In search of the molecular mechanisms of adaptation memory in rods: basic activity of phosphodiesterase

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Retinal rods, the photoreceptors responsible for twilight vision, are capable of adapting to a wide range of light levels. The molecular mechanisms of light adaptation have been well studied, but an interesting question is what changes occur in the phototransduction cascade after the adaptive light stimuli are eliminated. Previously, we showed the phenomenon of adaptation memory in amphibian rods: after background illumination photoreceptor sensitivity to light remained reduced for several minutes, while the dark current recovered within 20—30 s. This suggests the existence of additional, as yet unknown, regulatory mechanisms of the phototransduction cascade that act after the adaptive effect of light. In search of specific mechanisms that could explain the effect of adaptation memory, we performed electrophysiological experiments on isolated frog rods to evaluate the basal activity of the effector enzyme of the phototransduction cascade, the phosphodiesterase type 6, in the dark and after saturating background illumination. It was found that the post-adaptation state of rods was characterized by increased basal phosphodiesterase activity, which gradually decreased to the dark level within tens of seconds after turning off the adaptive illumination. These results also suggest that the components of the phototransduction cascade may undergo some unstudied changes after light adaptation.

Full Text

Restricted Access

About the authors

D. A. Nikolaeva

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences

Email: lubkins@yandex.ru
Russian Federation, 194223, Saint-Petersburg, Thorez, 44

M. L. Firsova

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences

Email: lubkins@yandex.ru
Russian Federation, 194223, Saint-Petersburg, Thorez, 44

L. A. Astakhova

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences

Author for correspondence.
Email: lubkins@yandex.ru
Russian Federation, 194223, Saint-Petersburg, Thorez, 44

References

  1. Astakhova L. A., Firsov M. L., Govardovskii V. I. Kinetics of turn-offs of frog rod phototransduction cascade. J. Gen. Physiol. 2008. V. 132(5). P. 587—604. https://doi.org/10.1085/jgp.200810034
  2. Astakhova L. A., Samoiliuk E. V., Govardovskii V. I., Firsov M. L. cAMP controls rod photoreceptor sensitivity via multiple targets in the phototransduction cascade. J. Gen. Physiol. 2012. V. 140(4). P. 421—433. https://doi.org/10.1085/jgp.201210811
  3. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J. Physiol. 1979. V. 288. P. 613—634. https://doi.org/10.1113/jphysiol.1979.sp012716
  4. Calvert P. D., Govardovskii V. I., Arshavsky V. Y., Makino C. L. Two temporal phases of light adaptation in retinal rods. J. Gen. Physiol. 2002. V. 119(2). P. 129—146. https://doi.org/10.1085/jgp.119.2.129
  5. Cornwall M. C., Fain G. L. Bleached pigment activates transduction in isolated rods of the salamander retina. J. Physiol. 1994. V. 480(2). P. 261—279. https://doi.org/10.1113/jphysiol.1994.sp020358
  6. Cornwall M. C., Matthews H. R., Crouch R. K., Fain G. L. Bleached pigment activates transduction in salamander cones. J. Gen. Physiol. 1995. V. 106(3). P. 543—557. https://doi.org/10.1085/jgp.106.3.543
  7. Govardovskii V. I. Firsov M. L. Unknown mechanisms regulating the GPCR signal cascade in vertebrate photoreceptors. Neurosci. Behav. Physiol. 2012. V. 42. P. 180—192. https://doi.org/10.1007/s11055-011-9551-1
  8. Hodgkin A. L., Nunn B. J. Control of light-sensitive current in salamander rods. J. Physiol. 1988. V. 403. P. 439—471. https://doi.org/10.1113/jphysiol.1988.sp017258
  9. Hodgkin A. L., McNaughton P.A., Nunn B. J. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J. Physiol. 1985. V. 358. P. 447—468. https://doi.org/10.1113/jphysiol.1985.sp015561
  10. Lamb T. D. Photoreceptor physiology and evolution: cellular and molecular basis of rod and cone phototransduction. J. Physiol. 2022. V. 600(21). P. 4585—4601. https://doi.org/10.1113/JP282058
  11. Nikolaeva D. A., Nekrasova M. A., Rotov A. Y., Astakhova L. A. Adaptation memory in photoreceptors: different mechanisms in rods and cones. Front. Mol. Neurosci. 2023. V. 16. P. 1135088. https://doi.org/10.3389/fnmol.2023.1135088
  12. Paglia M. J., Mou H., Cote R. H. Regulation of photoreceptor phosphodiesterase (PDE6) by phosphorylation of its inhibitory gamma subunit re-evaluated. J. Biol. Chem. 2002. V. 277. P. 5017—5023. http://dx.doi.org/10.1074/jbc.M106328200
  13. Pugh Jr., Edward N., Lamb T. D. Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In: Handbook of biological physics. 2000. V. 3. 183—255. https://doi.org/10.1016/S1383—8121(00)80008—1
  14. Rotov A. Y., Astakhova L. A., Firsov M. L., Govardovskii V. I. Light adaptation of retinal rods, adaptation memory, and afterimages. Neurosci. Behav. Physiol. 2021. V. 51. P. 116—122. https://doi.org/10.1007/s11055-020-01046-2
  15. Vinberg F., Chen J., Kefalov V. J. Regulation of calcium homeostasis in the outer segments of rod and cone photoreceptors. Prog. Retin. Eye Res. 2018.V. 67. P. 87—101. https://doi.org/10.1016/j.preteyeres.2018.06.001

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Measurement of basic PDE activity in single rods of the frog retina in the dark and post-adaptation states: a - diagram of a typical experimental protocol, including light stimulation (shown by a thick black line) and a short-term testing application of 0.5 mM IBMX (shown by arrows); b - actual experimental recording of rod current using the protocol shown in panel a (for illustrative purposes, the recording was subjected to digital Gaussian filtering with a 7-sigma window); c - example of a change in the rod current during short-term application of 0.5 mM IBMX to its outer segment. The solid black line is the current curve of a rod in the dark state, the dotted line is the current curve of the same rod 45 s after turning off the 40-second adaptive background illumination with an intensity of 415 photons/μm2/s; d - the result of normalization to the dark current and extraction of the cubic root for the current curves shown in panel c (the current curve of a rod in the dark state, the dotted line is the current curve of the same rod 45 s after turning off the background illumination). The graph also shows linear regressions that approximate the linear portions of the curves and slope values characterizing the baseline PDE activity; e — changes in the basic activity of PDE relative to the dark value, along the y-axis — the increase factor; *—significant differences relative to unity (p < 0.05, Student’s t test).

Download (636KB)

Copyright (c) 2024 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies