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Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses

Nature volume 395, pages 805–808 (1998)Cite this article

Abstract

The subcellular compartmentalization of signalling molecules helps to ensure the selective activation of different signal-transduction cascades within a single cell1. Although there are many examples of compartmentalized signalling molecules, there are few examples of entire signalling cascades being organized as distinct signalling complexes. In Drosophila photoreceptors, the InaD protein, which consists of five PDZ domains, functions as a multivalent adaptor that brings together several components of the phototransduction cascade into a macromolecular complex2,3,4,5. Here we study single-photon responses in several photoreceptor mutant backgrounds, and show that the InaD macromolecular complex is the unit of signalling that underlies elementary responses. We show that the localized activity of this signalling unit promotes reliable single-photon responses as well as rapid activation and feedback regulation. Finally, we use genetic andelectrophysiological tools to illustrate how the assembly of signalling molecules into a transduction complex limits signal amplification in vivo.

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Figure 1: Disrupting the InaD signalling complex disrupts quantum bumps.
Figure 2: A quantum bump is an organized unit of signalling.
Figure 3: Amplification occurs downstream of PLC activation.

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References

  1. Tsunoda, S., Sierralta, J. & Zuker, C. Specificity in signaling pathways: assembly into multimolecular signaling complexes. Curr. Opin. Genet. Dev. 8, 419–422 (1998).

    Article  CAS  Google Scholar 

  2. Tsunoda, S. et al. Amultivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388, 243–249 (1997).

    Article  ADS  CAS  Google Scholar 

  3. Chevesich, J., Kreuz, A. J. & Montell, C. Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron 18, 95–105 (1997).

    Article  CAS  Google Scholar 

  4. Shieh, B. H. & Zhu, M. Y. Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16, 991–998 (1996).

    Article  CAS  Google Scholar 

  5. Huber, A. et al. The transient receptor potential protein (Trp), a putative store-operated Ca2+ channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J. 15, 7036–7045 (1996).

    Article  CAS  Google Scholar 

  6. Ranganathan, R., Malicki, D. M. & Zuker, C. S. Signal transduction in Drosophila photoreceptors. Annu. Rev. Neurosci. 18, 283–317 (1995).

    Article  CAS  Google Scholar 

  7. Zuker, C. S. The biology of vision in Drosophila. Proc. Natl Acad. Sci. USA 93, 571–576 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Baylor, D. A., Lamb, T. D. & Yau, K.-W. Responses of retinal rods to single photons. J. Physiol. (Lond.) 288, 613–634 (1979).

    CAS  Google Scholar 

  9. Yeandle, S. Studies on the slow potential and the effect of cations on the electrical responses of Limulus ommatidium.Thesis, Johns Hopkins Univ.((1957)).

    Google Scholar 

  10. Fuortes, M. T. F. & Hodgkin, A. L. Changes in time scale and sensitivity in the ommatidia of Limulus. J. Physiol. 172, 239–263 (1964).

    Article  CAS  Google Scholar 

  11. Scott, K., Leslie, A., Sun, Y., Hardy, R. & Zuker, C. Gαq protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 15, 919–927 (1995).

    Article  CAS  Google Scholar 

  12. Niemeyer, B. A., Suzuki, E., Scott, K., Jalink, K. & Zuker, C. S. The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85, 651–659 (1996).

    Article  CAS  Google Scholar 

  13. Stieve, H. (ed.) Bumps, the Elementary Excitatory Responses of Invertebrates (Dahlem Konferenzen, Springer, Berlin, (1986)).

    Book  Google Scholar 

  14. Johnson, E. & Pak, W. Electrophysiological study of Drosophila rhodopsin mutants. J. Gen. Physiol. 88, 651–673 (1986).

    Article  CAS  Google Scholar 

  15. Scott, K., Sun, Y. M., Beckingham, K. & Zuker, C. S. Calmodulin regulation of Drosophila light-activated channels and receptor function mediates termination of the light response in vivo. Cell 91, 375–383 (1997).

    Article  CAS  Google Scholar 

  16. Reinke, R., Krantz, D. E., Yen, D. & Zipursky, S. L. Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52, 291–301 (1988).

    Article  CAS  Google Scholar 

  17. van Vactor, D. J, Krantz, D. E., Reinke, R. & Zipursky, S. L. Analysis of mutants in Chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52, 281–290 (1988).

    Article  CAS  Google Scholar 

  18. Pearn, M. T., Randall, L. L., Shortridge, R. D., Burg, M. G. & Pak, W. L. Molecular, biochemical, and electrohysiological characterization of Drosophila norpA mutants. J. Biol. Chem. 271, 4937–4945 (1996).

    Article  CAS  Google Scholar 

  19. Deland, M. C. & Pak, W. L. Reversibly temperature sensitive phototransduction mutant of Drosophila melanogaster. Nature 244, 84–86 (1973).

    Article  ADS  Google Scholar 

  20. Scott, K. & Zuker, C. Lights out: deactivation of the phototransduction cascade. Trends Biochem. Sci. 22, 350–354 (1997).

    Article  CAS  Google Scholar 

  21. Hardie, R. C. & Minke, B. Phosphoinositide-mediated phototransduction in Drosophila photoreceptors: the role of Ca2+ and trp. Cell Calcium 18, 256–274 (1995c).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank members of the Zuker lab for reading the manuscript and for discussions. C.S.Z. is an investigator of the Howard Hughes Medical Institute. This work was funded in part by a grant from the National Eye Institute.

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  1. Howard Hughes Medical Institute and Departments of Biology and Neurosciences, University of California at San Diego, La Jolla, 92093-0649, California, USA

    Kristin Scott & Charles S. Zuker

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  1. Kristin Scott
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Correspondence to Charles S. Zuker.

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Scott, K., Zuker, C. Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses. Nature 395, 805–808 (1998). https://doi.org/10.1038/27448

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