Molecular and biochemical characterization of folate transport proteins in retinal müller cells

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 6, 2010, Pages 3226-3235

  Renee Bozard, B ^a   Ganapathy, Preethi S ^a   Duplantier, Jennifer ^a   Mysona, Barbara ^a   Ha, Yonju ^a   Roon, Penny ^a   Smith, Robert ^a   David Goldman, I ^b   Prasad, Puttur ^a   Martin, Pamela M ^a   Ganapathy, Vadivel ^a   Smith, Sylvia B ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCARBOXYLASE; FOLATE RECEPTOR 1; FOLIC ACID; PROTON COUPLED FOLATE TRANSPORTER; REDUCED FOLATE CARRIER; 5 METHYLTETRAHYDROFOLIC ACID; 5-METHYLTETRAHYDROFOLATE; CARRIER PROTEIN; CELL SURFACE RECEPTOR; FOLR1 PROTEIN, MOUSE; SLC46A1 PROTEIN, MOUSE; TETRAHYDROFOLIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; MOUSE; MUELLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; DRUG EFFECT; ENDOSOME; GENE EXPRESSION REGULATION; GENETICS; GLIA; METABOLISM; PH; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ENDOSOMES; GENE EXPRESSION REGULATION; HYDROGEN-ION CONCENTRATION; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEUROGLIA; RECEPTORS, CELL SURFACE; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRAHYDROFOLATES; THIAMINE PYROPHOSPHATE;

EID: 77953266081     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4833     Document Type: Article

References (50)

1. Knox DL, Chen MF, Guilarte TR, Dang CV, Burnette J. Nutritional amblyopia: folic acid, vitamin B-12, and other vitamins. Retina. 1982;2:288-293.
2. Smiddy WE, Green WR. Nutritional amblyopia: a histopathologic study with retrospective clinical correlation. Graefe's Arch Clin Exp Ophthalmol. 1987;225:321-324.
3. Golnik KC, Schaible ER. Folate-responsive optic neuropathy. J Neurophthalmol. 1994;14:163-169.
4. Miller NR. The optic nerve. Curr Opin Neurol. 1996;9:5-15.
5. Sadun A, Rubin R. Residual psychophysical deficits following recovery from the Cuban epidemic of optic neuropathy. In: Laksh-minarayan V, ed. Basic and Clinical Applications of Vision Science. Dordrecht: Kluwer; 1997:231-234.
6. Garner CD, Lee EW, Louis-Ferdinand RT. Müller cell involvement in methanol-induced retinal toxicity. Toxicol Appl Pharmacol. 1995;130:101-107.
7. Johlin FC, Swain E, Smith C, Tephly TR. Studies on the mechanism of methanol poisoning: purification and comparison of rat and human liver 10-formyltetrahydrofolate dehydrogenase. Mol Pharmacol. 1989;35:745-750.
8. Selhub J, Bagley LC, Miller J, Rosenberg IH. B vitamins, homocys-teine, and neurocognitive function in the elderly. Am J Clin Nutr. 2000;71:614S-620S.
9. Heuberger RA, Fisher AI, Jacques PF, et al. Relation of blood homocysteine and its nutritional determinants to age-related macu-lopathy in the third National Health and Nutrition Examination Survey. Am J Clin Nutr. 2002;76:897-902.
10. Axer-Siegel R, Bourla D, Ehrlich R, et al. Association of neovascular age-related macular degeneration and hyperhomocysteinemia. Am J Ophthalmol. 2004;137:84-89.
11. Tsina EK, Marsden DL, Hansen RM, Fulton AB. Maculopathy and retinal degeneration in cobalamin C methylmalonic aciduria and homocystinuria. Arch Ophthalmol. 2005;123:1143-1146.
12. Seddon JM, Gensler G, Klein ML, Milton RC. Evaluation of plasma homocysteine and risk of age-related macular degeneration. Am J Ophthalmol. 2006;141:201-203.
13. Bleich S, Jünemann A, von Ahsen N, et al. Homocysteine and risk of open-angle glaucoma. J Neural Transm. 2002;109:1499-1504.
14. Yang G, Lu J, Pan C. The impact of plasma homocysteine level on development of retinopathy in type 2 diabetes mellitus. Zhonghua Nei Ke Za Zhi. 2002;41:34-38.
15. Spiegelstein O, Eudy JD, Finnell RH. Identification of two putative novel folate receptor genes in humans and mouse. Gene. 2000; 258:117-125.
16. Antony AC. Folate receptors. Annu Rev Nutr. 1996;16:501-521.
17. Lee HC, Shoda R, Krall JA, Foster JD, Selhub J, Rosenberry TL. Folate binding protein from kidney brush border membranes contains components characteristic of a glycoinositol phospholipid anchor. Biochemistry. 1992;31:3236-3243
18. Shen F, Wu M, Ross JF, Miller D, Ratnam M. Folate receptor type gamma is primarily a secretory protein due to lack of an efficient signal for glycosylphosphatidylinositol modification: protein characterization and cell type specificity. Biochemistry. 1995;34: 5660-5665.
19. Sirotnak FM, Tolner B. Carrier-mediated membrane transport of folates in mammalian cells. Ann Rev Nutr. 1999;19:91-122.
20. Ganapathy V, Smith SB, Prasad PD. SLC19: the folate/thiamine transporter family. Pflugers Arch. 2004;447:641-646.
21. Qiu A, Jansen M, Sakaris A, et al. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell. 2006;127:917-928.
22. Shayeghi M, Latunde-Dada GO, Oakhill JS, et al. Identification of an intestinal heme transporter. Cell. 2005;122:789-801.
23. Unal ES, Zhao R, Qiu A, Goldman ID. N-linked glycosylation and its impact on the electrophoretic mobility and function of the human proton-coupled folate transporter (HsPCFT). Biochim Biophys Acta. 2008;1778:1407-1414.
24. Zhao R, Goldman ID. The molecular identity and characterization of a proton-coupled folate transporter-PCFT: biological ramifications and impact on the activity of pemetrexed. Cancer Metast Rev. 2007;26:129-139.
25. Umapathy NS, Gnana-Prakasam JP, Martin PM, et al. Cloning and functional characterization of the proton-coupled electrogenic folate transporter and analysis of its expression in retinal cell types. Invest Ophthalmol Vis Sci. 2007;48:5299-5305.
26. Chancy CD, Kekuda R, Huang W, et al. Expression and differential polarization of the reduced-folate transporter-1 and the folate receptor a in mammalian RPE. J Biol Chem. 2000;275:20676-20684.
27. Smith SB, Kekuda R, Gu X, Chancy C, Conway SJ, Ganapathy V. Expression of folate receptor alpha in the mammalian RPE and retina. Invest Ophthalmol Vis Sci. 1999;40:840-848.
28. Bridges CC, El-Sherbeny A, Ola MS, Ganapathy V, Smith SB. Tran-scellular transfer of folate across the RPE. Curr Eye Res. 2002;24: 129-138.
29. Naggar H, Ola MS, Moore P, et al. Downregulation of reduced-folate transporter by glucose in cultured RPE cells and in RPE of diabetic mice. Invest Ophthalmol Vis Sci. 2002;43:556-563.
30. Smith SB, Huang W, Chancy C, Ganapathy V. Regulation of the reduced folate transporter by nitric oxide in cultured human retinal pigment epithelial cells. Biochem Biophys Res Commun. 1999;257:279-283.
31. Naggar H, Fei YJ, Ganapathy V, Smith SB. Regulation of reduced-folate transporter-1 (RFT-1) by homocysteine and identity of transport systems for homocysteine uptake in retinal pigment epithelial (RPE) cells. Exp Eye Res. 2003;77:687-697.
32. Hosoya K, Fujita K, Tachikawa M. Involvement of reduced folate carrier 1 in the inner blood-retinal barrier transport of methyltet-rahydrofolate. Drug Metab Pharmacokinet. 2008;23:285-292.
33. Sarthy V, Ripps H. The Retinal Muller Cell. New York: Kluwer Academic/Plenum Publishers; 2001:14-116.
34. Li Q, Puro DG. Diabetes-induced dysfunction of the glutamate transporter in retinal Muller cells. Invest Ophthalmol Vis Sci. 2002;43:3109-3116.
35. Wang Z, Li W, Mitchell CK, Carter-Dawson L. Activation of protein kinase C reduces GLAST in the plasma membrane of rat Muller cells in primary culture. Vis Neurosci. 2003;20:611-619
36. c, in the newly developed rat retinal Muller cell line (TR-MUL). Glia. 2003;43:208-217.
37. c) exchanger in cultured retinal ganglion cells and regulation by nitric oxide and oxidative stress. Cell Tiss Res. 2006; 324:189-202.
38. Kim D, Kim MJ, Lee JH, et al. Concomitant distribution shift of glial GABA transporter and S100 calcium-binding proteins in the rat retina after kainate-induced excitotoxic injury. Neurosci Lett. 2003;353:17-20.
39. El-Sherbeny A, Naggar H, Miyauchi S, et al. Osmoregulation of taurine transporter function and expression in retinal pigment epithelial, ganglion, and Muller cells. Invest Ophthalmol Vis Sci. 2004;45:694-701.
40. Jiang G, Mysona B, Dun Y, et al. Expression, subcellular localization and regulation of sigma receptor in retinal Muller cells. Invest Ophthamol Vis Sci. 2006;47:5576-5582.
41. Sarthy VP, Brodjian SJ, Dutt K, Kennedy BN, French RP, Crabb JW. Establishment and characterization of a retinal Muller cell line. Invest Ophthalmol Vis Sci. 1998;39:212-216.
42. Zhao R, Min SH, Wang Y, Campanella E, Low PS, Goldman ID. A role for the proton-coupled folate transporter (PCFT-SLC46A1) in folate receptor-mediated endocytosis. J Biol Chem. 2009;284: 4267-4274.
43. Wollack JB, Makori B, Ahlawat S, et al. Characterization of folate uptake by choroid plexus epithelial cells in a rat primary culture model. JNeurochem. 2008;104:1494-1503
44. Zhao R, Matherly LH, Goldman ID. Membrane transporters and folate homeostasis: intestinal absorption and transport into systemic compartments and tissues. Expert Rev Mol Med. 2009;11:e4.
45. Zhao R, Gao F, Wang Y, Diaz GA, Gelb BD, Goldman ID. Impact of the reduced folate carrier on the accumulation of active thiamin metabolites in murine leukemia cells. J Biol Chem. 2001;276: 1114-1118.
46. Nakai Y, Inoue K, Abe N, et al. Functional characterization of human proton-coupled folate transporter/heme carrier protein 1 heterologously expressed in mammalian cells as a folate transporter. J Pharmacol Exp Ther. 2007;322:469-476.
47. Yokooji T, Mori N, Murakami T. Site-specific contribution of proton-coupled folate transporter/haem carrier protein 1 in the intestinal absorption of methotrexate in rats. J Pharm Pharmacol. 2009;61:911-918.
48. Rijnboutt S, Jansen G, Posthuma G, Hynes JB, Schornagel JH, Strous GJ. Endocytosis of GPI-linked membrane folate receptor-a. J Cell Biol. 1996;132:35-47.
49. Kamen AK, Smith AK, Anderson RGW. The folate receptor works in tandem with a probenecid-sensitive carrier in MA104 cells in vitro.J Clin Invest. 1991;87:1442-1449.
50. Zwiener RJ, Johnson CA, Anderson RGW, Kamen BA. Purified folate receptor-5-methyltetrahydrofolic acid interaction at neutral and acid pH. Cancer Res Ther Control. 1992;3:37-42.