Developmental regulation of calcium-dependent feedback in Xenopus rods.
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 approximately 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 approximately 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.
Solessio
Eduardo
E
Center for Vision Research, Weiskotten Hall, SUNY Upstate Medical University, 750 East Adams St., Syracuse, NY 13210, USA. solessie@upstate.edu
Mani
Shobana S
SS
Cuenca
Nicolas
N
Engbretson
Gustav A
GA
Barlow
Robert B
RB
Knox
Barry E
BE
D000221:Adaptation, Ocular / Q000502:physiology* / Q000528:radiation effects; D000222:Adaptation, Physiological / Q000502:physiology / Q000528:radiation effects; D000375:Aging / Q000502:physiology*; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D002478:Cells, Cultured; D003198:Computer Simulation; D005246:Feedback / Q000187:drug effects / Q000502:physiology; D008027:Light; D008564:Membrane Potentials / Q000502:physiology* / Q000528:radiation effects; D008954:Models, Biological; D017948:Retinal Rod Photoreceptor Cells / Q000196:embryology* / Q000502:physiology* / Q000528:radiation effects; D015398:Signal Transduction / Q000502:physiology; D014981:Xenopus
D002118:Calcium