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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

Published online by Cambridge University Press:  01 September 2004

SCOTT L. RUNYON ,
KEVIN J. WASHICOSKY ,
RANDALL J. BRENNEMAN* ,
JEREMY R. KELLY ,
RASHMI V. KHADILKAR ,
KEVIN F. HEACOCK ,
SHAELAN M. MCCORMICK ,
KELLY E. WILLIAMS  and
ROBERT N. JINKS
SCOTT L. RUNYON
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
KEVIN J. WASHICOSKY
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
RANDALL J. BRENNEMAN*
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
JEREMY R. KELLY
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
RASHMI V. KHADILKAR
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
KEVIN F. HEACOCK
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
SHAELAN M. MCCORMICK
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
KELLY E. WILLIAMS
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
ROBERT N. JINKS
Affiliation:
Department of Biology, Biological Foundations of Behavior Program, and Biochemistry and Molecular Biology Program, Franklin & Marshall College, Lancaster, Pennsylvania
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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.

Keywords

PhotoreceptorsPhotoreceptor metabolismEfferent neurotransmissionCircadian rhythmsSecond messenger
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 5 , September 2004 , pp. 749 - 763
Copyright
2004 Cambridge University Press

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