Skip to main content

Temporal and spatial expression of Drosophila Neurexin during the life cycle visualized using a DNRX-Gal4/UAS-reporter

Abstract

Drosophila neurexin (DNRX) plays a critical role in proper architecture development and synaptic function in vivo. However, the temporal and spatial expression pattern of DNRX still remains unclear. For this study, we generated a novel Drosophila transgenic strain termed the DNRX-Gal4 transgenic line, with characteristic features in agreement with the endogenous DNRX expression pattern. DNRX expression was examined by driving the expression of a GFP reporter (nuclear-localized and membrane- localized GFP) using the DNRX-Gal4 promoter. We found that DNRX was expressed preferentially in central and motor neurons in embryos, larvae and adults, but not in glial cells. DNRX was expressed in pre- and post-synaptic areas in third instar larvae neuromuscular junctions (NMJs). Reporter expression was also observed in the salivary glands, guts, wings and legs of adult flies. In the adult brain, reporter expression was observed throughout several brain regions, including the mushroom body (MBs), antennal lobe (AL) and optic lobe neurons, which is consistent with endogenous DNRX expression via antibody staining. Interestingly, DNRX was also expressed in clock neurons. Meanwhile, we found that DNRX expression in the MBs was required for olfactory learning and memory.

References

  1. Akalal, D.B., Wilson, C.F., Zong, L., Tanaka, N.K., Ito, K., and Davis, R.L. (2006). Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn Mem 13, 659–668.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  2. Chen, K., Gracheva, E.O., Yu, S.C., Sheng, Q., Richmond, J., and Featherstone, D.E. (2010). Neurexin in embryonic Drosophila neuromuscular junctions. PloS One 5, e11115.

    PubMed Central  Article  PubMed  Google Scholar 

  3. Dean, C., Scholl, F.G., Choih, J., DeMaria, S., Berger, J., Isacoff, E., and Scheiffele, P. (2003). Neurexin mediates the assembly of presynaptic terminals. Nature Neurosci 6, 708–716.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  4. Graf, E.R., Zhang, X., Jin, S.X., Linhoff, M.W., and Craig, A.M. (2004). Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013–1026.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  5. Huang, W.L., Tung, C.W., Liaw, C., Huang, H.L., and Ho, S.Y. (2014). Rule-based knowledge acquisition method for promoter prediction in human and Drosophila species. Sci World J 2014, 327306.

    Google Scholar 

  6. Li, J., Ashley, J., Budnik, V., and Bhat, M.A. (2007). Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron 55, 741–755.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  7. McGuire, S.E., Le, P.T., and Davis, R.L. (2001). The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330–1333.

    Article  CAS  PubMed  Google Scholar 

  8. Missler, M., Fernandez-Chacon, R., and Sudhof, T.C. (1998). The making of neurexins. J Neurochem 71, 1339–1347.

    Article  CAS  PubMed  Google Scholar 

  9. Missler, M., Zhang, W., Rohlmann, A., Kattenstroth, G., Hammer, R.E., Gottmann, K., and Sudhof, T.C. (2003). Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423, 939–948.

    Article  CAS  PubMed  Google Scholar 

  10. Reese, M.G. (2001). Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Com Chem 26, 51–56.

    Article  CAS  Google Scholar 

  11. Sharma, Y., Cheung, U., Larsen, E.W., and Eberl, D.F. (2002). PPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in drosophila. Genesis 34, 115–118.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  12. Sun, M., Liu, L., Zeng, X., Xu, M., Liu, L., Fang, M., and Xie, W. (2009). Genetic interaction between Neurexin and CAKI/CMG is important for synaptic function in Drosophila neuromuscular junction. Neurosci Res 64, 362–371.

    Article  CAS  PubMed  Google Scholar 

  13. Sun, M., Xing, G., Yuan, L., Gan, G., Knight, D., With, S.I., He, C., Han, J., Zeng, X., Fang, M., Boulianne, G.L., and Xie, W. (2011). Neuroligin 2 is required for synapse development and function at the Drosophila neuromuscular junction. J Neurosci 31, 687–699.

    Article  CAS  PubMed  Google Scholar 

  14. Tabuchi, K., and Sudhof, T.C. (2002). Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 79, 849–859.

    Article  CAS  PubMed  Google Scholar 

  15. Tian, Y., Li, T., Sun, M., Wan, D., Li, Q., Li, P., Zhang, Z.C., Han, J., and Xie, W. (2013). Neurexin regulates visual function via mediating retinoid transport to promote rhodopsin maturation. Neuron 77, 311–322.

    Article  CAS  PubMed  Google Scholar 

  16. Tully, T., and Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A, 157, 263–277.

    Article  CAS  PubMed  Google Scholar 

  17. Zeng, X., Sun, M., Liu, L., Chen, F., Wei, L., and Xie, W. (2007). Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett 581, 2509–2516.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mingkuan Sun.

Additional information

This article is published with open access at link.springer.com

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sun, M., Zeng, X. & Xie, W. Temporal and spatial expression of Drosophila Neurexin during the life cycle visualized using a DNRX-Gal4/UAS-reporter. Sci. China Life Sci. 59, 68–77 (2016). https://doi.org/10.1007/s11427-015-4946-9

Download citation

Keywords

  • Drosophila
  • neurexin
  • Gal4
  • motor neuron
  • NMJs