The contribution of glycolytic and oxidative pathways to retinal photoreceptor function

Investigative Ophthalmology and Visual Science

Volumn 44, Issue 6, 2003, Pages 2708-2715

  Bui, Bang V ^a   Kalloniatis, Michael ^a,b   Vingrys, Algis J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUTAMINE; LACTIC ACID;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL METABOLISM; CERVICAL SPINE DISLOCATION; CONTROLLED STUDY; DARK ADAPTATION; ELECTRORETINOGRAPHY; GLUCOSE METABOLISM; GLYCOLYSIS; HYPOXEMIA; LIGHT ADAPTATION; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RAT; RETINA;

AEROBIOSIS; ANAEROBIOSIS; ANIMALS; ANOXEMIA; DARK ADAPTATION; DRUG COMBINATIONS; ELECTRORETINOGRAPHY; GLUCOSE; GLUTAMINE; GLYCOLYSIS; HYPOGLYCEMIA; LACTIC ACID; OXIDATIVE STRESS; OXYGEN; PHOTORECEPTORS, VERTEBRATE; PHOTOTRANSDUCTION; RATS; RATS, LONG-EVANS; VITREOUS BODY;

EID: 0038823729     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.02-1054     Document Type: Article

References (71)

1. Ames A, Li Y-Y, Heher EC, Kimble CR. Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J Neurosci. 1992;12:840-853.
2. Napper GA, Pianta MJ, Kalloniatis M. Localization of amino acid neurotransmitters following in vitro ischemia and anoxia in the rat retina. Vis Neurosci. 2001;18:413-427.
3. Yotsukura J, Adachi-Usami E. Correlation of electroretinographic changes with visual prognosis in central retinal artery occlusion. Ophthalmologica. 1993;207:13-18.
4. Johnson MA, Hood DG. Rod photoreceptor transduction is affected in central retinal vein occlusion associated with iris neovascularisation. J Opt Soc Am. 1996;13:572-576.
5. Kang-Derwent J, Linsenmeier RA. Effects of hypoxemia on the a-and b-waves of the electroretinogram in the cat retina. Invest Ophthalmol Vis Sci. 2000;41:3634-3642.
6. Steinberg RH. Monitoring communications between photoreceptors and pigment epithelial cell: effects of "mild" systemic hypoxia. Invest Ophthalmol Vis Sci. 1987;28:1888-1904.
7. Linsenmeier RA. Electrophysiological consequences of retinal hypoxia. Graefes Arch Clin Exp Ophthalmol. 1990;228:143-150.
8. Zuckerman R, Cheasty JE, Wang Y. Optical mapping of inner retinal tissue PO2. Curr Eye Res. 1993;12:809-825.
9. Winkler BS. Glycolytic and oxidative metabolism in relation to retinal function. J Gen Physiol. 1981;77:667-692.
10. Wang L, Kondo M, Bill A. Glucose metabolism in cat outer retina: effects of light and hyperoxia. Invest Ophthalmol Vis Sci. 1997;38:48-55.
11. Cringle SJ, Yu DY, Yu PK, Su EN. Intraretinal oxygen consumption in the rat in vivo. Invest Ophthalmol Vis Sci. 2002;43:1922-1927.
12. Bill A, Sperber GO. Aspects of oxygen and glucose consumption in the retina: effects of high intraocular pressure and light. Graefes Arch Clin Exp Ophthalmol. 1990;228:124-127.
13. Witkovsky P, Yang CY. Transport and phosphorylation of 2-deoxy-D-glucose by amphibian retina: effects of light and darkness. J Gen Physiol. 1982;80:173-190.
14. Macaluso C, Onoe S, Niemeyer G. Changes in glucose level affect rod function more than cone function in the isolated, perfused cat eye. Invest Ophthalmol Vis Sci. 1992;33:2798-2808.
15. Winkler BS, Dang L, Malinoski C, Easter SS Jr. An assessment of rat photoreceptor sensitivity to mitochondrial blockade. Invest Ophthalmol Vis Sci. 1997;38:1569-1577.
16. Tsacopoulos M, Magistretti PJ. Metabolic coupling between glia and neurons. J Neurosci. 1996;16:877-885.
17. Sonnewald U, Westergaard N, Schousboe A. Glutamate transport and metabolism in astrocytes. Glia. 1997;21:56-63.
18. Bui BV, Vingrys AJ. Development of receptoral responses in pigmented and albino guinea-pigs (Cavia porcellus). Doc Ophthalmol. 1999;99:151-170.
19. Naarendorp F, Sato Y, Cajdric A, Hubbard NP. Absolute and relative sensitivity of the scotopic system of rat: electroretinography and behavior. Vis Neurosci. 2001;18:641-656.
20. Dureau P, Bonnel S, Menasche M, Dufier JL, Abitbol M. Quantitative analysis of intravitreal injections in the rat. Curr Eye Res. 2001;22:74-77.
21. Hughes A. A schematic eye for the rat. Vision Res. 1979;19:569-588.
22. Hsu SC, Molday RS. Glucose metabolism in photoreceptor outer segments: its role in phototransduction and in NADPH-requiring reactions. J Biol Chem. 1994;269:17954-17959.
23. Hood DC, Birch DG. A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Vis Neurosci. 1990;5:379-387.
24. Nixon PJ, Bui BV, Armitage JA, Vingrys AJ. The contribution of cone responses to rat electroretinograms. Clin Exp Ophthalmol. 2001;29:193-196.
25. Effron B, Gong G. A leisurely look at the bootstrap, the jackknife, and cross-validation. Am Stat. 1983;37:36-48.
26. Howard DR, Sawyer DC. Electroretinography of acute hypoxic and increased intraocular pressure status in the dog. Am J Vet Res. 1975;36:81-84.
27. Linsenmeier RA, Mines AH, Steinberg RH. Effects of hypoxia and hypercapnia on the light peak and electroretinogram of the cat. Invest Ophthalmol Vis Sci. 1983;24:37-46.
28. Graymore CN. Biochemistry of the retina. In: Graymore CN, ed. Biochemistry of the Eye. London: Academic Press; 1970:645-735.
29. Cohen LH, Noell WK. Glucose catabolism of rabbit retina before and after development of visual function. J Neurochem. 1960;5:253-276.
30. Ames A, Walseth TF, Heyman RA, et al. Light-induced increases in cGMP metabolic flux correspond with electrical responses of photoreceptors. J Biol Chem. 1986;261:13034-13042.
31. Penn RD, Hagin WA. Kinetics of the photocurrent of retinal rods. Biophysical J. 1972;12:1073-1094.
32. Hughes WF. Quantitation of ischemic damage in the rat retina. Exp Eye Res. 1991;53:573-582.
33. Quastel JH. Fifty years of biochemistry: a personal account. Can J Biochem. 1974;52:71-82.
34. Cox DW, Bachelard HS. Attenuation of evoked field potentials from dentate granule cells by low glucose, pyruvate + malate, and sodium fluoride. Brain Res. 1982;239:527-534.
35. Lewis LD, Ljunggren B, Ratcheson RA, Siesjo BK. Cerebral energy state in insulin-induced hypoglycemia, related to blood glucose and to EEG. J Neurochem. 1974;23:673-679.
36. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG. Energy on demand. Science. 1999;283:496-497.
37. Dienel GA, Hertz L. Glucose and lactate metabolism during brain activation. J Neurosci Res. 2001;66:824-838.
38. Chung I, Zhang Y, Eubanks JH, Zhang L. Attenuation of hypoxic current by intracellular applications of ATP regenerating agents in hippocampal CA1 neurons of rat brain slices. Neuroscience. 1998;86:1101-1107.
39. Ouanonou A, Zhang Y, Zhang L. Changes in the calcium dependence of glutamate transmission in the hippocampal CA1 region after brief hypoxia-hypoglycemia. J Neurophysiol. 1999;82:1147-1155.
40. Zeevalk GD, Nicklas WJ. Lactate prevents the alterations in tissue amino acids, decline in ATP, and cell damage due to aglycemia in retina. J Neurochem. 2000;75:1027-1034.
41. McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR. Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem. 1996;66:386-393.
42. Hassel B, Johannessen CU, Sonnewald U, Fonnum F. Quantification of the GABA shunt and the importance of the GABA shunt versus the 2-oxoglutarate dehydrogenase pathway in GABAergic neurons. J Neurochem. 1998;71:1511-1518.
43. Tornquist P, Alm A. Retinal and choroidal contribution to retinal metabolism in vivo: a study in pigs. Acta Physiol Scand. 1979;106:351-357.
44. Kumagai AK, Glasgow BJ, Pardridge WM. GLUT1 glucose transporter expression in the diabetic and nondiabetic human eye. Invest Ophthalmol Vis Sci. 1994;35:2887-2894.
45. Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H. Ultracytochemical localization of the erythrocyte/HepG2-type glucose transporter (GLUT1) in cells of the blood-retinal barrier in the rat. Invest Ophthalmol Vis Sci. 1992;33:377-383.
46. Pelligrino DA, Segil LJ, Albrecht RF. Brain glucose utilization and transport and cortical function in chronic vs. acute hypoglycemia. Am J Physiol. 1990;259:E729-E735.
47. Crane PD, Pardridge WM, Braun LD, Nyerges AM, Oldendorf WH. The interaction of transport and metabolism on brain glucose utilization: a reevaluation of the lumped constant. J Neurochem. 1981;36:1601-1604.
48. Wender R, Brown AM, Fern R, et al. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci. 2000;20:6804-6810.
49. Feise G, Kogure K, Busto KR, Scheinberg P, Reinmuth OM. Effect of insulin hypoglycemia upon cerebral energy metabolism and EEG activity in the rat. Brain Res. 1977;126:263-280.
50. Swanson RA, Choi DW. Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab. 1993;13:162-169.
51. Johnson NF. Retinal glycogen content during ischaemia. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1977;203:271-282.
52. Mizuno K, Sato K. Reassessment of histochemistry of retinal glycogen. Exp Eye Res. 1975;21:489-497.
53. Wassilewa P, Hockwin O, Korte I. Glycogen concentration changes in retina, vitreous body and other eye tissues caused by disturbances of blood circulation. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1976;199:115-120.
54. Lipton P. Regulation of glycogen in the dentate gyrus of the in vitro guinea pig hippocampus: effect of combined deprivation of glucose and oxygen. J Neurosci Methods. 1989;28:147-154.
55. Linsenmeier RA, Yancey CM. Effects of hyperoxia on the oxygen distribution in the intact cat retina. Invest Ophthalmol Vis Sci. 1989;30:612-618.
56. Nihira M, Anderson K, Gorin FA, Burns MS. Primate rod and cone photoreceptors may differ in glucose accessibility. Invest Ophthalmol Vis Sci. 1995;36:1259-1270.
57. Okubo A, Sameshima M, Unoki K, Uehara F, Ohba N. Ultracytochemical demonstration of glycogen in cone, but not in rod, photoreceptor cells in the rat retina. Anat Anz. 1998;180:307-314.
58. Hirsch-Hoffman C, Niemeyer G. Changes in plasma glucose level affect rod-but not cone-ERG in the anesthetised cat. Clin Vision Sci. 1993;8:489-501.
59. Romano C, Price M, Bai HY, Olney JW. Neuroprotectants in Honghua: glucose attenuates retinal ischemic damage. Invest Ophthalmol Vis Sci. 1993;34:72-80.
60. Harik SI, Kalaria RN, Whitney PM, et al. Glucose transporters are abundant in cells with "occluding" junctions at the blood-eye barriers. Proc Natl Acad Sci USA. 1990;87:4261-4264.
61. Rennie MJ, Bowtell JL, Bruce M, Khogali SE. Interaction between glutamine availability and metabolism of glycogen, tricarboxylic acid cycle intermediates and glutathione. J Nutr. 2001;131:2488S-2490S.
62. Poitry-Yamate CL, Poitry S, Tsacopoulos M. Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J Neurosci. 1995;15:5179-5191.
63. Bittar PG, Charnay Y, Pellerin L, Bouras C, Magistretti PJ. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J Cereb Blood Flow Metab. 1996;16:1079-1089.
64. Stryer L. Biochemistry. 4th ed. New York: W. H. Freeman; 1995.
65. Napper GA, Kalloniatis M. Neurochemical changes following post-mortem ischemia in the rat retina. Vis Neurosci. 1999;16:1169-1180.
66. Halestrap AP, Price NT. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J. 1999;343:281-299.
67. Varoqui H, Zhu H, Yao D, Ming H, Erickson JD. Cloning and functional identification of a neuronal glutamine transporter. J Biol Chem. 2000;275:4049-4054.
68. Benjamin AM, Verjee ZH, Quastel JH. Kinetics of cerebral uptake processes in vitro of L-glutamine, branched-chain L-amino acids, and L-phenylalanine: effects of ouabain. J Neurochem. 1980;35:67-77.
69. Ereciñska M, Silver IA. Metabolism and role of glutamate in mammalian brain. Prog Neurobiol. 1990;35:245-296.
70. Tildon JT, McKenna MC, Stevenson J, Couto R. Transport of L-lactate by cultured rat brain astrocytes. Neurochem Res. 1993;18:177-184.
71. Broer S, Rahman B, Pellegri G, et al. Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT 1) expressing Xenopus laevis oocytes: expression of two different monocarboxylate transporters in astroglial cells and neurons. J Biol Chem. 1997;272:30096-30102.