Short- and long-term enzymatic regulation secondary to metabolic insult in the rat retina

Journal of Neurochemistry

Volumn 92, Issue 6, 2005, Pages 1350-1362

  Acosta, Monica L ^a   Kalloniatis, Michael ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Aminotransferase; Fluorocitrate; Glutamate; Lactate; Metabolism; Retina

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMINO ACID; ASPARTATE AMINOTRANSFERASE; GLUTAMATE AMMONIA LIGASE; LACTATE DEHYDROGENASE; TRICARBOXYLIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ANOXIA; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; ENERGY YIELD; ENZYMATIC ASSAY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME METABOLISM; ENZYME REGULATION; ENZYME SYNTHESIS; GLIA CELL; HYPOGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; MUELLER CELL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; ANIMALS; ASPARTATE AMINOTRANSFERASES; CELL HYPOXIA; CITRIC ACID CYCLE; DOWN-REGULATION; ENERGY METABOLISM; ENZYME INHIBITORS; ENZYMES; GLUTAMATE SYNTHASE; GLUTAMIC ACID; HYPOGLYCEMIA; LACTATE DEHYDROGENASES; NA(+)-K(+)-EXCHANGING ATPASE; NEUROGLIA; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RETINA; UP-REGULATION;

EID: 15244339527     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02976.x     Document Type: Article

References (95)

1. + transport. J. Neurosci. 12, 840-853.
2. Barnett N. L. and Osbome N. N. (1995) Prolonged bilateral carotid artery occlusion induces electrophysiological and immunohistochemical changes to the rat retina without causing histological damage. Exp. Eye Res. 61, 83-90.
3. Barnett N. L., Pow D. V. and Robinson S. R. (2000) Inhibition of Müller cell glutamine synthetase rapidly impairs the retinal response to light. Glia 30, 64-73.
4. Bittar P. G., Charnay Y., Pellerin L., Bouras C. and Magistretti P. J. (1996) Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J. Cereb. Blood Flow Metab. 16, 1079-1089.
5. Bonavita V. (1965) Molecular and kinetic properties of NAD- and NADP-linked dehydrogenases in the developing retina, in Biochemistry of the Retina (Graymore C. N., ed.), pp. 5-13. Academic Press, London.
6. Bonavita V., Ponte F. and Amore G. (1963) Neurochemical studies on the inherited retinal degeneration of the rat. I. Lactate dehydrogenase in the developing retina. Vision Res. 3, 271-280.
7. Bui B. V., Kalloniatis M. and Vingrys A. J. (2003) The contribution of glycolytic and oxidative pathways to retinal photoreceptor function. Invest. Ophthalmol. Vis. Sci. 44, 2708-2715.
8. Bui B. V., Kalloniatis M. and Vingrys A. J. (2004a) Retinal function loss after monocarboxylate transport inhibition. Invest. Ophthalmol. Vis. Sci. 45, 584-593.
9. Bui B. V., Vingrys A. J., Wellard J. and Kalloniatis M. (2004b) Monocarboxylate transport inhibition alters retinal function and cellular amino acids levels. Eur. J. Neurosci. 20, 1525-1537.
10. Buono R. J. and Lang R. K. (1999) Hypoxic repression of lactate dehydrogenase-B in retina, Exp. Eye Res. 69, 685-693.
11. Cáceda R., Gamboa J. L., Boero J. A., Monge C. C. and Arregui A. (2001) Energetic metabolism in mouse cerebral cortex during chronic hypoxia. Neurosci. Letter 301, 171-174.
12. Cahn R. D., Kaplan N. O., Levine L. and Zwilling E. (1962) Nature and development of lactic dehydrogenases. Science 136, 962-969.
13. Danbolt N. C. (2001) Glutamate uptake. Prog. Neurobiol. 65, 1-105.
14. Dawson D. M., Goodfriend T. L. and Kaplan N. O. (1964) Lactic dehydrogenases: functions of the two types. Rates of synthesis of the two major forms can be correlated with metabolic differentiation. Science 143, 929-933.
15. Dureau P., Bonnel S., Menasche M.; Dufier J. L. and Abitbol M. (2001) Quantitative analysis of intravitreal injections in the rat. Curr. Eye Res. 22, 74-77.
16. Edwards F. A., Konnerth A., Sakmann B. and Takahashi T. (1989) A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflugers Arch. 414, 600-612.
17. Else P. L., Windmill D. J. and Markus V. (1996) Molecular activity of sodium pumps in endotherms and ectotherms. Am. J. Physiol. 271, R1287-R1294.
18. Endo S., Ishiguro S.-I. and Tamai M. (1999) Possible mechanism for the decrease of mitochondrial aspartate aminotransferase activity in ischemic and hypoxic rat retinas. Biochim. Biophys. Acta 1450, 385-396.
19. Engelsen B., Westerberg E., Fonnum F. and Wieloch T. (1986) Effect of insulin-induced hypoglycemia on the concentrations of glutamate and related amino acids and energy metabolites in the intact and decorticated rat neostriatum. J. Neurochem. 47, 1634-1641.
20. Ereciñska M. and Silver I. A. (1990) Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 35, 245-296.
21. Erecinska M., Dagani F., Nelson D., Deas J. and Silver I. A. (1991) Relations between intracellular ions and energy metabolism: a study with monensin in synaptosomes, neurons, and C6 glioma cells. J. Neurosci. 11, 2410-2421.
22. Fletcher E. L. and Kalloniatis M. (1996) Neurochemical architecture of the normal and degenerating rat retina. J. Comp. Neurol. 376, 343-360.
23. Fletcher E. L. and Kalloniatis M. (1997a) Localization of amino acid neurotransmitters during postnatal development of the rat retina. J. Comp. Neurol. 380, 449-471.
24. Fletcher E. L. and Kalloniatis M. (1997b) Neurochemical development of the degenerating rat retina. J. Comp. Neurol. 388, 1-22.
25. Fonnum F., Johnsen A. and Hassel B. (1997) Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia 21, 106-113.
26. Gamberino W. C., Berkich D. A., Lynch C. J., Xu B. and LaNoue K. F. (1997) Role of pyruvate carboxylase in facilitation of synthesis of glutamate and glutamine in cultured astrocytes. J. Neurochem. 69, 2312-2325.
27. Gebhard R. (1991) Cytochemical demonstration of aspartate aminotransferase activity in the rat retina. Brain Res. 539, 337-341.
28. Graymore C. (1963) Metabolism of the developing retina. Lactic dehydrogenase isoenzyme in the normal and degenerating retina. A preliminary communication. Exp. Eye Res. 3, 5-8.
29. 3H-GABA accumulation in rabbit retina after kainic acid treatment. J. Neurosci. Res. 9, 239-251.
30. Hassel B., Paulsen R. E., Johnsen A. and Fonnum F. (1992) Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res. 576, 120-124.
31. Hassel B., Bachelard H., Jones P., Fonnum F. and Sonnewald U. (1997) Trafficking of amino acids between neurons and glia in vivo. Effects of inhibition of glial metabolism by fluoroacetate. J. Cereb. Blood Flow Metab. 17, 1230-1238.
32. Hong S.-S., Gibney G. T., Esquilin M., Yu J. and Xia Y. (2004) Effect of protein kinases on lactate dehydrogenase activity in cortical neurons during hypoxia. Brain Res. 1009, 195-202.
33. Izumi Y., Izumi M., Benz A. M. and Zorumski C. F. (2001) Lactate dehydrogenase release is facilitated by brief sonication of rat hippocampal slices and isolated retinas following acute neuronal damage. J. Neurosci. Meth. 108, 49-55.
34. Jablonski M. M. and Iannaccone A. (2000) Targeted disruption of Müller cell metabolism induces photoreceptor dysmorphogenesis. Glia 32, 192-204.
35. Kalloniatis M. and Fletcher E. L. (1993) Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. J. Comp. Neurol. 336, 174-193.
36. Kalloniatis M. and Napper G. A. (1996) Glutamate metabolic pathways in displaced ganglion cells of the chicken retina. J. Comp. Neurol. 367, 518-536.
37. Kalloniatis M. and Tomisich G. (1999) Amino acid neurochemistry of the vertebrate retina. Prog. Retin. Eye Res. 18, 811-866.
38. Kalloniatis M., Tomisich G. and Marc R. E. (1994) Neurochemical signatures revealed by glutamine labeling in the chicken retina. Vis. Neurosci. 11, 793-804.
39. Kalloniatis M., Marc R. E. and Murry R. (1996) Amino acid signatures in the primate retina. J. Neurosci. 16, 6807-6829.
40. Largo C., Cuevas P., Somjen G. G., del Rio R. M. and Herreras O. (1996) The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuronal survival. J. Neurosci. 16, 1219-1229.
41. Lieth E., LaNoue K. F., Berkich D. A., Xu B., RatZ. M., Taylor C. and Hutson S. M. (2001) Nitrogen shuttling between neurons and glial cells during glutamate synthesis. J. Neurochem. 76, 1712-1723.
42. Linsenmeier R. A. (1990) Electrophysiological consequences of retinal hypoxia. Graefes Arch. Clin. Exp. Ophthalmol. 228, 143-150.
43. Lowry O. H., Roberts N. R. and Lewis C. (1956) The quantitative histochemistry of the retina. J. Biol. Chem. 220, 879-892.
44. Marc R. E., Liu W.-L. S., Kalloniatis M., Raiguel S. F. and van Haesendonck E. (1990) Patterns of glutamate immunoreactivity in the goldfish retina. J. Neurosci. 10, 4006-4034.
45. Marc R. E., Murry R. F. and Basinger S. F. (1995) Pattern recognition of amino acid signatures in retinal neurons. J. Neurosci. 15, 5106-5129.
46. Miura S. (1966) Lactic dehydrogenase isoenzymes of the brain. Folio Psychiatr. Neurol. Jpn 20, 337-347.
47. Muronetz V. I., Shcherbatova N. A. and Nagradova N. K. (1996) Interaction of NAD-dependent dehydrogenases with human erythrocyte membranes. Appl. Biochem. Biotechnol. 61, 39-46.
48. Naarendorp F., Sato Y., Cajdric A. and Hubbard N. P. (2001) Absolute and relative sensitivity of the scotopic system of rat: electroretinography and behavior. Vis. Neurosci. 18, 641-656.
49. Napper G. A. and Kalloniatis M. (1999) Neurochemical changes following post-mortem ischemia in the rat retina. Vis. Neurosci. 16, 1169-1180.
50. Napper G. A., Pianta M. J. and Kalloniatis M. (1999) Reduced glutamate uptake by retinal glial cells under ischemic/hypoxic conditions. Vis. Neurosci. 16, 149-158.
51. Napper G. A., Pianta M. J. and Kalloniatis M. (2001) Localization of amino acid neurotransmitters following in vitro ischemia and anoxia in the rat retina. Vis. Neurosci. 18, 413-427.
52. O'Neal R. M. and Koeppe R. E. (1966) Precursors in vivo of glutamate, aspartate, and their derivatives of rat brain. J. Neurochem. 13, 835-847.
53. Patel A. and Koenig H. (1971) Some neurochemical aspects of fluorocitrate intoxication. J. Neurochem. 18, 621-628.
54. Paulsen R. E., Contestabile A., Villani L. and Fonnum F. (1987) An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J. Neurochem. 48, 1377-1385.
55. Paulsen R. E., Contestabile A., Villani L. and Fonnum F. (1988) The effect of fluorocitrate on transmitter amino acid release from rat striatal slices. Neurochem. Res. 13, 637-641.
56. Payet O., Maurin L., Bonne C. and Muller A. (2004) Hypoxia stimulates glutamate uptake in whole rat retinal cell in vitro. Neurosci. Lett. 356, 148-150.
57. Pellerin L. and Magistretti P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10 625-10 629.
58. Pellerin L., Pellegri G., Bittar P. G., Charnay Y., Bouras C., Martin J.-L., Stella N. and Magistretti P. J. (1998) Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20, 291-299.
59. 2+ pump. Biochem. Biophys. Res. Commun. 268, 625-627.
60. Pepe I. M., Notari L., Cugnoli C., Panfoli I. and Morelli A. (2002) ATP synthesis in the disk membranes of rod outer segments of bovine retina. J. Photochem. Photobiol. B 66, 148-152.
61. Peters R. A. (1957) Mechanism of the toxicity of the active constituent of Dichapetalum cymosum and related compounds. Adv. Enzymol. 18, 113-159.
62. Poitry S., Poitry-Yamate C., Ueberfeld J., MacLeish P. R. and Tsacopoulos M. (2000) Mechanisms of glutamate metabolic signaling in retinal glial (Müller) cells. J. Neurosci. 20, 1809-1821.
63. Poitry-Yamate C. L. and Tsacopoulos M. (1992) Glucose metabolism in freshly isolated Müller glial cells from a mammalian retina. J. Comp. Neurol. 320, 257-266.
64. Poitry-Yamate C. L., Poitry S. and Tsacopoulos M. (1995) Lactate released by Müller glial cells is metabolized by photoreceptors from mammalian retina. J. Neurosci. 15, 5179-5191.
65. Pow D. V. and Crook D. K. (1996) Direct immunocytochemical evidence for the transfer of glutamine from glial cells to neurons: use of specific antibodies directed against the D-stereoisomers of glutamate and glutamine. Neuroscience 70, 295-302.
66. Pow D. V. and Robinson S. R. (1994) Glutamate in some retinal neurons is derived solely from glia. Neuroscience. 60, 355-366.
67. Rego A. C., Areias F. M., Santos M. S. and Oliveira C. R. (1998) Effect of glucose deprivation and acute glutamate exposure in cultured retinal cells. Exp. Neurol. 153, 128-134.
68. Robin L. N. and Kalloniatis M. (1992) Interrelationship between retinal ischemic damage and turnover and metabolism of putative amino acid neurotransmitters, glutamate and GABA. Doc. Ophthalmol. 80, 272-300.
69. Ross C. D. and Godfrey D. A. (1985) Distributions of aspartate aminotransferase and malate dehydrogenase activities in rat retinal layers. J. Histochem. Cytochem. 33, 624-630.
70. Ross C. D., Bowers M. and Godfrey D. A. (1987) Distributions of the activities of aspartate aminotransferase isoenzymes in rat retinal layers. Neurosci. Lett. 74, 205-210.
71. Rowe W. B. and Meister A. (1970) Identification of 1-methionine-S- sulfoximine as the convulsant isomer of methionine sulfoximine. Proc. Natl Acad. Sci. USA 66, 500-506.
72. Salganicoff L. and DeRobertis E. (1965) Subcellular distribution of the enzymes of the glutamic acid, glutamine and gamma-aminobutyric acid cycles in rat brain. J. Neurochem. 12, 287-309.
73. Schurr A., Payne R. S., Miller J. J. and Rigor B. M. (1997) Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res. 774, 221-224.
74. Steinberg R. H. (1987) Monitoring communications between photoreceptors and pigment ephitelial cells: Effects of 'mild' systemic hypoxia. Invest. Ophthalmol. Vis. Sci. 28, 1888-1903.
75. Sun D., Rait J. L. and Kalloniatis M. (2003) Inner retinal neurons display differential responses to N-methyl-D-aspartate receptor activation. J. Comp. Neurol. 465, 38-56.
76. Swanson R. A. and Graham S. H. (1994) Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res. 664, 94-100.
77. Tholey G., Roth-Schechter B. F. and Mandel P. (1981) Activitiy and isoenzyme pattern of lactate dehydrogenase in neurons and astroblasts cultured from brains of chick embryos. J. Neurochem. 36, 77-81.
78. Tsacopoulos M. and Magistretti P. J. (1996) Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885.
79. Tsacopoulos M., Poitry-Yamate C. L., MacLeish P. R. and Poitry S. (1998) Trafficking of molecules and metabolic signals in the retina. Prog. Retin. Eye Res. 17, 429-442.
80. Venkov L., Rosental L. and Manolova M. (1976) Subcellular distribution of LDH isoenzymes in neuronal- and glial-enriched fractions. Brain Res. 109, 323-333.
81. Virgili M., Paulsen R., Villani L., Contestabile A. and Fonnum F. (1991) Temporary impairment of Muller cell metabolism in the rat retina by intravitreal injection of fluorocitrate. Exp. Eye Res. 53, 115-122.
82. Winkler B. S. (1972) The electroretinogram of the isolated rat retina. Vision Res. 12, 1183-1198.
83. Winkler B. S. (1981) Glycolytic and oxidative metabolism in relation to retinal function. J. General Physiol. 77, 667-692.
84. Winkler B. S. (1983) The intermediary metabolism of the retina: Biochemical and functional aspects, in Biochemistry of the Eye (Anderson R. E., ed.), pp. 227-242. American Academy of Ophthalmology, San Francisco.
85. Winkler B. S. (1995) A quantitative assessment of glucose metabolism in the isolated rat retina, in Les Seminaires Ophthalmologiques D'ipsen: Vision and Adaptation (Doly C. Y., Droy-Lefaix M.-T., eds), pp. 78-96. Elsevier Science, Amsterdam.
86. Winkler B. S., Dang L., Malinoski C. and Easter S. S. (1997) An assessment of rat photoreceptor sensitivity to mitochondrial blockade. Invest. Ophthalmol. Vis. Sci. 38, 1569-1577.
87. Winkler B. S., Kapousta-Bruneau N., Arnold M. J. and Green D. (1999) Effects of inhibiting glutamine synthetase and blocking glutamate uptake on b-wave generation in the isolated rat retina. Vis. Neurosci. 16, 345-353.
88. Winkler B. S., Arnold M. J., Brassell M. A. and Puro D. G. (2000) Energy metabolism in human retinal Müller cells. Invest. Ophthalmol Vis. Sci. 41, 3183-3190.
89. Winkler B. S., Sauer M. W. and Starnes C. A. (2003) Modulation of the Pasteur effect in retinal cells: implications for understanding compensatory metabolic mechanisms. Exp. Eye Res. 76, 715-723.
90. Winkler B. S., Sauer M. W. and Starnes C. A. (2004a) Effects of L-glutamate/D-aspartate and monensin on lactic acid production in retina and cultured retinal Müller cells. J. Neurochem. 89, 514-525.
91. Winkler B. S., Starnes C. A., Sauer M. W., Firouzgan Z. and Chen S.-C. (2004b) Cultured retinal neuronal cells and Müller cells both show net production of lactate. Neurochem. Int. 45, 311-320.
92. Wuntch T., Chen R. F. and Vesell E. S. (1970a) Lactate dehydrogenase isozymes: kinetic properties at high enzyme concentrations. Science 167, 63-65.
93. Wuntch T., Chen R. F. and Vesell E. S. (1970b) Lactate dehydrogenase isozymes: further kinetic studies at high enzyme concentration. Science 169, 480-481.
94. Zeevalk G. D. and Nicklas W. J. (1997) Contribution of glial metabolism to neuronal damage caused by partial inhibition of energy metabolism in retina. Exp. Eye Res. 65, 397-405.
95. Zeevalk G. D. and Nicklas W. J. (2000) Lactate prevents the alterations in tissue amino acids, decline in ATP, and cell damage due to aglycemia in retina. J. Neurochem. 75, 1027-1034.