The Journal of General Physiology
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Published online Oct 25 2004. doi:10.1085/jgp.200409162
The Rockefeller University Press, 0022-1295 $8.00
JGP, Volume 124, Number 5, 569-585
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Developmental regulation of calcium-dependent feedback in Xenopus rods

Eduardo Solessio1, Shobana S. Mani1, Nicolas Cuenca4, Gustav A. Engbretson1,3, Robert B. Barlow1, and Barry E. Knox1,2

1 Department of Ophthalmology and Center for Vision Research, SUNY Upstate Medical University, Syracuse, NY 13210
2 Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, NY 13210
3 Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, NY 13244
4 Department of Biotechnology, Universidad de Alicante, Alicante, Spain

Address correspondence to Eduardo Solessio, Center for Vision Research, Weiskotten Hall, SUNY Upstate Medical University, 750 East Adams St., Syracuse, NY 13210. Fax: (315) 464-7712; email: solessie{at}upstate.edu

The kinetics of activation and inactivation in the phototransduction pathway of developing Xenopus rods were studied. The gain of the activation steps in transduction (amplification) increased and photoresponses became more rapid as the rods matured from the larval to the adult stage. The time to peak was significantly shorter in adults (1.3 s) than tadpoles (2 s). Moreover, adult rods recovered twice as fast from saturating flashes than did larval rods without changes of the dominant time constant (2.5 s). Guanylate cyclase (GC) activity, determined using IBMX steps, increased in adult rods from ~1.1 s–1 to 3.7 s–1 5 s after a saturating flash delivering 6,000 photoisomerizations. In larval rods, it increased from 1.8 s–1 to 4.0 s–1 9 s after an equivalent flash. However, the ratio of amplification to the measured dark phosphodiesterase activity was constant. Guanylate cyclase–activating protein (GCAP1) levels and normalized Na+/Ca2+, K+ exchanger currents were increased in adults compared with tadpoles. Together, these results are consistent with the acceleration of the recovery phase in adult rods via developmental regulation of calcium homeostasis. Despite these large changes, the single photon response amplitude was ~0.6 pA throughout development. Reduction of calcium feedback with BAPTA increased adult single photon response amplitudes threefold and reduced its cutoff frequency to that observed with tadpole rods. Linear mathematical modeling suggests that calcium-dependent feedback can account for the observed differences in the power spectra of larval and adult rods. We conclude that larval Xenopus maximize sensitivity at the expense of slower response kinetics while adults maximize response kinetics at the expense of sensitivity.

Key Words: signal transduction • photoreceptors • G protein cascade • retina • adaptation


Abbreviations used in this paper: BAPTA-AM, 1,2-bis (2-aminophenoxy) ethane-N,N,N',N'-tetraacetic acid tetrakis (acetoxymethyl ester); ERG, electroretinogram; GC, guanylate cyclase; GCAP, GC-activating protein; IBMX, 3-isobutyl-1-methylxanthine; PDE, phosphodiesterase; R*, photoisomerizations per flash; ROS, rod outer segment.


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