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. 1981 Jun 1;77(6):667–692. doi: 10.1085/jgp.77.6.667

Glycolytic and oxidative metabolism in relation to retinal function

PMCID: PMC2215447  PMID: 6267165

Abstract

Measurements of lactate production and ATP concentration in superfused rat retinas were compared with extracellular photoreceptor potentials (Fast PIII). The effect of glucose concentration, oxygen tension, metabolic inhibition, and light were studied. Optimal conditions were achieved with 5-20 mM glucose and oxygen. The isolated retina had a high rate of lactate production and maintained the ATP content of a freshly excised retina, and Fast PIII potentials were similar to in vivo recordings. Small (less than 10%) decreases in aerobic and anaerobic lactate production were observed after illumination of dark- adapted retinas. There were no significant differences in ATP content in dark- and light-adapted retinas. In glucose-free medium, lactate production ceased, and the amplitude of Fast PIII and the level of ATP declined, but the rates of decline were slower in oxygen than in nitrogen. ATP levels were reduced and the amplitude of Fast PIII decreased when respiration was inhibited, and these changes were dependent on glucose concentration. Neither glycolysis alone nor Krebs cycle activity alone maintained the superfused rat retina at an optimal level. Retinal lactate production and utilization of ATP were inhibited by ouabain. Mannose but not galactose or fructose produced lactate and maintained ATP content and Fast PIII. Iodoacetate blocked lactate production and Fast PIII and depleted the retina of ATP. Pyruvate, lactate, and glutamine maintained ATP content and Fast PIII reasonably well (greater than 50%) in the absence of glucose, even in the presence of iodoacetate. addition of glucose, mannose, or 2-deoxyglucose to medium containing pyruvate and iodoacetate abolished Fast PIII and depleted the retina of its ATP. It is suggested that the deleterious effects of these three sugars depend upon their cellular uptake and phosphorylation during the blockade of glycolysis by iodoacetate.

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Selected References

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  1. AMES A., 3rd, GURIAN B. S. Effects of glucose and oxygen deprivation on function of isolated mammalian retina. J Neurophysiol. 1963 Jul;26:617–634. doi: 10.1152/jn.1963.26.4.617. [DOI] [PubMed] [Google Scholar]
  2. Arden G. B. Voltage gradients across the receptor layer of the isolated rat retina. J Physiol. 1976 Apr;256(2):333–360.1. doi: 10.1113/jphysiol.1976.sp011328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berman A. L., Azimova A. M., Gribakin F. G. Localization of Na+, K+-ATPase and Ca2+-activated Mg2+-dependent ATPase in retinal rods. Vision Res. 1977;17(4):527–536. doi: 10.1016/0042-6989(77)90051-7. [DOI] [PubMed] [Google Scholar]
  4. Biernbaum M. S., Bownds M. D. Influence of light and calcium on guanosine 5'-triphosphate in isolated frog rod outer segments. J Gen Physiol. 1979 Dec;74(6):649–669. doi: 10.1085/jgp.74.6.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bownds D., Brodie A. E. Light-sensitive swelling of isolated frog rod outer segments as an in vitro assay for visual transduction and dark adaptation. J Gen Physiol. 1975 Oct;66(4):407–425. doi: 10.1085/jgp.66.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. COHEN L. H., NOELL W. K. Glucose catabolism of rabbit retina before and after development of visual function. J Neurochem. 1960 May;5:253–276. doi: 10.1111/j.1471-4159.1960.tb13363.x. [DOI] [PubMed] [Google Scholar]
  7. Carretta A., Cavaggioni A. On the metabolism of the rod outer segments. J Physiol. 1976 Jun;257(3):687–697. doi: 10.1113/jphysiol.1976.sp011392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Delmelle M., Noell W. K., Organisciak D. T. Hereditary retinal dystrophy in the rat: rhodopsin, retinol, vitamin A deficiency. Exp Eye Res. 1975 Oct;21(4):369–380. doi: 10.1016/0014-4835(75)90047-0. [DOI] [PubMed] [Google Scholar]
  9. FUTTERMAN S. Metabolism of the retina. III. The role of reduced triphoshopyridine nucleotide in the visual cycle. J Biol Chem. 1963 Mar;238:1145–1150. [PubMed] [Google Scholar]
  10. Frank R. N., Goldsmith T. H. Effects of cardiac glycosides on electrical activity in the isolated retina of the frog. J Gen Physiol. 1967 Jul;50(6):1585–1606. doi: 10.1085/jgp.50.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GLOCKLIN V. C., POTTS A. M. THE METABOLISM OF RETINAL PIGMENT CELL EPITHELIUM. II. RESPIRATION AND GLYCOLYSIS. Invest Ophthalmol. 1965 Apr;4:226–234. [PubMed] [Google Scholar]
  12. GRAYMORE C. N., TANSLEY K., KERLY M. Metabolism of the developing retina. 2. The effect of an inherited retinal degeneration on the development of glycolysis in the rat retina. Biochem J. 1959 Jul;72:459–461. doi: 10.1042/bj0720459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GRAYMORE C. Metabolism of the developing retina. I. Aerobic and anaerobic glycolysis in the developing rat retina. Br J Ophthalmol. 1959 Jan;43(1):34–39. doi: 10.1136/bjo.43.1.34. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GRAYMORE C. Metabolism of the developing retina. III. Respiration in the developing normal rat retina and the effect of an inherited degeneration of the retinal neuroepithelium. Br J Ophthalmol. 1960 Jun;44:363–369. doi: 10.1136/bjo.44.6.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GRAYMORE C., TANSLEY K. Iodoacetate poisoning of the rat retina. II. Glycolysis in the poisoned retina. Br J Ophthalmol. 1959 Aug;43:486–493. doi: 10.1136/bjo.43.8.486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HOPKINSON L., KERLY M. The effect of monoiodoacetate on the aerobic metabolism of ox retina in vitro. Biochem J. 1959 May;72(1):22–27. doi: 10.1042/bj0720022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Jaffe M. J., Pautler E. L. The effect of light on the respiration of retinas of several vertebrate and invertebrate species with special emphasis on the effects of acetylcholine and gamma-aminobutyric acid on the frog retina. Exp Eye Res. 1975 Jun;20(6):531–540. doi: 10.1016/0014-4835(75)90220-1. [DOI] [PubMed] [Google Scholar]
  19. KUWABARA T., COGAN D. G. Retinal glycogen. Arch Ophthalmol. 1961 Nov;66:680–688. doi: 10.1001/archopht.1961.00960010682013. [DOI] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROBERTS N. R., SCHULZ D. W., CLOW J. E., CLARK J. R. Quantitative histochemistry of retina. II. Enzymes of glucose metabolism. J Biol Chem. 1961 Oct;236:2813–2820. [PubMed] [Google Scholar]
  21. MERRIAM F. C., KINSEY V. E. Studies on the crystalline lens: technic for in vitro culture of crystalline lenses and observations. Arch Ophthal. 1950 Jun;43(6):979–988. [PubMed] [Google Scholar]
  22. Miki N., Keirns J. J., Marcus F. R., Freeman J., Bitensky M. W. Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3820–3824. doi: 10.1073/pnas.70.12.3820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mizuno K., Sato K. Reassessment of histochemistry of retinal glycogen. Exp Eye Res. 1975 Nov;21(5):489–497. doi: 10.1016/0014-4835(75)90130-x. [DOI] [PubMed] [Google Scholar]
  24. NOELL W. K. The visual cell: electric and metabolic manifestations of its life processes. Am J Ophthalmol. 1959 Nov;48(5):347–370. doi: 10.1016/0002-9394(59)90589-6. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Sloviter H. A., Kamimoto T. The isolated, persed rat brain preparation metabolizes mannose but not maltose. J Neurochem. 1970 Jul;17(7):1109–1111. doi: 10.1111/j.1471-4159.1970.tb02266.x. [DOI] [PubMed] [Google Scholar]
  27. Wheeler G. L., Bitensky M. W. A light-activated GTPase in vertebrate photoreceptors: regulation of light-activated cyclic GMP phosphodiesterase. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4238–4242. doi: 10.1073/pnas.74.10.4238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Winkler B. S. A role for metabolism in photoreceptor electrogenesis. Exp Eye Res. 1978 Jan;26(1):107–110. doi: 10.1016/0014-4835(78)90158-6. [DOI] [PubMed] [Google Scholar]
  29. Winkler B. S. Calcium and the fast and slow components of P3 of the electroretinogram of the isolated rat retina. Vision Res. 1974 Jan;14(1):9–15. doi: 10.1016/0042-6989(74)90110-2. [DOI] [PubMed] [Google Scholar]
  30. Winkler B. S. Dependence of rat and rabbit photoreceptor potentials upon anaerobic and aerobic metabolism in vitro. Exp Eye Res. 1975 Dec;21(6):545–548. doi: 10.1016/0014-4835(75)90036-6. [DOI] [PubMed] [Google Scholar]
  31. Winkler B. S., Riley M. V. Influence of calcium on retinal ATPases. Invest Ophthalmol Vis Sci. 1980 May;19(5):562–564. [PubMed] [Google Scholar]
  32. Winkler B. S., Riley M. V. Na+-K+ and HCO-3 ATPase activity in retina: dependence on calcium and sodium. Invest Ophthalmol Vis Sci. 1977 Dec;16(12):1151–1154. [PubMed] [Google Scholar]
  33. Winkler B. S., Simson V., Benner J. Importance of bicarbonate in retinal function. Invest Ophthalmol Vis Sci. 1977 Aug;16(8):766–768. [PubMed] [Google Scholar]
  34. Winkler B. S. The electroretinogram of the isolated rat retina. Vision Res. 1972 Jun;12(6):1183–1198. doi: 10.1016/0042-6989(72)90106-x. [DOI] [PubMed] [Google Scholar]
  35. 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]

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