Cellular and subcellular expression of monocarboxylate transporters in the pigment epithelium and retina of the rat

Neuroscience

Volumn 90, Issue 1, 1999, Pages 319-331

  Bergersen, L ^a,b   Johannsson E ^a   Veruki, M L ^a   Nagelhus, E A ^a   Halestrap, A ^c   Sejersted, O M ^a   Ottersen, O P ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN SCHOOL OF SPORT SCIENCES   (Norway)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Electron microscopy; Freeze substitution; Immunocytochemistry; Monocarboxylate transporters; Outer retina; Pigment epithelium

Indexed keywords

ANIMAL TISSUE; ARTICLE; ENERGY CONSUMPTION; MUELLER CELL; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA;

ANIMALS; CARRIER PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TRANSPORTER TYPE 1; MALE; MICROSCOPY, ELECTRON; MONOCARBOXYLIC ACID TRANSPORTERS; MONOSACCHARIDE TRANSPORT PROTEINS; PIGMENT EPITHELIUM OF EYE; RATS; RATS, WISTAR; RETINA;

EID: 0344527986     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00427-8     Document Type: Article

References (58)

1. Adler A.J., Southwick R.E. Distribution of glucose and lactate in the interphotoreceptor matrix. Ophthal. Res. 24:1992;243-252.
2. Ames A. III Energy requirements of CNS cells as related to their function and to their vulnerability to ischemia: a commentary based on studies on retina. Can. J. Physiol. Pharmac. 70:1992;S158-S164.
3. Ames A. III, Li Y.Y. Energy requirements of glutamatergic pathways in rabbit retina. J. Neurosci. 12:1992;4234-4242.
4. Dringen R., Gebhardt R., Hamprecht B. Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res. 623:1993;208-214.
5. Edelman J.L., Miller S.S. Epinephrine stimulates fluid absorption across bovine retinal pigment epithelium. Invest. Ophthal. vis. Sci. 32:1991;3033-3040.
6. Garcia C.K., Goldstein J.L., Pathak R.K., Anderson R.G., Brown M.S. Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates: implications for the Cori cycle. Cell. 76:1994;865-873.
7. Garcia C.K., Brown M.S., Pathak R.K., Goldstein J.L. cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J. biol. Chem. 270:1995;1843-1849.
8. Gerhart D.Z., LeVasseur R.J., Broderius M.A., Drewes L.R. Glucose transporter localization in brain using light and electron immunocytochemistry. J. Neurosci. Res. 22:1989;464-472.
9. Gerhart D.Z., Enerson B.E., Zhdankina O.Y., Leino R.L., Drewes L.R. Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am. J. Physiol. 273:1997;E207-E213.
10. Gerhart D.Z., Enerson B.E., Zhdankina O.Y., Leino R.L., Drewes L.R. Expression of the monocarboxylate transporter MCT2 by rat brain glia. Glia. 22:1998;272-281.
11. Graymore C. N. (1969) General aspects of the metabolism of the retina. In The Eye (ed. Dawson H.), pp. 601-652. Academic, New York.
12. Hamann S., Zeuthen T., la Cour M., Nagelhus E., Ottersen O.P., Agre P., Nilsen S. Aquaporins in complex tissues: communicating networks of water channels in human and rat eye. Am. J. Physiol., Cell Physiol. 274:1998;C1332-C1345.
13. Harik S.I., Kalaria R.N., Whitney P.M., Andersson L., Lundahl P., Ledbetter S.R., Perry G. Glucose transporters are abundant in cells with "occluding" junctions at the blood-eye barriers. Proc. natn. Acad. Sci. U.S.A. 87:1990;4261-4264.
14. Hsu S.C., Molday R.S. Glycolytic enzymes and a GLUT-1 glucose transporter in the outer segments of rod and cone photoreceptor cells. J. biol. Chem. 266:1991;21745-21752.
15. Huang B., Karovski C.J. Light-evoked expansion of subretinal space volume in the retina of the frog. J. Neurosci. 12:1992;4243-4252.
16. Jackson V.N., Price N.T., Carpenter L., Halestrap A.P. Cloning of the monocarboxylate transporter isoform MCT2 from rat testis provides evidence that expression in tissues is species-specific and may involve post-transcriptional regulation. Biochem. J. 324:1997;447-453.
17. Jóhannsson E., Nagelhus E.A., McCullagh K.J., Sejersted O.M., Blackstad T.W., Bonen A., Ottersen O.P. Cellular and subcellular expression of the monocarboxylate transporter MCT1 in rat heart. A high-resolution immunogold analysis. Circulation Res. 80:1997;400-407.
18. Joseph D.P., Miller S.S. Apical and basal membrane ion transport mechanisms in bovine retinal pigment epithelium. J. Physiol., Lond. 435:1991;439-463.
19. Juel C. Lactate-proton cotransport in skeletal muscle. Physiol. Rev. 77:1997;321-358.
20. Kenyon E., Yu K., La Cour M., Miller S.S. Lactate transport mechanisms at apical and basolateral membranes of bovine retinal pigment epithelium. Am. J. Physiol. 267:1994;C1561-C1573.
21. Kenyon E., Maminishkis A., Joseph D.P., Miller S.S. Apical and basolateral membrane mechanisms that regulate pHi in bovine retinal pigment epithelium. Am. J. Physiol. 273:1997;C456-C472.
22. Kirchhof B., Ryan S.J. Differential permeance of retina and retinal pigment epithelium to water: implications for retinal adhesion. Int. Ophthal. 17:1993;19-20.
23. - co-transport in frog retinal pigment epithelium. Acta ophthal. scand. 75:1997;405-408.
24. Leino R.L., Gerhart D.Z., van Bueren A.M., McCall A.L., Drewes L.R. Ultrastructural localization of GLUT 1 and GLUT 3 glucose transporters in rat brain. J. Neurosci. Res. 49:1997;617-626.
25. Li J.D., Govardovskii V.I., Steinberg R.H. Light-dependent hydration of the space surrounding photoreceptors in the cat retina. Vis. Neurosci. 11:1994;743-752.
26. Lin H., Miller S.S. pH regulation in frog retinal pigment epithelium: two apical membrane mechanisms. Am. J. Physiol. 261:1991;C132-C142.
27. Lin H., la Cour M., Andersen M.V., Miller S.S. Proton-lactate cotransport in the apical membrane of frog retinal pigment epithelium. Expl Eye Res. 59:1994;679-688.
28. Mantych G.J., Hageman G.S., Devaskar S.U. Characterization of glucose transporter isoforms in the adult and developing human eye. Endocrinology. 133:1993;600-607.
29. Marmor R. I. (1994) Mechanism of normal retinal adhesion. In Surgical Retina (ed. Ryan S. J.), pp. 1931-1934. Mosby, St Louis, MO.
30. Masterson E., Chader G.J. Characterization of glucose transport by cultured chick pigmented epithelium. Expl Eye Res. 32:1981;279-289.
31. Matsubara A., Laake J.H., Davanger S., Usami S., Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J. Neurosci. 16:1996;4457-4467.
32. McKenna M.C., Tildon J.T., Stevenson J.H., Boatright R., Huang S. Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: differences revealed using aminooxyacetate. Devl Neurosci. 15:1993;320-329.
33. Moseley H., Foulds W.S., Allan D., Kyle P.M. Routes of clearance of radioactive water from the rabbit vitreous. Br. J. Ophthal. 68:1984;145-151.
34. Nagelhus E.A., Veruki M.L., Torp R., Haug F.M., Laake J.H., Nielsen S., Agre P., Ottersen O.P. Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Müller cells and fibrous astrocytes. J. Neurosci. 18:1998;2506-2519.
35. Ottersen O.P., Zhang N., Walberg F. Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience. 46:1992;519-534.
36. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. natn. Acad. Sci. U.S.A. 25:1994;10625-10629.
37. Philp N., Chu P., Pan T.C., Zhang R.Z., Chu M.L., Stark K., Boettiger D., Yoon H., Kieber-Emmons T. Developmental expression and molecular cloning of REMP, a novel retinal epithelial membrane protein. Expl Cell Res. 219:1995;64-73.
38. Philp N., Yoon H., Grollman E.F. Monocarboxylate transporter MCT1 is located in the apical membrane and MCT-3 in the basal membrane of rat RPE. Am. J. Physiol. 274:1998;R1824-R1828.
39. Poitry-Yamate C.L., Poitry S., Tsacopoulos M. Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J. Neurosci. 15:1995;5179-5191.
40. Poole R.C., Halestrap A.P. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am. J. Physiol. 264:1993;C761-C782.
41. Price N.T., Jackson V.N., Halestrap A.P. Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirm the existence of a transporter family with an ancient past. Biochem. J. 329:1998;321-328.
42. Schurr A., Payne R.S., Miller J.J., Rigor B.M. Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J. Neurochem. 69:1997;423-426.
43. Schwarz H., Humbel B.M. Influence of fixatives and embedding media on immunolabelling of freeze-substituted cells. Scanning Microsc. Suppl. 3:1989;57-63.
44. Sickel W. Electrical and metabolic manifestations of receptor and higher-order neuron activity in vertebrate retina. Adv. exp. Med. Biol. 24:1972;101-118.
45. Sugasawa K., Deguchi J., Okami T., Yamamoto A., Omori K., Uyama M., Tashiro Y. Immunocytochemical analyses of distributions of Na, K-ATPase and GLUT1, insulin and transferrin receptors in the developing retinal pigment epithelial cells. Cell Struct. Funct. 19:1994;21-28.
46. 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. Ophthal. vis. Sci. 33:1992;377-383.
47. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16:1996;877-885.
48. van Lookeren Campagne M., Oestreicher A.B., van der Krift T.P., Gispen W.H., Verkleij A.J. Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J. Histochem. Cytochem. 83:1991;47-56.
49. Veruki M.L., Wassle H. Immunohistochemistry localization of dopamine D1 receptors in rat retina. Eur. J. Neurosci. 8:1996;2286-2297.
50. Wang B.L., Larsson L.I. Simultaneous demonstration of multiple antigens by indirect immunofluorescence or immunogold staining: novel light and electron microscopical double and triple staining method employing primary antibodies from the same species. Histochemistry. 83:1985;47-56.
51. Wang L., Tornquist P., Bill A. Glucose metabolism in pig outer retina in light and darkness. Acta physiol. scand. 160:1997;75-81.
52. Wang L., Tornquist P., Bill A. Glucose metabolism of the inner retina in pigs in darkness and light. Acta physiol. scand. 160:1997;71-74.
53. Wang L., Kondo M., Bill A. Glucose metabolism in cat outer retina. Effects of light and hyperoxia. Invest. Ophthal. vis. Sci. 38:1997;48-55.
54. Wilson M.C., Jackson V.N., Heddle C., Price N.T., Pilegaard H., Juel C., Bonen A., Hutter O.F., Halestrap A.P. Lactic acid efflux from white skeletal muscle is catalysed by the monocarboxylate transporter isoform MCT3. J. biol. Chem. 273:1998;15920-15926.
55. Winkler B.S. Glycolytic and oxidative metabolism in relation to retinal function. J. gen. Physiol. 77:1981;667-692.
56. Yoon H., Fanelli A., Grollman E.F., Philp N.J. Identification of a unique monocarboxylate transporter (MCT3) in retinal pigment epithelium. Biochem. biophys. Res. Commun. 234:1997;90-94.
57. Zeuthen T. (1996) Molecular Mechanisms of Water Transport, pp. 1-170. Springer & Lands, Austin, TX.
58. 2O by membrane proteins in retinal pigment epithelium of bullfrog. J. Physiol., Lond. 497:1996;3-17.