Role of the glutamate 185 residue in proton translocation mediated by the proton-coupled folate transporter SLC46A1

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 1, 2009, Pages

  Unal, Ersin Selcuk ^a   Zhao, Rongbao ^a   Goldman, I David ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ALBERT EINSTEIN CANCER CENTER   (United States)

Author keywords

Folate transport; Heme carrier protein 1; Hereditary folate malabsorption; Methotrexate; Pemetrexed; Proton coupled folate transporter heme carrier protein 1; Proton coupled transporters

Indexed keywords

BIOTIN; CARRIER PROTEIN; FOLIC ACID; FOLINIC ACID; GLUTAMIC ACID; METHOTREXATE; PEMETREXED; PROTEIN SLC46A1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; INTESTINE ABSORPTION; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; TRANSPORT KINETICS;

AMINO ACID SEQUENCE; CELL MEMBRANE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FOLIC ACID; GLUTAMIC ACID; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; LEUCOVORIN; MEMBRANE TRANSPORT PROTEINS; METHOTREXATE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION;

EID: 67650073369     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00096.2009     Document Type: Article

References (55)

1. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science 301: 610-615, 2003.
2. Andrews NC. When is a heme transporter not a heme transporter? When it's a folate transporter. Cell Metab 5: 5-6, 2007.
3. Carrasco N, Antes LM, Poonian MS, Kaback HR. Lac permease of Escherichia coli: histidine-322 and glutamic acid-325 may be components of a charge-relay system. Biochemistry 25: 4486-4488, 1986.
4. Carrasco N, Puttner IB, Antes LM, Lee JA, Larigan JD, Lolkema JS, Roepe PD, Kaback HR. Characterization of site-directed mutants in the lac permease of Escherichia coli. 2. Glutamate-325 replacements. Biochemistry 28: 2533-2539, 1989.
5. Chattopadhyay S, Moran RG, Goldman ID. Pemetrexed: biochemical and cellular pharmacology, mechanisms, and clinical applications. Mol Cancer Ther 6: 404-417, 2007.
6. Crane RK. The gradient hypothesis and other models of carrier-mediated active transport. Rev Physiol Biochem Pharmacol 78: 99-159, 1977.
7. + and substrate transport by the proton-dependent amino acid symporter PAT1. Biochem J 386: 607-616, 2005.
8. Galic S, Schneider HP, Broer A, Deitmer JW, Broer S. The loop between helix 4 and helix 5 in the monocarboxylate transporter MCT1 is important for substrate selection and protein stability. Biochem J 376: 413-422, 2003.
9. Grewer C, Watzke N, Rauen T, Bicho A. Is the glutamate residue Glu-373 the proton acceptor of the excitatory amino acid carrier 1? J Biol Chem 278: 2585-2592, 2003.
10. Guan L, Kaback HR. Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35: 67-91, 2006.
11. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 3: 177-182, 1997.
12. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301: 616-620, 2003.
13. Jardetzky O. Simple allosteric model for membrane pumps. Nature 211: 969-970, 1966.
14. +/lactose symport. J Biol Chem 274: 4074-4081, 1999.
15. Kaback HR, Sahin-Toth M, Weinglass AB. The Kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2: 610-620, 2001.
16. Kamen BA, Smith AK. A review of folate receptor-α cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv Drug Delivery Res 56: 1085-1097, 2004.
17. Lam-Yuk-Tseung S, Govoni G, Forbes J, Gros P. Iron transport by Nramp2/DMT1: pH regulation of transport by 2 histidines in transmembrane domain 6. Blood 101: 3699-3707, 2003.
18. Lemieux MJ. Eukaryotic major facilitator superfamily transporter modeling based on the prokaryotic GlpT crystal structure. Mol Membr Biol 24: 333-341, 2007.
19. Lichtarge O, Sowa ME. Evolutionary predictions of binding surfaces and interactions. Curr Opin Struct Biol 12: 21-27, 2002.
20. Livingstone CD, Barton GJ. Identification of functional residues and secondary structure from protein multiple sequence alignment. Methods Enzymol 266: 497-512, 1996.
21. Luecke H, Richter HT, Lanyi JK. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science 280: 1934-1937, 1998.
22. 2+ transport and uncoupled fluxes. Pflügers Arch 451: 544-558, 2006.
23. Matherly LH, Goldman DI. Membrane transport of folates. Vitam Horm 66: 403-456, 2003.
24. Meredith D, Price RA. Molecular modeling of PepT1 - towards a structure. J Membr Biol 213: 79-88, 2006.
25. Mita AC, Sweeney CJ, Baker SD, Goetz A, Hammond LA, Patnaik A, Tolcher AW, Villalona-Calero M, Sandler A, Chaudhuri T, Molpus K, Latz JE, Simms L, Chaudhary AK, Johnson RD, Rowinsky EK, Takimoto CH. Phase I and pharmacokinetic study of pemetrexed administered every 3 wk to advanced cancer patients with normal and impaired renal function. J Clin Oncol 24: 552-562, 2006.
26. Onsager L. The motion of ions: principles and concepts. Science 166: 1359-1364, 1969.
27. Pao SS, Paulsen IT, Saier MH Jr. Major facilitator superfamily. Microbiol Mol Biol Rev 62: 1-34, 1998.
28. Pinto LH, Dieckmann GR, Gandhi CS, Papworth CG, Braman J, Shaughnessy MA, Lear JD, Lamb RA, DeGrado WF. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc Natl Acad Sci USA 94: 11301-11306, 1997.
29. Puttner IB, Sarkar HK, Padan E, Lolkema JS, Kaback HR. Characterization of site-directed mutants in the lac permease of Escherichia coli. 1. Replacement of histidine residues. Biochemistry 28: 2525-2533, 1989.
30. Qiu A, Jansen M, Sakaris A, Min SH, Chattopadhyay S, Tsai E, Sandoval C, Zhao R, Akabas MH, Goldman ID. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127: 917-928, 2006.
31. Qiu A, Min SH, Jansen M, Malhotra U, Tsai E, Cabelof DC, Matherly LH, Zhao R, Akabas MH, Goldman ID. Rodent intestinal folate transporters (SLC46A1): secondary structure, functional properties, and response to dietary folate restriction. Am J Physiol Cell Physiol 293: C1669-C1678, 2007.
32. Rahman B, Schneider HP, Broer A, Deitmer JW, Broer S. Helix 8 and helix 10 are involved in substrate recognition in the rat monocarboxylate transporter MCT1. Biochemistry 38: 11577-11584, 1999.
33. Rastogi VK, Girvin ME. Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402: 263-268, 1999.
34. Sahin-Toth M, Kaback HR. Arg-302 facilitates deprotonation of Glu-325 in the transport mechanism of the lactose permease from Escherichia coli. Proc Natl Acad Sci USA 98: 6068-6073, 2001.
35. Sahin-Toth M, Karlin A, Kaback HR. Unraveling the mechanism of the lactose permease of Escherichia coli. Proc Natl Acad Sci USA 97: 10729-10732, 2000.
36. Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS. The major facilitator superfamily. J Mol Microbiol Biotechnol 1: 257-279, 1999.
37. Sharif KA, Goldman ID. Rapid determination of membrane transport parameters in adherent cells. Biotechniques 28: 926-932, 2000.
38. + channel. J Gen Physiol 117: 469-490, 2001.
39. Steel A, Nussberger S, Romero MF, Boron WF, Boyd CA, Hediger MA. Stoichiometry and pH dependence of the rabbit proton-dependent oligopeptide transporter PepT1. J Physiol 498: 563-569, 1997.
40. Stokstad ELR. Historical perspective on key advances in the biochemistry and physiology of folates. In: Folic Acid Metabolism in Health and Disease, edited by MF Picciano and ELR Stokstad. New York: Wiley-Liss, 1990, p. 1-21.
41. Stover PJ. Physiology of folate and vitamin B12 in health and disease. Nutr Rev 62: S3-S12, 2004.
42. Takimoto CH, Hammond-Thelin LA, Latz JE, Forero L, Beeram M, Forouzesh B, de Bono J, Tolcher AW, Patnaik A, Monroe P, Wood L, Schneck KB, Clark R, Rowinsky EK. Phase I and pharmacokinetic study of pemetrexed with high-dose folic acid supplementation or multivitamin supplementation in patients with locally advanced or metastatic cancer. Clin Cancer Res 13: 2675-2683, 2007.
43. +-coupled nutrient, micronutrient and drug transporters in the mammalian small intestine. Exp Physiol 92: 603-619, 2007.
44. Tredan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 99: 1441-1454, 2007.
45. Umapathy NS, Gnana-Prakasam JP, Martin PM, Mysona B, Dun Y, Smith SB, Ganapathy V, Prasad PD. Cloning and functional characterization of the proton-coupled electrogenic folate transporter and analysis of its expression in retinal cell types. Invest Ophthalmol Vis Sci 48: 5299-5305, 2007.
46. 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 1178: 1407-1414, 2008.
47. von Heijne G. Membrane-protein topology. Nat Rev Mol Cell Biol 7: 909-918, 2006.
48. Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O'Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PC, Iwata S, Henderson PJ, Cameron AD. Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322: 709-713, 2008.
49. Zhao R, Babani S, Gao F, Liu L, Goldman ID. The mechanism of transport of the multitargeted antifolate, MTA-LY231514, and its cross resistance pattern in cell with impaired transport of methotrexate. Clin Cancer Res 6: 3687-3695, 2000.
50. Zhao R, Gao F, Hanscom M, Goldman ID. A prominent low-pH methotrexate transport activity in human solid tumor cells: contribution to the preservation of methotrexate pharmacological activity in HeLa cells lacking the reduced folate carrier. Clin Cancer Res 10: 718-727, 2004.
51. Zhao R, Matherly LH, Goldman ID. Membrane transporters and folate homeostasis: intestinal absorption and transport into systemic compartments and tissues. Expert Rev Mol Med 11: e4, 2009.
52. Zhao R, Min SH, Qiu A, Sakaris A, Goldberg GL, Sandoval C, Malatack JJ, Rosenblatt DS, Goldman ID. The spectrum of mutations in the PCFT gene, coding for an intestinal folate transporter, that are the basis for hereditary folate malabsorption. Blood 110: 1147-1152, 2007.
53. 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 284: 4267-4274, 2009.
54. Zhao R, Qiu A, Tsai E, Jansen M, Akabas MH, Goldman ID. The proton-coupled folate transporter (PCFT): impact on pemetrexed transport and on antifolate activities compared with the reduced folate carrier. Mol Pharmacol 74: 854-862, 2008.
55. Zvelebil MJ, Barton GJ, Taylor WR, Sternberg MJ. Prediction of protein secondary structure and active sites using the alignment of homologous sequences. J Mol Biol 195: 957-961, 1987.