Ca2+-dependent metarhodopsin inactivation mediated by calmodulin and NINAC myosin III.
Phototransduction in flies is the fastest known G protein-coupled signaling cascade, but how this performance is achieved remains unclear. Here, we investigate the mechanism and role of rhodopsin inactivation. We determined the lifetime of activated rhodopsin (metarhodopsin = M( *)) in whole-cell recordings from Drosophila photoreceptors by measuring the time window within which inactivating M( *) by photoreisomerization to rhodopsin could suppress responses to prior illumination. M( *) was inactivated rapidly (tau approximately 20 ms) under control conditions, but approximately 10-fold more slowly in Ca2+-free solutions. This pronounced Ca2+ dependence of M( *) inactivation was unaffected by mutations affecting phosphorylation of rhodopsin or arrestin but was abolished in mutants of calmodulin (CaM) or the CaM-binding myosin III, NINAC. This suggests a mechanism whereby Ca2+ influx acting via CaM and NINAC accelerates the binding of arrestin to M( *). Our results indicate that this strategy promotes quantum efficiency, temporal resolution, and fidelity of visual signaling.
Liu
Che-Hsiung
CH
Department of Physiology, Development and Neuroscience, Cambridge University, Cambridge CB23DY, UK.
Satoh
Akiko K
AK
Postma
Marten
M
Huang
Jiehong
J
Ready
Donald F
DF
Hardie
Roger C
RC
D000367:Age Factors; D000818:Animals; D030801:Animals, Genetically Modified; D019393:Arrestin / Q000378:metabolism; D002118:Calcium / Q000378:metabolism*; D002147:Calmodulin / Q000378:metabolism*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster; D005136:Eye Proteins / Q000378:metabolism; D005786:Gene Expression Regulation / Q000235:genetics; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D009154:Mutation / Q000502:physiology; D018995:Myosin Heavy Chains / Q000378:metabolism; D018408:Patch-Clamp Techniques; D010775:Photic Stimulation / Q000379:methods; D017956:Photoreceptor Cells, Invertebrate / Q000187:drug effects / Q000502:physiology; D012243:Rhodopsin / Q000378:metabolism*; D014785:Vision, Ocular / Q000187:drug effects / Q000502:physiology*
D019393:Arrestin; D002147:Calmodulin; D029721:Drosophila Proteins; D005136:Eye Proteins; C013110:metarhodopsins; D012243:Rhodopsin; C072308:ninaC protein, Drosophila; D018995:Myosin Heavy Chains; D002118:Calcium
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