking and actomyosin ring constriction in meiotic cytokinesis of Drosophila males. Mol Biol Cell 18:5034–5047

    Article  PubMed  CAS  Google Scholar 

  • Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45–57

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo A, Brand AH (1997) Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development 124:3253–3262

    PubMed  CAS  Google Scholar 

  • Hummel T, Krukkert K, Roos J, Davis G, Klambt C (2000) Drosophila Futsch/22C10 is a MAP1B like protein required for dendritic and axonal development. Neuron 26:357–370

    Article  PubMed  CAS  Google Scholar 

  • Jafar-Nejad H, Andrews HK, Acar M, Bayat V, Wirtz-Peitz F, Mehta SQ, Knoblich JA, Bellen HJ (2005) Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev Cell 9:351–363

    Article  PubMed  CAS  Google Scholar 

  • Jankovics F, Sinka R, Erdélyi M (2001) An interaction type of genetic screen reveals a role of the Rab11 gene in oskar mRNA localization in the developing Drosophila melanogaster oocyte. Genetics 158:1177–1188

    PubMed  CAS  Google Scholar 

  • Lighthouse DV, Buszczak M, Spradling AC (2008) New components of the Drosophila fusome suggest it plays novel roles in signalling and transport. Dev Biol (in press)

  • Lin DM, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS (1994) Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation and altered. Neuron 13:1055–1069

    Article  PubMed  CAS  Google Scholar 

  • Pelissier A, Chauvin JP, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13:1848–1857

    Article  PubMed  CAS  Google Scholar 

  • Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD (1998) Hydrolysis of GTP on rab11 is required for the direct delivery of transferring from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 95:6187–6192

    Article  PubMed  CAS  Google Scholar 

  • Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, Gould GW, Sullivan W (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol 163:143–154

    Article  PubMed  CAS  Google Scholar 

  • Riggs B, Fasulo B, Royou A, Mische S, Cao J, Hays TS, Sullivan W (2007) The concentration of Nuf, a Rab11 effector, at the microtubule-organizing center is cell cycle regulated, dynein-dependent, and coincides with furrow formation. Mol Biol Cell 18:3313–3322

    Article  PubMed  CAS  Google Scholar 

  • Satoh AK, O’Tousa JE, Ozaki K, Ready DF (2005) Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132:1487–1497

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tear G (1999) Neuronal guidance: a genetic perspective. Trends Genet 15:113–118

    Article  PubMed  CAS  Google Scholar 

  • Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1133

    Article  PubMed  CAS  Google Scholar 

  • Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericetriolar recycling endosome. J Cell Biol 135:913–924

    Article  PubMed  CAS  Google Scholar 

  • Van Vactor D (1999) Axon guidance. Curr Biol 9:R797–R799

    Article  PubMed  Google Scholar 

  • Van Vactor D, Kopczynski C (1999) Techniques for anatomical analysis of the Drosophila embryonic nervous system. In: Richter J (ed) A comparative methods approach to the study of oocytes and embryos. Oxford University Press, New York, pp 490–513

    Google Scholar 

  • Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J (2000) Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 151:1207–1220

    Article  PubMed  CAS  Google Scholar 

  • Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to M. Gonzales-Gaitan, D. Ready, and the Bloomington Drosophila stock centre (Indiana) for fly stocks and to the Developmental Studies Hybridoma Bank (University of Iowa) for antibodies. We also extend our thanks to the National Scanning Confocal Microscopy Facility (sponsored by DST).

Author information

Authors and Affiliations

  1. Cytogenetics Laboratory, Department of Zoology, Banaras Hindu University, Varanasi, 221 005, India

    Tanmay Bhuin & Jagat K. Roy

Authors
  1. Tanmay Bhuin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jagat K. Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jagat K. Roy.

Additional information

This work was supported by the DST (to J.K.R.) and SRF from ICMR, New Delhi (to T.B.).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhuin, T., Roy, J.K. Rab11 is required for embryonic nervous system development in Drosophila . Cell Tissue Res 335, 349–356 (2009). https://doi.org/10.1007/s00441-008-0711-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-008-0711-8

Keywords

Search

Navigation