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Two components of the receptor current are developed from distinct elementary signals in Limulus ventral nerve photoreceptor

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Abstract

Transient elementary currents, bumps, stimulated by short dim light flashes were measured in ventral nerve photoreceptors of Limulus. It is demonstrated that light activates two types of bumps, which form two distinct components of the receptor current at higher light intensities. The two bump types, which are both assumed to be activated by single absorbed photons, differ in current amplitude and kinetic parameters. The current amplitude of one bump type is smaller than 0.3 nA and that of the other type is in the usual current range of up to several nanoamperes. The average latency of small bumps measured from the short stimulus flash is shorter than that of the large bumps. The small bumps have slower activation kinetics than the large bumps. It is demonstrated that with increasing flash intensity the small bumps overlap first and form a macroscopic current, on top of which the large bumps are superimposed. Results indicate that a single absorbed photon selectively activates only one kind of the enzyme cascades evoking one bump type. We conclude that the active meta conformation of a rhodopsin molecule selectively binds a specific type of G-protein, which is involved in the stimulation of one of the transduction cascades. The two bump types, which are the elements of two macroscopic current components support the previous assumption that light activates different transduction mechanisms in Limulus photoreceptors.

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References

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

    Google Scholar 

  • Borsellino A, Fuortes MGF (1968) Responses to single photons in visual cells of Limulus. J Physiol (London) 196:507–539

    Google Scholar 

  • Calman BG, Chamberlain SC (1982) Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol 80:839–862

    Google Scholar 

  • Contzen K, Nagy K, Stieve H (1992) Quantum bumps that form two components of the light-activated current in Limulus photoreceptors. In: Elsner N, Richter DW (eds) Rhythmogenesis in neurons and networks. Georg Thieme Verlag, Stuttgart, New York, p 289

    Google Scholar 

  • Deckert A, Nagy K, Helrich CS, Stieve H (1992) Three components in the light-induced current of the Limulus ventral photoreceptor. J Physiol (London) 453:69–96

    Google Scholar 

  • Dodge FA, Knight BW, Toyoda J (1968) Voltage noise in Limulus visual cells. Science 160:88–90

    Google Scholar 

  • Faddis MN, Brown JE (1993) Intracellular injection of heparin and polyamines. Effects on phototransduction in Limulus ventral photoreceptors. J Gen Physiol 101:909–931

    Google Scholar 

  • Fein A, Payne R (1989) Phototransduction in Limulus photoreceptors: Roles of calcium and inositol trisphosphate. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 173–185

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Frank TM, Fein A (1991) The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. J Gen Physiol 97:697–723

    Google Scholar 

  • Hamdorf K, Razmjoo S (1979) Photoconvertible pigment states and excitation in Calliphora; the induction and properties of the prolonged depolarising afterpotential. Biophys Struct Mechanism 5:137–161

    Google Scholar 

  • Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8: 643–651

    Google Scholar 

  • Keiper W, Schnakenberg J, Stieve H (1984) Statistical analysis of quantum bump parameters in Limulus ventral photoreceptors. Z Naturforsch 39c:781–790

    Google Scholar 

  • Kirkwood A, Weiner D, Lisman JE (1989)An estimate of the number of G regulatory proteins activated per excited rhodopsin in living Limulus ventral photoreceptors. Proc Natl Acad Sci, USA 86:3872–3876

    Google Scholar 

  • Levine E, Crain E, Robinson P, Lisman J (1987) Nontransducing rhodopsin. J Gen Physiol 90:575–586

    Google Scholar 

  • Lisman J (1985) The role of metarhodopsin in the generation of spontaneous quantum bumps in ultraviolet receptors of Limulus median eye. Evidence for reverse reactions into an active state. J Gen Physiol 85:171–187

    Google Scholar 

  • Lisman JE, Brown JE (1971) Two light-induced processes in the photoreceptor cells of Limulus ventral eye. J Gen Physiol 58:544–561

    Google Scholar 

  • Maaz G, Nagy K, Stieve H, Klomfaß J (1981) The electrical light response of the Limulus ventral nerve photoreceptor, a superposition of distinct components — observable by variation of the state of light adaptation. J Comp Physiol 141:303–310

    Google Scholar 

  • Nagy K (1990) Kinetic properties of single ion channels activated by light in Limulus ventral nerve photoreceptors. Eur Biophys J 19:47–54

    Google Scholar 

  • Nagy K (1991) Biophysical processes in invertebrate photoreceptors: recent progress and a critical overview based on Limulus photoreceptors. Q Rev Biophys 24:165–226

    Google Scholar 

  • Nagy K (1992) Non-independent quantum bumps in Limulus ventral nerve photoreceptors — a new insight in the light transduction mechanism. Neurosci Lett 144:99–102

    Google Scholar 

  • Nagy K (1993) Cyclic nucleotides and inositol trisphosphate activate distinct components of the receptor current in Limulus ventral nerve photoreceptors. Neurosci Lett 152:1–4

    Google Scholar 

  • Nagy K, Stieve H (1990) Light-activated single channel currents in Limulus ventral photoreceptors. Eur Biophys J 18:221–224

    Google Scholar 

  • Nagy K, Contzen K, Stieve H (1992) Different sorts of quantum bumps form two components of the receptor current in Limulus photoreceptors. Proceedings of The sensory systems and communications in arthropods. Hamburg (in press)

  • Nasi E (1991) Two light-dependent conductances in Lima rhabdomeric photoreceptors. J Gen Physiol 97:55–72

    Google Scholar 

  • Nasi E, Gomes MP (1992) Light-activated ion channels in solitary photoreceptors of the scallop Pecten irradians. J Gen Physiol 99: 747–769

    Google Scholar 

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

    Google Scholar 

  • Payne R, Walz B, Levy S, Fein A (1988) The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Philos Trans R Soc Lond Ser B 320:359–379

    Google Scholar 

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

    Google Scholar 

  • Reuß H (1991) Bumps, die elementaren Reizantworten der Photorezeptorzelle des Limulus polyphemus. Dissertation, RWTH Aachen

    Google Scholar 

  • Reuß H, Stieve H (1992) Two different bump types of the ventral nerve photoreceptor of Limulus. Z Naturforsch 48c:92–95

    Google Scholar 

  • Robinson PR, Wood SF, Szuts EZ, Fein A, Hamm HE, Lisman JE (1990) Light-dependent GTP-binding proteins in squid photoreceptors. Biochem J 272:79–85

    Google Scholar 

  • Srebo R, Behbehani M (1972) Light adaptation of discrete waves in the Limulus photoreceptors. J Gen Physiol 60:86–101

    Google Scholar 

  • Stieve H (1986) Bumps, the elementary excitatory responses of invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konferenzen. Springer, Berlin Heidelberg New York, pp 199–230

    Google Scholar 

  • Stieve H, Benner S (1992) The light-induced rise in cytosolic calcium starts later that the receptor current of Limulus ventral photoreceptor. Vision Res. 32:403–416

    Google Scholar 

  • Stieve H, Bruns M (1980) Dependence of bump rate and bump size in Limulus ventral nerve photoreceptors on light adaptation and calcium concentration. Biophys Struct Mechanism 6:271–285

    Google Scholar 

  • Stieve H, Bruns M (1983) Bump latency distribution and bump adaptation of Limulus ventral nerve photoreceptor in varied extracellular calcium concentration. Biophys Struct Mechanism 9:323–339

    Google Scholar 

  • Stieve H, Schlösser B (1989) The light energy dependence of the Limulus photoreceptor current in two defined states of adaptation. Z Naturforsch 44c:999–1014

    Google Scholar 

  • Stieve H, Schnakenberg J, Kuhn A, Reuss H (1986) An automatic gain control in the Limulus photoreceptor. In: Lüttgau HC (ed) Progress in Zoology, Vol 33. Membrane control of cellular activity. Gustav Fischer Verlag, Stuttgart, pp 367–376

    Google Scholar 

  • Stieve H, Reuß H, Hennig HT, Klomfaß J (1991) Single photon evoked events of the ventral nerve photoreceptor cell of Limulus. Facilitation, adaptation and dependence on lowered external calcium. Z Naturforsch 46c:461–486

    Google Scholar 

  • Stieve H, Niemeyer B, Aktories K, Hamm HE (1992) Disturbing GTP-binding protein function through microinjection into the visual cell of Limulus. Z Naturforsch 47c:915–921

    Google Scholar 

  • Tsuda M (1987) Photoreception and phototransduction in invertebrate photoreceptors. Photochem Photobiol 45:915–931

    Google Scholar 

  • Tsuda M, Tsuda T (1990) Two distinct light regulated G-proteins in octopus photoreceptors. Biochim Biophys Acta 1052:204–210

    Google Scholar 

  • Yeandle S (1958) Evidence of quantized slow potentials in the eye of Limulus. Am J Ophtalmol 46:82–87

    Google Scholar 

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

    Google Scholar 

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Nagy, K., Contzen, K. & Stieve, H. Two components of the receptor current are developed from distinct elementary signals in Limulus ventral nerve photoreceptor. Eur Biophys J 22, 341–350 (1993). https://doi.org/10.1007/BF00213557

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  • DOI: https://doi.org/10.1007/BF00213557

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