Energy sources for glutamate neurotransmission in the retina: Absence of the aspartate/glutamate carrier produces reliance on glycolysis in glia

Journal of Neurochemistry

Volumn 101, Issue 1, 2007, Pages 120-131

  Xu, Y ^a   Ola, M S ^a   Berkich, D A ^a   Gardner, T W ^a   Barber, A J ^a   Palmieri, F ^b   Hutson, S M ^c   LaNoue, K F ^a,d  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF BARI   (Italy)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d Cellular and Molecular Physiology   (United States)

Author keywords

Aspartate glutamate carrier; Glutamate glutamine cycle; Glycolysis; Malate aspartate shuttle; M ller cells; Retina

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; EXCITATORY AMINO ACID TRANSPORTER; GLUCOSE; GLUTAMIC ACID; LACTIC ACID; MALIC ACID; PYRUVIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DARK ADAPTATION; GLIA; GLYCOLYSIS; IMMUNOHISTOCHEMISTRY; LIGHT ADAPTATION; MALE; MUELLER CELL; NERVE CELL; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; OXIDATION KINETICS; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RAT; RETINA CELL;

ADENOSINE TRIPHOSPHATE; AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; ANTIPORTERS; ENERGY METABOLISM; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; GLYCOLYSIS; MALATES; MALE; METABOLIC NETWORKS AND PATHWAYS; NEUROGLIA; NEURONS; ORGAN CULTURE TECHNIQUES; PHOTORECEPTORS; PHOTOTRANSDUCTION; RATS; RATS, SPRAGUE-DAWLEY; RETINA; SYNAPTIC TRANSMISSION;

EID: 33947279377     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04349.x     Document Type: Article

References (45)

1. Ahmed J., Braun R. D., Dunn R. Jr and Linsenmeier R. A. (1993) Oxygen distribution in the macaque retina. Invest. Ophthalmol. Vis. Sci. 34, 516-521.
2. Ames A. III and Li Y. Y. (1992) Energy requirements of glutamatergic pathways in rabbit retina. J. Neurosci. 12, 4234-4242.
3. Ames A. III, Li Y. Y., Heher E. C. and Kimble C. R. (1992) Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J. Neurosci. 12, 840-853.
4. Bill A. and Sperber G. O. (1990) Aspects of oxygen and glucose consumption in the retina: effects of high intraocular pressure and light. Graefes Arch. Clin. Exp. Ophthalmol. 228, 124-127.
5. Bouvier M., Szatkowski M., Amato A. and Attwell D. (1992) The glial cell glutamate uptake carrier countertransports pH-changing anions. Nature 360, 471-474.
6. Boyer P. D., Koeppe O. J. and Luchsinger W. W. (1956) Direct oxygen transfer in enzymic syntheses coupled to adenosine triphosphate degradation. J. Am. Chem. Soc. 78, 356-357.
7. Braun R. D., Linsenmeier R. A. and Goldstick T. K. (1995) Oxygen consumption in the inner and outer retina of the cat. Invest. Ophthalmol. Vis. Sci. 36, 542-554.
8. Bui B. V., Kalloniatis M. and Vingrys A. J. (2004) Retinal function loss after monocarboxylate transport inhibition. Invest. Ophthalmol. Vis. Sci. 45, 584-593.
9. Cerdan S., Rodrigues T. B., Sierra A., Benito M., Fonseca C. P. and Garcia-Martin M. L. (2006) The redox switch/redox coupling hypothesis. Neurochem. Int. 48, 523-530.
10. Chiry O., Pellerin L., Monnet-Tschudi F., Fishbein W. N., Merezhinskaya N., Magistretti P. J. and Clarke S. (2006) Expression of the monocarboxylate transporter MCT1 in the adult human brain cortex. Brain Res. 1070, 65-70.
11. Dienel G. A. and Cruz N. F. (2004) Nutrition during brain activation: does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought? Neurochem. Int. 45, 321-351.
12. 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.
13. Hinkle P. C., Kumar M. A., Resetar A. and Harris D. L. (1991) Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry 30, 3576-3582.
14. Kasischke K. A., Vishwasrao H. D., Fischer P. J., Zipfel W. R. and Webb W. W. (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocyte glycolysis. Science 305, 99-103.
15. LaNoue K. F. and Schoolwerth A. C. (1979) Metabolite transport in mitochondria (review). Annu. Rev. Biochem. 48, 871-922.
16. LaNoue K. F. and Tischler M. E. (1974) Electrogenic characteristics of the mitochondrial glutamate/aspartate antiporter. J. Biol. Chem. 249, 7522-7528.
17. LaNoue K. F., Berkich D. A., Conway M., Barber A. J., Hu L. Y., Taylor C. and Hutson S. (2001) Role of specific aminotransferases in de novo glutamate synthesis and redox shuttling in the retina. J. Neurosci. Res. 66, 914-922.
18. LaNoue K., Carson V., Berkich D. A. and Hutson S. M. (2006) Mitochondrial/cytosolic interactions via metabolite shuttles and transporters, in Handbook of Neurochemistry and Molecular Neurobiology, 3rd edition (Lajtha A., editor in chief, Gibson G. E. and Dienel G., volume editors), Springer, Heidelberg, Germany; in press.
19. 2+-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated Chinese hamster ovary cells. J. Biol. Chem. 278, 38 686-38 692.
20. Lewis G. P. and Fisher S. K. (2003) Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int. Rev. Cytol. 230, 263-290.
21. Lieth E., LaNoue K. F., Antonetti D. A. and Ratz M. (2000) Diabetes reduces glutamate oxidation and glutamine synthesis in the retina. The Penn State Retina Research Group. Exp. Eye Res. 70, 723-730.
22. 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.
23. Linsenmeier R. A. (1986) Effects of light and darkness on oxygen distribution and consumption in the cat retina. J. Gen. Physiol. 88, 521-542.
24. Magistretti P. J. (2000) Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling. Brain Res. 886, 108-112.
25. Magistretti P. J. and Pellerin L. (1999) Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol. Sci. 14, 177-182.
26. Magistretti P. J., Pellerin L., Rothman D. L. and Shulman R. J. (1999) Energy on demand. Science 283, 496-497.
27. Miki N., Keirns J. J., Marcus F. R., Freeman J. and Bitensky M. W. (1973) Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light. Proc. Natl Acad. Sci. USA 70, 3820-3824.
28. Ola M. S., Berkich D. A., Xu Y., King T. M., Gardner T. W., Simpson I. A. and LaNoue K. F. (2006) Analysis of glucose metabolism in diabetic rat retinas. Am. J. Physiol. Endocrinol. Metab. 290, E1057-E1067.
29. Ottersen O. P., Zhang N. and Walberg F. (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46, 519-534.
30. Oz G., Berkich D. A., Henry P. G., Xu Y., LaNoue K. F., Hutson S. M. and Gruetter R. (2004) Neuroglial metabolism in the awake rat retina: CO2 fixation increases with brain activity. J. Neurosci. 24, 11 273-11 279.
31. Pang J. J., Gao F. and Wu S. M. (2002) Relative contributions of bipolar cell and amacrine cell inputs to light responses of ON, OFF and ON-OFF retinal ganglion cells. Vision Res. 42, 19-27.
32. Patel M. S. (1989) CO2-fixing enzymes, in Neuromethods: Carbohydrate and Energy Metabolism (Baker G. D., ed.), pp. 309-340. The Humana Press Inc, Clifton, NJ.
33. Pow D. V. and Robinson S. R. (1994) Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60, 355-366.
34. Purich D. L. (1998) Advances in the enzymology of glutamine synthesis. Adv. Enzymol. Relat. Areas Mol. Biol. 72, 9-42.
35. Ramos M., del Arco A., Pardo B. et al. (2003) Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res. Dev. Brain Res. 143, 33-46.
36. Sarthy V. P., Pignataro L., Pannicke T., Weick M., Reichbach A., Harada T., Tanaka K. and Marc R. (2005) Glutamate transport by retinal Muller cells in glutamate/aspartate transporter-knockout mice. Glia 49, 184-196.
37. Sibson N. R., Dhankhar A., Mason G. F., Rothman D. L., Behar K. L. and Shulman R. G. (1998) Stoichiometriccoupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl Acad. Sci. USA 95, 316-321.
38. Tsacopoulos M. and Magistretti P. J. (1996) Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885.
39. Wang L., Tornquist P. and Bill A. (1997a) Glucose metabolism in pig outer retina in light and darkness. Acta Physiol. Scand. 160, 75-81.
40. Wang L., Kondo M. and Bill A. (1997b) Glucose metabolism in cat outer retina. Effects of light and hyperoxia. Invest. Ophthalmol. Vis. Sci. 38, 48-55.
41. Williamson J. R. and Corkey B. E. (1969) Assays of intermediates of the citric acid cycle and related compounds by fluorometric enzyme methods, in Methods of Enzymology (Lowenstein J. M., ed.), pp. 435-513. Academic Press, New York.
42. Winkler B. S. (1972) The electroretinogram of the isolated rat retina. Vision Res. 12, 1183-1198.
43. Winkler B. S. (1995) A Quantitative Assessment of Glucose Metabolism in the Isolated Rat Retina. Les Seminarires Ophthalmologiques d' IPSEN: Vision et adaptation. pp. 78-96. Elsevier, Amsterdam.
44. Xu Y., Oz G., LaNoue K. F., Keiger C. J., Berkich D. A., Gruetter R. and Hutson S. M. (2004) Whole brain glutamate evaluated by steady state kinetics using a double isotope procedure, effects of gabapentin. J. Neurochem. 90, 1104-1116.
45. Yau K. W. and Nakatani K. (1984) Cation selectivity of light-sensitive conductance in retinal rods. Nature 309, 352-354.