Skip to main content Accessibility help
×
Home

Central regulation of photosensitive membrane turnover in the lateral eye of Limulus. II. Octopamine acts via adenylate cyclase/cAMP-dependent protein kinase to prime the retina for transient rhabdom shedding

  • SCOTT L. RUNYON (a1), KEVIN J. WASHICOSKY (a1), RANDALL J. BRENNEMAN* (a1), JEREMY R. KELLY (a1), RASHMI V. KHADILKAR (a1), KEVIN F. HEACOCK (a1), SHAELAN M. MCCORMICK (a1), KELLY E. WILLIAMS (a1) and ROBERT N. JINKS (a1)...

Abstract

Why photoreceptors turn over a portion of their photoreceptive membrane daily is not clear; however, failure to do so properly leads to retinal degeneration in vertebrates and invertebrates. Little is known about the molecular mechanisms that regulate shedding and renewal of photoreceptive membrane. Photoreceptor cells in the lateral eye of the horseshoe crab Limulus turn over their photoreceptive membrane (rhabdom) in a brief, synchronous burst in response to dawn each morning. Transient rhabdom shedding (TRS), the first phase of rhabdom turnover in Limulus, is triggered by dawn, but requires a minimum of 3–5 h of overnight priming from the central circadian clock (Chamberlain & Barlow, 1984). We determined previously that the clock primes the lateral eye for TRS using the neurotransmitter octopamine (OA) (Khadilkar et al., 2002), and report here that OA primes the eye for TRS through a Gs-coupled, adenylate cyclase (AC)/cyclic adenosine 3′,5′-monophosphate (cAMP)/cAMP-dependent protein kinase (PKA) signaling cascade. Long-term intraretinal injections (6–7 h @ 1.4 μl/min) of the AC activator forskolin, or the cAMP analogs Sp-cAMP[S] and 8-Br-cAMP primed the retina for TRS in eyes disconnected from the circadian clock, and/or in intact eyes during the day when the clock is quiescent. This suggests that OA primes the eye for TRS by stimulating an AC-mediated rise in intracellular cAMP concentration ([cAMP]i). Co-injection of SQ 22,536, an AC inhibitor, or the PKA inhibitors H-89 and PKI (14-22) with OA effectively antagonized octopaminergic priming by reducing the number of photoreceptors primed for TRS and the amount of rhabdom shed by those photoreceptors compared with eyes treated with OA alone. Our data suggest that OA primes the lateral eye for TRS in part through long-term phosphorylation of a PKA substrate.

Copyright

Corresponding author

Address correspondence and reprint requests to: Robert N. Jinks, Department of Biology, Franklin & Marshall College, P.O. Box 3003, Lancaster, PA 17604-3003, USA. E-mail: rjinks@fandm.edu

References

Hide All

REFERENCES

Abel, T. & Kandel, E. (1998). Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Research. Brain Research Reviews 26, 360378.
Aréchiga, H. & Rodríguez-Sosa, L. (1998). Circadian clock function in isolated eyestalk tissue of crayfish. Proceedings of the Royal Society B. (London) 265, 18191823.
Barlow, Jr., R.B. (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856870.
Barlow, R. (2001). Circadian and efferent modulation of visual sensitivity. Progress in Brain Research 131, 487503.
Basinger, S., Hoffman, R., & Matthes, M. (1976). Photoreceptor shedding is initiated by light in the frog retina. Science 194, 10741076.
Battelle, B.-A. (2002). Circadian efferent input to Limulus eyes: Anatomy, circuitry, and impact. Microscopy Research and Technique 58, 345355.
Battelle, B.-A. & Wishart, A.C. (1990). Cyclic AMP-linked octopamine receptors in Limulus eyes: Pharmacological characteristics. Investigative Ophthalmology and Visual Science (Suppl.) 31, 331.
Battelle, B.-A., Andrews, A.W., Calman, B.G., Sellers, J.R., Greenberg, R.M., & Smith, W.C. (1998). A myosin III from Limulus eyes is a clock-regulated phosphoprotein. Journal of Neuroscience 18, 45484559.
Battelle, B.-A., Williams, C.D., Schremser-Berlin, J.-L., & Cacciatore, C. (2000). Regulation of arrestin mRNA levels in Limulus lateral eye: Separate and combined influences of circadian efferent input and light. Visual Neuroscience 17, 217227.
Battelle, B.-A., Dabdoub, A., Malone, M.A., Andrews, A.W., Cacciatore, C., Calman, B.G., Smith, W.C., & Payne, R. (2001). Immunocytochemical localization of opsin, visual arrestin, myosin III, and calmodulin in Limulus lateral eye retinular cells and ventral photoreceptors. Journal of Comparative Neurology 435, 211225.
Besharse, J.C., Iuvone, P.M., & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. In Progress in Retinal Research, Vol. 7, ed. Osborne, N.N. & Chader, G.J., pp. 2161. Oxford: Pergamon.
Birch, D.G., Berson, E.L., & Sandberg, M.A. (1984). Diurnal rhythm in the human rod ERG. Investigative Ophthalmology and Visual Science 25, 236238.
Birch, D.G., Sandberg, M.A., & Berson, E.L. (1986). Diurnal rhythm in the human rod ERG: Relationship to cyclic lighting. Investigative Ophthalmology and Visual Science 27, 268270.
Blest, A.D. (1988). The turnover of phototransductive membrane in compound eyes and ocelli. Advances in Insect Physiology 20, 153.
Cahill, G.M. & Hasegawa, M. (1997). Circadian oscillators in vertebrate retinal photoreceptor cells. Biological Signals 6, 191200.
Chamberlain, S.C. & Barlow, Jr., R.B. (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361363.
Chamberlain, S.C. & Barlow, Jr., R.B. (1984). Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. Journal of Neuroscience 4, 27922810.
Chyb, S., Hevers, W., Forte, M., Wolfgang, W.J., Selinger, Z., & Hardie, R.C. (1999). Modulation of the light response by cAMP in Drosophila photoreceptors. Journal of Neuroscience 19, 87998807.
Dabdoub, A., Payne, R., & Jinks, R.N. (2002). Protein kinase C-induced disorganization and endocytosis of photosensitive membrane in Limulus photoreceptors. Journal of Comparative Neurology 442, 217225.
Delmas, P., Wanaverbecq, N., Abogadie, F.C., Mistry, M., & Brown, D.A. (2002). Signaling microdomains define the specificity of receptor-mediated InsP3 pathways in neurons. Neuron 14, 209220.
Dolph, P.J., Ranganathan, R., Colley, N.J., Hardy, R.W., Socolich, M., & Zuker, C.S. (1993). Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 260, 19101916.
Edwards, S.C. & Battelle, B.-A. (1987). Octopamine- and cyclic AMP-stimulated phosphorylation of protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 28112820.
Fahrenbach, W.H. (1975). The visual system of the horseshoe crab Limulus polyphemus. International Review of Cytology 41, 285349.
Fahrenbach, W.H. (1981). The morphology of the horseshoe crab (Limulus polyphemus) visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216, 655659.
Glass, D.B., Cheng, H.-C., Mende-Mueller, L., Reed, J., & Walsh, D.A. (1989). Primary structural determinants essential for potent inhibition of cAMP-dependent protein kinase by inhibitory peptides corresponding to the active portion of the heat-stable inhibitor protein. Journal of Biological Chemistry 264, 88028810.
Goldsmith, B.A. & Abrams, T.W. (1991). Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase. Proceedings of the National Academy of Sciences of the U.S.A. 88, 90219025.
Grace, M.S., Chiba, A., & Menaker, M. (1999). Circadian control of photoreceptor outer segment membrane turnover in mice genetically incapable of melatonin synthesis. Visual Neuroscience 16, 909918.
Greengard, P., Jen, J., Nairn, A.C., & Stevens, C.F. (1991). Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253, 11351138.
Herberg, F.W., Taylor, S.S., & Dostmann, W.R.G. (1996). Active site mutations define the pathway for the cooperative activation of cAMP-dependent protein kinase. Biochemistry 35, 29342942.
Hünenberger, P.H., Helms, V., Narayana, N., Taylor, S.S., & McCammon, J.A. (1999). Determinants of ligand binding to cAMP-dependent protein kinase. Biochemistry 38, 23582366.
Jinks, R.N., Asrican, B.W., & Khadilkar, R.V. (1999). Does octopamine, via a protein phosphatase inhibitor, mediate circadian efferent regulation of photosensitive membrane shedding in the lateral eye of the horseshoe crab Limulus? Investigative Ophthalmology and Visual Science 40, s612.
Jinks, R.N., White, R.H., & Chamberlain, S.C. (1996). Dawn, diacylglycerol, calcium, and protein kinase C—the retinal wrecking crew. A signal transduction cascade for rhabdom shedding in the Limulus eye. Journal of Photochemistry and Photobiology B: Biology 34, 4552.
Johnson, D.A., Akamine, P., Radzio-Andzelm, E., Madhusudan, & Taylor, S.S. (2001). Dynamics of cAMP-dependent protein kinase. Chemical Reviews 101, 22432270.
Kass, L. & Barlow, Jr., R.B. (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. I. Octopamine-induced increases in retinal sensitivity. Journal of Neuroscience 4, 908.
Kass, L. & Zhang, H.-J. (1992). Clock controls gain in Limulus photoreceptors by changing voltage-dependent conductances. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1327.
Kass, L., Pelletier, J.L., Renninger, G.H., & Barlow, Jr., R.B. (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. II. Intracellular recordings in vitro. Journal of Comparative Physiology A 164, 95105.
Kaupp, U.B. & Seifert, R. (2002). Cyclic nucleotide-gated ion channels. Physiological Reviews 82, 769824.
Khadilkar, R.V., Mytinger, J.R., Thomason, L.E., Runyon, S.L., Washicosky, K.J., & Jinks, R.N. (2002). Central regulation of photosensitive membrane turnover in the lateral eye of Limulus. I. Octopamine primes the retina for daily transient rhabdom shedding. Visual Neuroscience 19, 283297.
LaVail, M.M. (1976). Rod outer segment disc shedding in rat retina: Relationship to cyclic lighting. Science 194, 10711074.
Lonze, B.E. & Ginty, D.D. (2002). Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605623.
Mahoney, D.F., Sacunas, R.B., & Chamberlain, S.C. (2001). Rhabdom shedding in the Limulus lateral eye: Seasons and weather. Society for Neuroscience Abstracts 27, 1903.
Meyer, Jr., R.B. & Miller, J.P. (1974). Analogs of cyclic AMP and cyclic GMP: General methods of synthesis and the relationship of structure to enzymatic activity. Life Sciences 14, 10191040.
Montell, C. (1999). Visual transduction in Drosophila. Annual Review of Cell and Developmental Biology 15, 231268.
Nguyen-Legros, J. & Hicks, D. (2000). Renewal of photoreceptor outer segments and their phagocytosis by the retinal pigment epithelium. International Review of Cytology 196, 245313.
Pieprzyk, A.R., Weiner, W.W., & Chamberlain, S.C. (2003). Mechanisms controlling the sensitivity of the Limulus lateral eye in natural lighting. Journal of Comparative Physiology A 189, 643653.
Roeder, T. (1999). Octopamine in invertebrates. Progress in Neurobiology 59, 533561.
Rothermel, J.D. & Parker Botelho, L.H. (1988). A mechanistic and kinetic analysis of the interactions of the diastereoisomers of adenosine 3′,5′-(cyclic)phosphorothioate with purified cyclic AMP-dependent protein kinase. Biochemical Journal 251, 757762.
Rufiange, M., Dumont, M., & Lachapelle, P. (2002). Correlating retinal function with melatonin secretion in subjects with an early or late circadian phase. Investigative Ophthalmology and Visual Science 43, 24912499.
Runyon, S.L., Kelly, J.R., & Jinks, R.N. (2002). Cyclic adenosine 3′,5′-monophosphate (cAMP) analogs mimic circadian efferent priming of the Limulus lateral eye for transient rhabdom shedding. Society for Neuroscience Abstracts 28, 843.2.
Russ, J.C. (1986). Practical Stereology. pp. 3553. New York: Plenum Press.
Sacunas, R.B., Papuga, M.O., Malone, M.A., Pearson, Jr., A.C., Marjanovic, M., Stroope, D.G., Weiner, W.W., Chamberlain, S.C., & Battelle, B.-A. (2002). Multiple mechanisms of rhabdom shedding in the lateral eye of Limulus polyphemus. Journal of Comparative Neurology 449, 2642.
Scholubbers, H.G., van Knippenberg, P.H., Baraniak, J., Stec, W.J., Morr, M., & Jastorff, B. (1984). Investigations on stimulation of lac transcription in vivo in Escherichia coli by cAMP analogues. Biological activities and structure–activity correlations. European Journal of Biochemistry 138, 101109.
Seamon, K.B., Padgett, W., & Daly, J.W. (1981). Forskolin: Unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proceedings of the National Academy of Sciences of the U.S.A. 78, 33633367.
Shabb, J.B. (2001). Physiological substrates of cAMP-dependent protein kinase. Chemical Reviews 101, 23812411.
Silva, A.J., Kogan, J.H., Frankland, P.W., & Kida, S. (1998). CREB and Memory. Annual Review of Neuroscience 21, 127148.
Smith, W.C., Greenberg, R.M., Calman, B.G., Hendrix, M.M., Hutchinson, L., Donoso, L.A., & Battelle, B.-A. (1995). Isolation and expression of an arrestin cDNA from the horseshoe crab lateral eye. Journal of Neurochemistry 64, 113.
Tsunoda, S., Sierralta, J., Sun, Y., Bodner, R., Suzuki, E., Becker, A., Socolich, M., & Zuker, C.S. (1997). A multivalent PDZ-domain protein assembles signaling complexes in a G-protein-coupled cascade. Nature 388, 243249.
Wang, L.-Y., Salter, M.W., & MacDonald, J.F. (1991). Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253, 11321135.
White, M.P. & Hock, P.A. (1992). Effects of continuous darkness on ERG correlates of disc shedding in rabbit retina. Experimental Eye Research 54, 173180.
Wiebe, E.M., Wishart, A.C., Edwards, S.C., & Battelle, B.-A. (1989). Calcium/ calmodulin-stimulated phosphorylation of photoreceptor proteins in Limulus. Visual Neuroscience 3, 107118.
Wilden, U., Hall, S.W., & Kühn, H. (1986). Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 83, 11741178.
Young, R.W. (1976). Visual cells and the concept of renewal. Investigative Ophthalmology and Visual Science 15, 700725.
Yusta, B., Ortiz-Caro, J., Pascaul, A., & Aranda, A. (1988). Comparison of the effects of forskolin and dibutyryl cyclic AMP in neuroblastoma cells: Evidence that some of the actions of dibutyryl cyclic AMP are mediated by butyrate. Journal of Neurochemistry 51, 18081818.
Zhang, H.-J., Jinks, R.N., Wishart, A.C., Battelle, B.-A., Chamberlain, S.C., Fahrenbach, W.H., & Kass, L. (1994). An enzymatically enhanced recording technique for Limulus ventral photoreceptors: Physiology, biochemistry, and morphology. Visual Neuroscience 11, 4152.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed