A glia-neuron alanine/ammonium shuttle is central to energy metabolism in bee retina

Journal of Physiology

Volumn 586, Issue 8, 2008, Pages 2077-2091

  Coles, Jonathan A ^a,b   Martiel, Jean Louis ^c   Laskowska, Karolina ^a,b  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c LABORATOIRE TIMC IMAG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 2 METHYLAMINOPROPIONIC ACID; ALANINE; AMMONIA; CHLORIDE; GLUCOSE; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; LACTIC ACID; OXYGEN; PYRUVIC ACID;

AMMONIUM UPTAKE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEE; CONTROLLED STUDY; ENERGY METABOLISM; GLIA CELL; GLUCOSE METABOLISM; MICROELECTRODE; MITOCHONDRION; NERVE CELL; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PHOTORECEPTOR; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; RETINA; AMINO ACID METABOLISM; CELL METABOLISM; INTRACELLULAR TRANSPORT;

ALANINE; ANIMALS; BEES; CELLS, CULTURED; ENERGY METABOLISM; NEUROGLIA; NEURONS; QUATERNARY AMMONIUM COMPOUNDS; RETINA;

EID: 42149145459     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.148734     Document Type: Article

References (57)

1. Andersen B, Rassov A, Westergaard N & Lundgren K (1999). Inhibition of glycogenolysis in primary rat hepatocytes by 1,4-dideoxy-1,4-imino-d-arabinitol. Biochem J 342, 545-550.
2. + ion-selective microelectrode based on the antibiotics nonactin/monactin. Pflugers Arch 412, 359-362.
3. Cardinaud B, Coles JA, Perrottet P, Spencer AJ, Osborne AJ & Tsacopoulos M (1994). The composition of the interstitial fluid in the retina of the honeybee drone: Implications for the supply of substrates of energy metabolism from blood to neurons. Proc R Soc Lond B Biol Sci 257, 49-58.
4. Chih CP & Roberts EL Jr (2003). Energy substrates for neurons during neural activity: A critical review of the astrocyteneuron lactate shuttle hypothesis. J Cereb Blood Flow Metab 23, 1263-1281.
5. +. J Physiol 495, 305-318.
6. Coles JA & Orkand RK (1983). Modification of potassium movement through the retina of the drone (Apis mellifera ♂) by glial uptake. J Physiol 340, 157-174.
7. Coles JA, Orkand RK & Yamate C (1989). Chloride enters glial cells and photoreceptors in response to light stimulation in the retina of the honey bee drone. Glia 2, 287-297.
8. + in the supraoptic nucleus of the rat during reflex bursting activity by oxytocin neurones. J Physiol 439, 383-409.
9. Coles JA & Schneider-Picard G (1989). Amplification of small signals by voltage-gated sodium channels in drone photoreceptors. J Comp Physiol 165, 109-118.
10. + activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol 290, 525-549.
11. Coles JA & Tsacopoulos M (1981). Ionic and possible metabolic interactions between sensory neurones and glial cells in the retina of the honeybee drone. J Exp Biol 95, 75-92.
12. Coles JA, Vega C & Marcaggi P (2000). Metabolic trafficking between cells in nervous tissue. Prog Brain Res 125, 241-254.
13. Corrigan JJ (1969). d -Amino acids in animals. Science 164, 142-145.
14. de Bari L, Atlante A, Guaragnella N, Principato G & Passarella S (2002). d -Lactate transport and metabolism in rat liver mitochondria. Biochem J 365, 391-403.
15. Dienel GA, Ball KK & Cruz NF (2007). A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: Implications for glycogen turnover. J Neurochem 102, 466-478.
16. Dimitracos SA & Tsacopoulos M (1985). The recovery from a transient inhibition of the oxidative metabolism of the photoreceptors of the drone (Apis mellifera ♂). J Exp Biol 119, 165-181.
17. Dionne VE (1976). Characterization of drug iontophoresis with a fast microassay technique. Biophys J 16, 705-717.
18. Elamari A, Gisin N, Munoz JL, Poitry S, Tsacopoulos M & Zbinden H (1997). Photon-counting optical-fiber sensor for the detection of ammonia in neurochemical applications. Sensors Actuators B 38 -39, 183-188.
19. Evêquoz V, Stadelmann A & Tsacopoulos M (1983). The effect of light on glycogen turnover in the retina of the intact honeybee drone (Apis mellifera). J Comp Physiol 150, 69-75.
20. Fillenz M (2005). The role of lactate in brain metabolism. Neurochem Int 47, 413-417.
21. Fujisawa T, Akagi S, Kawase M, Yamamoto M & Ohmori S (2005). d -Lactate metabolism in starved octopus ocellatus. J Exp Zool 303A, 489-496.
22. Halestrap AP & Poole RC (1989). The transport of pyruvate and lactate across mitochondrial and plasma membranes. In Anion Transport Protein of the Red Blood Cell Membrane, ed. Hamasaki NJM, pp. 73-86. Elsevier, Amsterdam.
23. Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL & Shulman RG (2006). Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26, 865-877.
24. +/amino acid transporter rat PAT2 (Slc36a2). Br J Pharmacol 144, 28-41.
25. Larrabee MG (1992). Extracellular intermediates of glucose metabolism: fluxes of endogenous lactate and alanine through extracellular pools in embryonic sympathetic ganglia. J Neurochem 59, 1041-1052.
26. Mackenzie B, Schafer MK, Erickson JD, Hediger MA, Weihe E & Varoqui H (2003). Functional properties and cellular distribution of the system A glutamine transporter SNAT1 support specialized roles in central neurons. J Biol Chem 8, 23720-23730.
27. + in glial cells of bee retina. J Gen Physiol 116, 125-141.
28. Marcaggi P, Jeanne M & Coles JA (2004). Neuron-glial trafficking of NH 4 + and K +: Separate routes of uptake into glial cells of bee retina. Eur J Neurosci 19, 966-976.
29. + into bee retinal glial cells. Eur J Neurosci 11, 167-177.
30. Morikawa A, Hamase K & Zaitsu K (2003). Determination of d -alanine in the rat central nervous system and periphery using column-switching high-performance liquid chromatography. Anal Biochem 312, 66-72.
31. Nehlig A & Coles JA (2007). Cellular pathways of energy metabolism in the brain: Is glucose used by neurons or astrocytes? Glia 55, 1238-1250.
32. Nehlig A, Wittendorp-Rechenmann E & Lam CD (2004). Selective uptake of [14 C]2-deoxyglucose by neurons and astrocytes: High-resolution microautoradiographic imaging by cellular 14 C-trajectography combined with immunohistochemistry. J Cereb Blood Flow Metab 24, 1004-1014.
33. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R & Magistretti PJ (2007). Activity-dependent regulation of energy metabolism by astrocytes: An update. Glia 55, 1251-1262.
34. Pellerin L & Magistretti PJ (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91, 10625-10629.
35. Perrelet A (1970). The fine structure of the retina of the honeybee drone. Z Zellforsch Mikrosk Anat 108, 530-562.
36. Pfeuffer J, Tkác I, Choi I-Y, Merkle H, Ugurbil K, Garwood M & Gruetter R (1999). Localized in vivo 1 H NMR detection of neurotransmitter labeling in rat brain during infusion of [1- 13 C]d -glucose. Magn Reson Med 41, 1077-1083.
37. Poitry-Yamate CL, Poitry S & Tsacopoulos M (1995). Lactate released by Mller cells is metabolized by photoreceptors from mammalian retina. J Neurosci 15, 5179-5191.
38. Provent P, Kickler N, Barbier EL, Bergerot ARF, Goury S, Marcaggi P, Segebarth C & Coles JA (2007). The ammonium-induced increase in rat brain lactate concentration is rapid and reversible and is compatible with trafficking and signaling roles for ammonium. J Cereb Blood Flow Metab 27, 1830-1840.
39. Roos A & Boron WF (1981). Intracellular pH. Physiol Rev 61, 296-434.
40. Sacktor B & Childress CC (1967). Metabolism of proline in insect flight muscle and its significance in stimulating the oxidation of pyruvate. Arch Biochem Biophys 120, 583-588.
41. Saravelos SG & Tsacopoulos M (1995). Iodoacetate inhibits the biosynthesis of alanine in glial cells and its utilization in photoreceptors of the honeybee drone (Apis mellifera) retina. J Comp Physiol B 165, 341-347.
42. Serres S, Bouyer JJ, Bezancon E, Canioni P & Merle M (2003). Involvement of brain lactate in neuronal metabolism. NMR Biomed 16, 430-439.
43. Suarez RK, Darveau CA, Welch KC Jr, O'Brien DM, Roubik DW & Hochachka PW (2005). Energy metabolism in orchid bee flight muscles: carbohydrate fuels all. J Exp Biol 208, 3573-3579.
44. Tekkok SB, Brown AM, Westenbroek R, Pellerin L & Ransom BR (2005). Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J Neurosci Res 81, 644-652.
45. Tsacopoulos M, Coles JA & Van de Werve G (1987). The supply of metabolic substrate from glia to photoreceptors in the retina of the honeybee drone. J Physiol (Paris) 82, 279-287.
46. Tsacopoulos M, Evêquoz-Mercier V, Perrottet P & Buchner E (1988). Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate. Proc Natl Acad Sci U S A 85, 8727-8731.
47. Tsacopoulos M & Magistretti PJ (1996). Metabolic coupling between glia and neurons. J Neurosci 16, 877-885.
48. Tsacopoulos M, Orkand RK, Coles JA, Levy S & Poitry S (1983). Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature 301, 604-606.
49. Tsacopoulos M & Poitry S (1982). Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera). J Gen Physiol 80, 19-55.
50. Tsacopoulos M, Poitry S & Borsellino A (1981). Diffusion and consumption of oxygen in the superfused retina of the drone (Apis mellifera) in darkness. J Gen Physiol 77, 601-628.
51. Tsacopoulos M, Poitry-Yamate CL & Poitry S (1997 a). Ammonium and glutamate released by neurons are signals regulating the nutritive function of a glial cell. J Neurosci 17, 2383-2390.
52. Tsacopoulos M, Poitry-Yamate CL, Poitry S, Perrottet P & Veuthey AL (1997 b). The nutritive function of glia is regulated by signals released by neurons. Glia 21, 84-91.
53. Tsacopoulos M, Veuthey AL, Saravelos G, Perrottet P & Tsoupras G (1994). Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci 14, 1339-1351.
54. Véga C, Martiel JL, Drouhault D, Burckhart MF & Coles JA (2003). Uptake of locally applied deoxyglucose, glucose and lactate by axons and Schwann cells of rat vagus nerve. J Physiol 546, 551-564.
55. Véga C, Poitry-Yamate CL, Jirounek P, Tsacopoulos M & Coles JA (1998). Lactate is released and taken up by isolated rabbit vagus nerve during aerobic metabolism. J Neurochem 71, 330-337.
56. Veuthey AL, Tsacopoulos M, Ruiz de Millan L & Perrottet P (1994). Cellular and subcellular localization of hexokinase, glutamate dehydrogenase and alanine aminotransferase in the honeybee drone retina. J Neurochem 62, 1939-1946.
57. Vrba R (1962). Glucose metabolism in rat brain. Nature 195, 663-665.