Skip to main content
SpringerLink
Log in

The latency of the response of Limulus photoreceptors to inositol trisphosphate lacks the calcium-sensitivity of that to light

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

The latent period before depolarization of Limulus ventral photoreceptors by light flashes was compared with that following brief, intracellular, pressure-injection of d-myo-inositol 1,4,5 trisphosphate. At temperatures between 18 °C and 22 °C and with an extracellular calcium concentration of 10 mM, the responses of 4 cells to light and to injections of 100 μM inositol trisphosphate displayed average latencies of 71 and 56 ms, respectively. The latencies of responses to InsP3 included an estimated 20 ms dead-time inherent in the injection method. Reducing the temperature lengthened the latency of the response to light (Q10 approximately 3.2 between 7 and 22 °C) more than that to inositol trisphosphate (Q10 approximately 2.3). Bathing the photoreceptors in seawater containing no added calcium and 1 mM of the calcium chelator EGTA greatly increased the latency of the light response at all temperatures, but did not increase the latency of the response to inositol trisphosphate. We conclude that the response to inositol trisphosphate lacks the calcium- and temperature-sensitive latent period which characterizes the response to light. If inositol trisphosphate acts, via the release of stored calcium, to stimulate an intermediate in the visual cascade, then that intermediate would appear to be downstream from the latency-generating mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

InsP 3 :

D-myo-inositol 1,4,5 trisphosphate

ASW :

Artificial seawater

Ca i :

Cytosolic free calcium ion concentration

Ca 0 :

Extracellular calcium ion concentration

References

  • Ammann D, Buehrer T, Schefer U, Mueller M, Simon W (1987) Intracellular neutral carrier-based Ca2+ microelectrode with subnanomolar detection limit. Pflügers Arch 409:223–228

    Google Scholar 

  • Bacigalupo J, Johnson EC, Vergara C, Lisman JE (1991) Light-dependent channels in excised patches of Limulus ventral photoreceptors are opened by cyclic GMP. Proc Natl Acad Sci USA 88:7938–7942

    Google Scholar 

  • Baumann O, Walz B (1989) Calcium and inositol polyphosphate-sensitivity of the calcium-sequestering endoplasmic reticulum in the photoreceptor cells of the honey bee drone. J Comp Physiol A 165:627–636

    Google Scholar 

  • Bolsover SR, Brown JE (1985) Calcium ion, an intracellular messenger of light adaptation, also participates in excitation of Limulus photoreceptors. J Physiol (Lond) 364:381–393

    Google Scholar 

  • Brown JE, Blinks JR (1974) Changes in intracellular free calcium during illumination of invertebrate photoreceptors. Detected with aequorin. J Gen Physiol 64:643–665

    Google Scholar 

  • Brown JE, Rubin LJ (1984) A direct demonstration that inositol trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochem Biophys Res Comm 125:1137–1142

    Google Scholar 

  • Brown JE, Rubin LJ, Ghalayini AJ, Tarver AL, Irvine RF, Berridge MJ, Anderson RE (1984) Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311:160–162

    Google Scholar 

  • Brown JE, Watkins DC, Malbon CC (1987) Light-induced changes in the content of inositol phosphates in squid (Loligo pealei) retina. Biochem J 247:293–297

    Google Scholar 

  • Corson DW, Fein A (1983) Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys J 44:299–304

    Google Scholar 

  • Devary O, Heichal O, Blumenfeld A, Cassel A, Suss A, Barash A, Rubinstein T, Minke B, Selinger Z (1987) Coupling of photoexcited rhodopsin to phospholipid hydrolysis in fly photoreceptors. Proc Natl Acad Sci USA 84:6939–6943

    Google Scholar 

  • Fein A, Charlton JS (1977) Enhancement and phototransduction in the ventral eye of Limulus. J Gen Physiol 69:553–569

    Google Scholar 

  • Fein A, Payne R, Corson DW, Berridge MJ, Irvine RF (1984) Photoreceptor excitation and adaptation by inositol 1,4,5 trisphosphate. Nature 311:157–160

    Google Scholar 

  • Fuortes MGF, Yeandle S (1964) Probability of occurrences of discrete potential waves in the eye of Limulus. J Gen Physiol 47:443–463

    Google Scholar 

  • Hastings JW, Mitchell G, Mattingly PH, Blinks JR, Van Leeuwen M (1969) Response of aequorin bioluminescence to rapid changes in calcium concentration. Nature 222:1047–1050

    Google Scholar 

  • Inouye S, Noguchi M, Sakaki Y, Takagi Y, Miyata T, Iwagana S, Miyata T, Tsuji FI (1985) Cloning and sequence analysis of cDNA for the luminescent protein aequorin. Proc Natl Acad Sci USA 82:3154–3158

    Google Scholar 

  • Inouye S, Aoyama S, Miyata T, Tsuji FI, Sakaki Y (1989) Overex-pression and purification of the recombinant calcium-binding protein apoaequorin. J Biochem 105:473–477

    Google Scholar 

  • Johnson EC, Robinson PR, Lisman JE (1986) cGMP is involved in the excitation of invertebrate photoreceptors. Nature 324:468–470

    Google Scholar 

  • Kishi Y, Tanino H, Goto T (1972) The structure confirmation of the light-emitting moiety of bioluminescent jellyfish Aequorea. Tetrahed Lett 1972:2747–2748

    Google Scholar 

  • Levy S, Fein A (1985) Relationship between light-sensitivity and intracellular free calcium in Limulus ventral photoreceptors. J Gen Physiol 85:805–841

    Google Scholar 

  • Lisman JE (1976) Effects of removing extracellular Ca2+ on excitation and adaptation in Limulus ventral photoreceptors. Biophys J 16:1331–1335

    Google Scholar 

  • Martinez II JM, Srebro R (1976) Calcium and the control of discrete wave latency in the ventral photoreceptor of Limulus. J Physiol (Lond) 261:535–562

    Google Scholar 

  • Miledi R, Parker I (1989) Latencies of membrane currents evoked by Xenopus oocytes by receptor activation, inositol trisphosphate and calcium. J Physiol (Lond) 415:189–210

    Google Scholar 

  • Musicki B, Kishi Y, Shimomura O (1986) Structure of the functional part of the photoprotein aequorin. J Chem Soc Chem Comm 1986:1566–1568

    Google Scholar 

  • O'Day PM, Gray-Keller MP (1989) Evidence for electrogenic Na+/ Ca exchange in Limulus ventral photoreceptors. J Gen Physiol 93:473–492

    Google Scholar 

  • O'Day PM, Johnson EC, Baumgard M (1991) Effects of Li+, Ca2+ and PDE inhibitors on excitation of Limulus photoreceptors. Biophys J 59:540a

    Google Scholar 

  • Payne R, Fein A (1987) Inositol 1,4,5 trisphosphate releases calcium from specialized sites within Limulus photoreceptors. J Cell Biol 104:933–937

    Google Scholar 

  • Payne R, Corson DW, Fein A (1986a) Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. J Gen Physiol 88:107–126

    Google Scholar 

  • Payne R, Corson DW, Fein A, Berridge MJ (1986b) Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 trisphosphate result from a rise in intracellular calcium. J Gen Physiol 88:127–142

    Google Scholar 

  • Payne R, Flores TM, Fein A (1990) Feedback inhibition by calcium limits the release of calcium by inositol trisphosphate in Limulus ventral photoreceptors. Neuron 4:547–555

    Google Scholar 

  • Rubin LJ, Brown JE (1985) Intracellular injection of calcium buffers blocks IP3-induced but not light-induced electrical responses of Limulus ventral photoreceptors. Biophys J 47:38a

    Google Scholar 

  • Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan Aequorea. J Cell Comp Physiol 59:223–240

    CAS  PubMed  Google Scholar 

  • Stieve H, Bruns M (1983) Bump latency distribution and bump adaptation of Limulus ventral nerve photoreceptor in varied extracellular calcium concentrations. Biophys Struct Mech 9:329–339

    Google Scholar 

  • Stieve H, Gaube H, Klomfass J (1986) Effect of external calcium concentration on the intensity dependence of light-induced membrane current and voltage signals in two defined states of adaptation in the photo-receptor of Limulus. Z Naturforsch 41c:1092–1110

    Google Scholar 

  • Szuts EZ, Wood SF, Reid MA, Fein A (1986) Light stimulates the rapid formation of inositol trisphosphate in squid retinae. Biochem J 240:929–932

    Google Scholar 

  • Wong F, Knight BW, Dodge FA (1980) Dispersion of latencies on photoreceptors of Limulus and the adapting-bump model. J Gen Physiol 76:517–537

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Maryland, 20742, College Park, MD, USA

    Richard Payne

  2. Department of Biochemistry, University of Maryland, 20742, College Park, MD, USA

    Thomas M. Flores

Authors
  1. Richard Payne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas M. Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Payne, R., Flores, T.M. The latency of the response of Limulus photoreceptors to inositol trisphosphate lacks the calcium-sensitivity of that to light. J Comp Physiol A 170, 311–316 (1992). https://doi.org/10.1007/BF00191419

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00191419

Key words

Search

Navigation