Changes in Intracellular Free Calcium Concentration during Illumination of Invertebrate Photoreceptors

Abstract

Aequorin, which luminesces in the presence of calcium, was injected into photoreceptor cells of Limulus ventral eye. A bright light stimulus elicited a large increase in aequorin luminescence, the aequorin response, indicating a rise of intracellular calcium ion concentration, Ca/. The aequorin response reached a maximum after the peak of the electrical response of the photoreceptor, decayed during a prolonged stimulus, and returned to an undetectable level in the dark. Reduction of Ca, reduced the amplitude of the aequorin response by a factor no greater than 3. Raising Cao increased the amplitude of the aequorin response. The aequorin response became smaller when membrane voltage was clamped to successively more positive values. These results indicate that the stimulus-induced rise of Cai may be due in part to a light-induced influx of Ca and in part to release of Ca from an intracellular store. Our findings are consistent with the hypothesis that a rise in Cai is a step in the sequence of events underlying light-adaptation in Limulus ventral photoreceptors. Aequorin was also injected into photoreceptors of Balanus. The aequorin responses were similar to those recorded from Limulus cells in all but two ways: (a) A large sustained aequorin luminescence was measured during a prolonged stimulus, and (b) removal of extracellular calcium reduced the aequorin response to an undetectable level.

Ion permeation through light-activated channels in rhabdomeric photoreceptors. Role of divalent cations.

“…The quantitatively disparate contribution of Ca influx to the photocurrent and its variable role as a modulatory factor may be related to the different mechanisms underlying the increase in cytosolic Ca that accompanies the photoresponse. In Limulus, the light-induced Ca transient survives superfusion with 0-Ca, implying that it is mostly due to internal release (Brown and Blinks, 1974). Because the peak concentration in the rhabdomeric lobe can reach tens of micromolar (Brown et al, 1977;Levy and Fein, 1985;Ukhanov et al, 1995), any additional Ca permeating through light-activated channels would not be expected to exert a major influence.…”

“…(Millecchia and Mauro, 1969;Brown and Mote, 1974); by contrast, a significant shift was reported in Balanus photoreceptors (Brown et al, 1971). A complementary observation in these two species is that the intracellular rise in Ca that accompanies the light response was drastically reduced in low-Ca external solution in Balanus but was only attenuated in Limulus (Brown and Blinks, 1974), suggestive of differences in the extent to which Ca influx may occur during the photoresponse.…”

Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements.

“…Less elaborate, but also well developed, are Ca2+-sequestering sub-surface cisternae associated with the nonreceptive plasma membrane areas of the cell (43) . These two prominent high-affinity Ca"-buffering SER elements thus possess a strategic position relative to the cell periphery where stimulus-induced changes of Cai+ (6,8,9,26) most probably take place.…”

“…The Ca pump has a high affinity for Ca 2+ ions : the threshold for activation of the pump is -5 X 10 -8 M, the apparent KM,c,, is -4 X 10 -7 M . When Na' or Li + is substituted for K+ , Ca uptake rate is decreased by 40-50% .The results show that the Ca t+ -sequestering SER in leech photoreceptors shares some basic properties with skeletal muscle sarcoplasmic reticulum and supports the idea that certain subregions of the SER in invertebrate photoreceptors function as effective Ca 2+ sinks/buffers close to the plasmalemma.Direct evidence from measurements with Ca 2+ indicators (6,8,9,26) and Ca'-sensitive microelectrodes (6), as well as indirect evidence from electrophysiological experiments (see, for example, references 1,15,24,25,35), suggest that the free calcium concentration (Caû,+) in the cytosol of photoreceptor cells of invertebrates increases upon illumination. Several laboratories have shown that this light-induced increase of Cap' modulates the adaptational state of the cells (see reference 7 for review), a Cat+-dependent potassium conductance (see, for example, reference 17, 18, 38), and mediates the light-induced pigment granule migration in fly photoreceptors (22) .…”

“…Direct evidence from measurements with Ca 2+ indicators (6,8,9,26) and Ca'-sensitive microelectrodes (6), as well as indirect evidence from electrophysiological experiments (see, for example, references 1,15,24,25,35), suggest that the free calcium concentration (Caû,+) in the cytosol of photoreceptor cells of invertebrates increases upon illumination. Several laboratories have shown that this light-induced increase of Cap' modulates the adaptational state of the cells (see reference 7 for review), a Cat+-dependent potassium conductance (see, for example, reference 17,18,38), and mediates the light-induced pigment granule migration in fly photoreceptors (22) .…”