Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 Feb;86(4):1224–1228. doi: 10.1073/pnas.86.4.1224

Transduction heats in retinal rods: tests of the role of cGMP by pyroelectric calorimetry.

W A Hagins 1, P D Ross 1, R L Tate 1, S Yoshikami 1
PMCID: PMC286660  PMID: 2537492

Abstract

The sensory dark current of vertebrate retinal rods is believed to be controlled by light activation of a chain of coupled biochemical cycles that finally regulate the cationic conductance of the plasma membrane by hydrolytically reducing the level of cGMP in rod outer segment cytoplasm. The scheme has been tested by measuring heat production by live frog retinas when stimulated with sequences of light flashes of progressively increasing energy. Using pyroelectric poly(vinylidene 1,1-difluoride) detectors that simultaneously measure transretinal voltage and retinal temperature change, four heat effects assignable to known biochemical cycles in rods have been found. As the dark current shuts down after a flash causing 180-1800 rhodopsin photoisomerizations per rod, a heat burst, q1, raises the retinal temperature 1-2 microK. q1 is closely regulated in size and slightly precedes dark current shutdown. Isobutylmethylxanthine slows and enlarges q1, delaying the dark-current response. Increasing cytoplasmic Ca2+ stops the dark current without affecting q1. Although rod heat production is consistent with splitting of 1-3 microM of free cytoplasmic cGMP during transduction, the kinetics of the two processes do not match the predictions of current cGMP control models.

Full text

PDF
1224

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [PMC free article] [PubMed] [Google Scholar]
  2. Blazynski C., Cohen A. I. Rapid declines in cyclic GMP of rod outer segments of intact frog photoreceptors after illumination. J Biol Chem. 1986 Oct 25;261(30):14142–14147. [PubMed] [Google Scholar]
  3. Chabre M. Trigger and amplification mechanisms in visual phototransduction. Annu Rev Biophys Biophys Chem. 1985;14:331–360. doi: 10.1146/annurev.bb.14.060185.001555. [DOI] [PubMed] [Google Scholar]
  4. Cooper A., Converse C. A. Energetics of primary processes in visula escitation: photocalorimetry of rhodopsin in rod outer segment membranes. Biochemistry. 1976 Jul 13;15(14):2970–2978. doi: 10.1021/bi00659a006. [DOI] [PubMed] [Google Scholar]
  5. Cote R. H., Nicol G. D., Burke S. A., Bownds M. D. Changes in cGMP concentration correlate with some, but not all, aspects of the light-regulated conductance of frog rod photoreceptors. J Biol Chem. 1986 Oct 5;261(28):12965–12975. [PMC free article] [PubMed] [Google Scholar]
  6. Dartnall H. J. The photosensitivities of visual pigments in the presence of hydroxylamine. Vision Res. 1968 Apr;8(4):339–358. doi: 10.1016/0042-6989(68)90104-1. [DOI] [PubMed] [Google Scholar]
  7. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  8. Goldberg N. D., Ames A. A., 3rd, Gander J. E., Walseth T. F. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J Biol Chem. 1983 Aug 10;258(15):9213–9219. [PubMed] [Google Scholar]
  9. Greengard P., Rudolph S. A., Sturtevant J. M. Enthalpy of hydrolysis of the 3' bond of adenosine 3',5'-monophosphate and guanosine 3',5'-monophosphate. J Biol Chem. 1969 Sep 10;244(17):4798–4800. [PubMed] [Google Scholar]
  10. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hagins W. A., Yoshikami S. Proceedings: A role for Ca2+ in excitation of retinal rods and cones. Exp Eye Res. 1974 Mar;18(3):299–305. doi: 10.1016/0014-4835(74)90157-2. [DOI] [PubMed] [Google Scholar]
  12. Haynes L. W., Kay A. R., Yau K. W. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 1986 May 1;321(6065):66–70. doi: 10.1038/321066a0. [DOI] [PubMed] [Google Scholar]
  13. Hodgkin A. L., McNaughton P. A., Nunn B. J., Yau K. W. Effect of ions on retinal rods from Bufo marinus. J Physiol. 1984 May;350:649–680. doi: 10.1113/jphysiol.1984.sp015223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Liebman P. A., Parker K. R., Dratz E. A. The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annu Rev Physiol. 1987;49:765–791. doi: 10.1146/annurev.ph.49.030187.004001. [DOI] [PubMed] [Google Scholar]
  15. Matthews H. R., Murphy R. L., Fain G. L., Lamb T. D. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature. 1988 Jul 7;334(6177):67–69. doi: 10.1038/334067a0. [DOI] [PubMed] [Google Scholar]
  16. Nakatani K., Yau K. W. Calcium and light adaptation in retinal rods and cones. Nature. 1988 Jul 7;334(6177):69–71. doi: 10.1038/334069a0. [DOI] [PubMed] [Google Scholar]
  17. PODOLSKY R. J., MORALES M. F. The enthalpy change of adenosine triphosphate hydrolysis. J Biol Chem. 1956 Feb;218(2):945–959. [PubMed] [Google Scholar]
  18. Reuter T. E., White R. H., Wald G. Rhodopsin and porphyropsin fields in the adult bullfrog retina. J Gen Physiol. 1971 Oct;58(4):351–371. doi: 10.1085/jgp.58.4.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ritchie J. M., Keynes R. D. The production and absorption of heat associated with electrical activity in nerve and electric organ. Q Rev Biophys. 1985 Nov;18(4):451–476. doi: 10.1017/s0033583500005382. [DOI] [PubMed] [Google Scholar]
  20. Robinson W. E., Hagins W. A. GTP hydrolysis in intact rod outer segments and the transmitter cycle in visual excitation. Nature. 1979 Aug 2;280(5721):398–400. doi: 10.1038/280398a0. [DOI] [PubMed] [Google Scholar]
  21. Stern J. H., Knutsson H., MacLeish P. R. Divalent cations directly affect the conductance of excised patches of rod photoreceptor membrane. Science. 1987 Jun 26;236(4809):1674–1678. doi: 10.1126/science.3037695. [DOI] [PubMed] [Google Scholar]
  22. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci. 1986;9:87–119. doi: 10.1146/annurev.ne.09.030186.000511. [DOI] [PubMed] [Google Scholar]
  23. Tasaki I., Byrne P. M., Masumura M. Detection of thermal responses of the retina by use of polyvinylidene fluoride multilayer detector. Jpn J Physiol. 1987;37(4):609–619. doi: 10.2170/jjphysiol.37.609. [DOI] [PubMed] [Google Scholar]
  24. Tasaki I., Nakaye T. Heat produced by the dark-adapted bullfrog retina in response to light pulses. Biophys J. 1986 Aug;50(2):285–293. doi: 10.1016/S0006-3495(86)83462-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. WALD G., BROWN P. K. The molar extinction of rhodopsin. J Gen Physiol. 1953 Nov 20;37(2):189–200. doi: 10.1085/jgp.37.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yau K. W., Nakatani K. Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature. 1985 Sep 19;317(6034):252–255. doi: 10.1038/317252a0. [DOI] [PubMed] [Google Scholar]
  27. Yee R., Liebman P. A. Light-activated phosphodiesterase of the rod outer segment. Kinetics and parameters of activation and deactivation. J Biol Chem. 1978 Dec 25;253(24):8902–8909. [PubMed] [Google Scholar]
  28. Zimmerman A. L., Baylor D. A. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 1986 May 1;321(6065):70–72. doi: 10.1038/321070a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES