Light-activated Ion Channels Photoreceptors of the Scallop Pecten irradians in Solitary

I N T R O D U C T I O N It has been established that gated ion channels underlie the generat ion o f the light response in both vertebrate and invertebrate photoreceptors (Bacigalupo and Lisman, 1983; Matthews, 1987). While in amphibian rods and cones unitary currents Address reprint requests to Dr. Enrico Nasi, Department of Physiology, Boston University School of Medicine, 80 E. Concord St., Boston, MA 02118. j. GEN. PHYSIOL. © The Rockefeller University Press • 0022-1295/92/05/0747/23 $2.00 Volume 99 May 1992 747-769 747 on A uust 9, 2017 jgp.rress.org D ow nladed fom 748 T H E JOURNAL OF GENERAL PHYSIOLOGY • VOLUME 99 • 1992 can only be resolved in the absence of extracellular divalent cations (Haynes, Kay, and Yau, 1986; Zimmerman and Baylor, 1986; Matthews, 1987), the transduction channels of invertebrate visual cells can be examined under physiological conditions. However, rapid progress toward a detailed characterization of their properties has been hindered in part by the technical difficulties involved in obtaining glia-free cells suitable for patch clamp recording from the standard invertebrate eye preparations (Bacigalupo and Lisman, 1983). We have circumvented some of these problems by enzymatically isolating visual cells from the eye of the scallop. One of the remarkable features of its retina is the presence of two separate layers of photoreceptors (Dakin, 1910). The proximal layer is composed of rhabdomeric cells that depolarize in response to light (McReynolds and Gorman, 1970a), while cells in the distal retina possess modified ciliary appendages (Miller, 1958; Barber, Evans, and Land, 1967) and produce hyperpolarizing photoresponses (McReynolds and Gorman, 1970a). In b o t h cases a light-induced increase in membrane conductance has been demonstrated (McReynolds and Gorman, 1970b), but with markedly different ion selectivity (Gorman and McReynolds, 1978). The apparent lack of interneurones and synaptic interconnections (Barber et al., 1967) indicates that these responses are true receptor potentials by primary sensory cells, making this organism particularly interesting for vision research. In this report we examine light-dependent, single-channel currents recorded from cell-attached patches in isolated photoreceptors of the rhabdomeric type. The properties of these channels closely resemble those of the cell's macroscopic light response. Patch clamp measurements in hyperpolarizing ciliary cells (Gomez and Nasi, 1991) will be described in a separate article. Preliminary reports of these results have appeared previously (Nasi and Gomez,

[1]  J. Lisman,et al.  Multiple conductance states of the light-activated channel of Limulus ventral photoreceptors. Alteration of conductance state during light , 1991, The Journal of general physiology.

[2]  T. Frank,et al.  The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors , 1991, The Journal of general physiology.

[3]  F Sachs,et al.  Quantitative video microscopy of patch clamped membranes stress, strain, capacitance, and stretch channel activation. , 1991, Biophysical journal.

[4]  Kim Cooper,et al.  Low access resistance perforated patch recordings using amphotericin B , 1991, Journal of Neuroscience Methods.

[5]  F. Sachs,et al.  The ultrastructure of patch-clamped membranes: a study using high voltage electron microscopy , 1991, The Journal of cell biology.

[6]  E. Nasi,et al.  Whole-cell clamp of dissociated photoreceptors from the eye of Lima scabra , 1991, The Journal of general physiology.

[7]  E. Nasi Electrophysiological properties of isolated photoreceptors from the eye of Lima scabra , 1991, The Journal of general physiology.

[8]  K. Nagy Kinetic properties of single-ion channels activated by light in Limulus ventral nerve photoreceptors , 1990, European Biophysics Journal.

[9]  K. Nagy,et al.  Light-activated single channel currents in Limulus ventral nerve photoreceptors , 1990, European Biophysics Journal.

[10]  R. Horn,et al.  Muscarinic activation of ionic currents measured by a new whole-cell recording method , 1988, The Journal of general physiology.

[11]  K. Yau,et al.  Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane , 1986, Nature.

[12]  D. Baylor,et al.  Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores , 1986, Nature.

[13]  J. Lisman,et al.  Ion channels activated by light in Limulus ventral photoreceptors , 1986, The Journal of general physiology.

[14]  P. Detwiler,et al.  Patch‐clamp recordings of the light‐sensitive dark noise in retinal rods from the lizard and frog. , 1985, The Journal of physiology.

[15]  J. Lisman,et al.  Single-channel currents activated by light in Limulus ventral photoreceptors , 1983, Nature.

[16]  B W Knight,et al.  Adapting bump model for ventral photoreceptors of Limulus , 1982, The Journal of general physiology.

[17]  B. Sakmann,et al.  Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches , 1981, Pflügers Archiv.

[18]  A. Hawkes,et al.  On the stochastic properties of single ion channels , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  E. A. Schwartz,et al.  A voltage‐clamp study of the light response in solitary rods of the tiger salamander. , 1979, The Journal of physiology.

[20]  A. Gorman,et al.  Ionic effects on the membrane potential of hyperpolarizing photoreceptor in scallop retina , 1978, The Journal of physiology.

[21]  A. Fein,et al.  Local membrane current in Limulus photoreceptors , 1975, Nature.

[22]  A. Gorman,et al.  Membrane Conductances and Spectral Sensitivities of Pecten Photoreceptors , 1970, The Journal of general physiology.

[23]  A. Gorman,et al.  Photoreceptor Potentials of Opposite Polarity in the Eye of the Scallop, Pecten irradians , 1970, The Journal of general physiology.

[24]  A. Finkelstein,et al.  The Water and Nonelectrolyte Permeability Induced in Thin Lipid Membranes by the Polyene Antibiotics Nystatin and Amphotericin B , 1970, The Journal of general physiology.

[25]  T. Andreoli,et al.  The Interaction of Polyene Antibiotics with Thin Lipid Membranes , 1968, The Journal of general physiology.

[26]  M. Fuortes,et al.  Probability of Occurrence of Discrete Potential Waves in the Eye of Limulus , 1964, The Journal of general physiology.

[27]  W. H. Miller Derivatives of Cilia in the Distal Sense Cells of the Retina of Pecten , 1958, The Journal of biophysical and biochemical cytology.

[28]  G. Dirnberger,et al.  Comparison of time constants of single channel patches, quantum bumps, and noise analysis inLimulus ventral photoreceptors , 2005, The Journal of Membrane Biology.

[29]  V. C. Barber,et al.  The fine structure of the eye of the mollusc Pecten maximus , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[30]  G. Matthews,et al.  Single-channel recordings demonstrate that cGMP opens the light-sensitive ion channel of the rod photoreceptor. , 1987, Proceedings of the National Academy of Sciences of the United States of America.