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Photomechanical Responses in Drosophila Photoreceptors

Science  12 Oct 2012:
Vol. 338, Issue 6104, pp. 260-263
DOI: 10.1126/science.1222376

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Feeling the Light

There has been a link missing in our understanding of the biochemical signaling mechanism initiated when photons are absorbed by rhodopsin in the photoreceptor cells of Drosophila eyes. Photoisomerization of rhodopsin activates a heterotrimeric guanine nucleotide—binding protein which leads to activation of phospholipase C. But how phospholipase C activates the transient receptor potential (TRP) or the transient receptor potential–like (TRPL) ion channels that produce the rest of the cellular response has been unclear. Hardie and Franze (p. 260; see the Perspective by Liman) propose that there is a physical mechanism at work. Atomic force microscopy revealed light-induced contractions of photoreceptor cells. Consistent with a physical coupling mechanism, manipulations of the membrane altered responses of the photoreceptor cells to light. Thus, physical changes in the membrane appear to couple phospholipase C activity to the opening of mechanosensitive TRP and TRPL channels.

Abstract

Phototransduction in Drosophila microvillar photoreceptor cells is mediated by a G protein–activated phospholipase C (PLC). PLC hydrolyzes the minor membrane lipid phosphatidylinositol 4,5-bisphosphate (PIP2), leading by an unknown mechanism to activation of the prototypical transient receptor potential (TRP) and TRP-like (TRPL) channels. We found that light exposure evoked rapid PLC-mediated contractions of the photoreceptor cells and modulated the activity of mechanosensitive channels introduced into photoreceptor cells. Furthermore, photoreceptor light responses were facilitated by membrane stretch and were inhibited by amphipaths, which alter lipid bilayer properties. These results indicate that, by cleaving PIP2, PLC generates rapid physical changes in the lipid bilayer that lead to contractions of the microvilli, and suggest that the resultant mechanical forces contribute to gating the light-sensitive channels.

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