CAFFEINE-SENSITIVE AND RYANODINE-SENSITIVE CA2-INDUCED CA2+ RELEASE FROM THE ENDOPLASMIC-RETICULUM IN HONEYBEE PHOTORECEPTORS()

Light stimulation of invertebrate microvillar photoreceptors causes a large rapid elevation in Ca-i, shown previously to modulate the adapta tional state of the cells. Ca-i rises, at least in part, as a result o f Ins(1,4,5)P-3-induced Ca2+ release from the submicrovillar endoplasm ic reticulum (ER). Here, we provide evidence for Ca2+-induced Ca2+ rel ease (CICR) in an insect photoreceptor. In situ microphotometric measu rements of Ca2+ fluxes across the ER membrane in permeabilized slices of drone bee retina show that (a) caffeine induces Ca2+ release from t he ER; (b) caffeine and Ins(1,4,5)P-3 open distinct Ca2+ release pathw ays because only caffeine-induced Ca2+ release is ryanodine sensitive and heparin insensitive, and because caffeine and Ins(1,4,5)P-3 have a dditive effects on the rate of Ca2+ release; (c) Ca2+ itself stimulate s release of Ca2+ via a ryanodine-sensitive pathway; and (d) cADPR is ineffective in releasing Ca2+. Microfluorometric intracellular Ca2+ me asurements with fluo-3 indicate that caffeine induces a persistent ele vation in Ca-i. Electrophysiological recordings demonstrate that caffe ine mimics all aspects of Ca2+-mediated facilitation and adaptation in drone photoreceptors. We conclude that the ER in drone photoreceptors contains, in addition to the Ins(1,4,5)P-3-sensitive release pathway, a CICR path way that meets key pharmacological criteria for a ryanodi ne receptor. Coexpression of both release mechanisms could be required for the production of rapid light-induced Ca2+ elevations, because Ca 2+ amplifies its own release through both pathways by a positive feedb ack. CICR may also mediate the spatial spread of Ca2+ release from the submicrovillar ER toward more remote ER subregions, thereby activatin g Ca2+-sensitive cell processes that are not directly involved in phot otransduction.