Major facilitator superfamily

Microbiology and Molecular Biology Reviews

Volumn 62, Issue 1, 1998, Pages 1-34

  Pao, Stephanie S ^a   Paulsen, Ian T ^a,b   Saier Jr , Milton H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ANTIPORTER; CARRIER PROTEIN; CYANIC ACID; FUCOSE; GALACTOSE; GLUCOSE; NITRATE; NITRITE; NUCLEOSIDE; OLIGOPEPTIDE; ORGANOPHOSPHATE; OXALIC ACID; PERMEASE; PHOSPHATE; PROTON;

AMINO ACID SEQUENCE; ARCHAEBACTERIUM; CELL MEMBRANE TRANSPORT; COMPUTER PROGRAM; EUKARYOTE; ION EXCHANGE; NONHUMAN; PHYLOGENY; PROTEIN FAMILY; PROTON TRANSPORT; REVIEW; SEQUENCE HOMOLOGY; TANDEM REPEAT;

ARCHAEA; EUKARYOTA;

EID: 0031888525     PISSN: 10922172     EISSN: None     Source Type: Journal    
DOI: 10.1128/mmbr.62.1.1-34.1998     Document Type: Review

References (96)

1. Abe, K., Z. S. Ruan, and P. C. Maloney. 1996. Cloning, sequencing, and expression in Escherichia coli of OxlT, the oxalate:formate exchange protein of Oxalobacter formigenes. J. Biol. Chem. 271:6789-6793.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Ambudkar, S. V., and P. C. Maloney. 1984. Characterization of phosphate: hexose 6-phosphate antiport in membrane vesicles of Streptococcus lactis. J. Biol. Chem. 259:12576-12585.
4. Anantharam, V., M. J. Allison, and P. C. Maloney. 1989. Oxalate:formate exchange: the basis for energy coupling in Oxalobacter. J. Biol. Chem. 264:7244-7250.
5. Bailey, T. L., and C. Elkan. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers, p. 28-36. In Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology. AAAI Press, Menlo Park, Calif.
6. Bairoch, A., P. Bucher, and K. Hofmann. 1997. The PROSITE database, its status in 1997. Nucleic Acids Res. 25:217-221.
7. Baldwin, S. A. 1993. Mammalian passive glucose transporters: members of an ubiquitous family of active and passive transport proteins. Biochem. Biophys. Acta 1154:17-49.
8. 7a.Boles, E., and C. P. Hollenberg. 1997. The molecular genetics of hexose transport in yeasts. FEMS. Microbiol. Rev. 21:85-111.
9. Brooker, R. J., and T. H. Wilson. 1985. Isolation and nucleotide sequencing of lactose carrier mutants that transport maltose. Proc. Natl. Acad. Sci. USA 82:3959-3963.
10. Bun-Ya, M., M. Nishimura, S. Harashima, and Y. Oshima. 1991. The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol. Cell. Biol. 11:3229-3238.
11. Calamia, J., and C. Manoil. 1990. Lac permease of Escherichia coli: topology and sequence elements promoting membrane insertion. Proc. Natl. Acad. Sci. USA 87:4937-4941.
12. Collier, L. S., N. N. Nichols, and E. L. Neidle. 1997. benK encodes a hydrophobic permease-like protein involved in benzoate degradation by Acinetobacter sp. strain ADP1. J. Bacteriol. 179:5943-5946.
13. Collins, J. C., S. F. Permuth, and R. J. Brooker. 1989. Isolation and characterization of lactose permease mutants with an enhanced recognition of maltose and diminished recognition of cellobiose. J. Biol. Chem. 264:14698-14703.
14. Crouzet, P., and L. Otten. 1995. Sequence and mutational analysis of a tartrate utilization operon from Agrobacterium vitis. J. Bacteriol. 177:6518-6526.
15. Dayhoff, M. O., W. C. Barker, and L. T. Hunt. 1983. Establishing homologies in protein sequences. Methods Enzymol. 91:524-545.
16. Dean, M., and R. Allikmets. 1995. Evolution of ATP-binding cassette transporter genes. Curr. Opin. Genet. Dev. 5:779-785.
17. Devereux, J., P. Hasberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programmes for the VAX. Nucleic Acids Res. 12:387-395.
18. Dimroth, P. 1997. Primary sodium ion translocating enzymes. Biochim. Biophys. Acta 1318:11-51.
19. Doolittle, R. F. 1986. Of urfs and orfs: a primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, Calif.
20. Essenberg, R. C. 1987. The stimulation by salts of hexose phosphate uptake by Escherichia coli. Biochem. J. 243:345-350.
21. Essenberg, R. C., C. Candler, and S. K. Nida. 1997. Brucella abortus strain 2308 putative glucose and galactose transporter gene: cloning and characterization. Microbiology 143:1549-1555.
22. Fath, M. J., and R. Kolter. 1993. ABC transporters: bacterial exporters. Microbiol. Rev. 57:995-1017.
23. Feng, D.-F., and R. F. Doolittle. 1990. Progressive alignment and phylogenelic tree construction of protein sequences. Methods Enzymol. 183:375-387.
24. Franco, P. J., and R. J. Brooker. 1994. Functional roles of Glu-269 and Glu-325 within the lactose permease of Escherichia coli. J. Biol. Chem. 269:7379-7386.
25. Fu, D., and P. C. Maloney. 1997. Evaluation of secondary structure of OxlT, the oxalate transporter of Oxalobacter formigenes, by circular dichroism spectroscopy. J. Biol. Chem. 272:2129-2135.
26. Garcia, C. K., J. L. Goldstein, R. K. Pathak, R. G. Anderson, and M. S. Brown. 1994. Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates: implications for the Cori cycle. Cell 76:865-873.
27. Goffeau, A., J. Park, I. T. Paulsen, J.-L. Jonniaux, T. Dinh, P. Mordant, and M. H. Saier, Jr. 1997. Multidrug-resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames within the major facilitator superfamily. Yeast 13:43-54.
28. Goswitz, V. C., and R. J. Brooker. 1993. Isolation of lactose permease mutants which recognize arabinose. Membr. Biochem. 10:61-70.
29. Goswitz, V. C., and R. J. Brooker. 1995. Structural features of the uniporter/symporter/anti-porter superfamily. Protein Sci. 4:534-537.
30. Gott, P., and W. Boos. 1988. The transmembrane topology of the sn-glycerol-3-phosphate permease of Escherichia coli analyzed by phoA and lacZ protein fusions. Mol. Microbiol. 2:655-663.
31. Griffith, J. K., M. E. Baker, D. A. Rouch, M. G. P. Page, R. A. Skurray, I. T. Paulsen, K. F. Chater, S. A. Baldwin, and P. J. F. Henderson. 1992. Membrane transport proteins: implications of sequence comparisons. Curr. Opin. Cell Biol. 4:684-695.
32. + symport protein, FucP, for transport of L-fucose into Escherichia coli. Mol. Microbiol. 12:799-809.
33. + symport protein, FucP, from Escherichia coli. Mol. Microbiol. 15:771-783.
34. Harrison, M. J., and M. L. van Buuren. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626-629.
35. Harwood, C. S., N. N. Nichols, M.-K. Kim, J. L. Ditty, and R. E. Parales. 1994. Identification of the pcaRKF gene cluster from Pseudomonas putida: involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J. Bacteriol. 176:6479-6488.
36. Henderson, P. J. F. 1991. Sugar transport proteins. Curr. Opin. Struct. Biol. 1:590-601.
37. Henderson, P. J. F., and M. C. J. Maiden. 1990. Homologous sugar transport proteins in Escherichia coli and their relatives in both prokaryotes and eukaryotes. Philos. Trans. R. Soc. London Ser. B 326:391-410.
38. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
39. Island, M. D., and R. J. Kadner. 1993. Interplay between the membrane-associated UhpB and UhpC regulatory proteins. J. Bacteriol. 175:5028-5034.
40. Jessen-Marshall, A. E., N. J. Paul, and R. J. Brooker. 1995. The conserved motif GXXX (D/E) (R/K)X G[X] (R/K) (R/K), in hydrophilic loop 2/3 of the lactose permease. J. Biol. Chem. 270:16251-16257.
41. Kaback, H. R. 1997. A molecular mechanism for energy coupling in a membrane transport protein, the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 94:5539-5543.
42. Kaback, H. R., E. Bibi, and P. D. Roepe. 1990. β-Galactoside transport in E. coli: a functional dissection of lac permease. Trends Biochem. Sci. 15:309-314.
43. Kaczorowski, G. J., and H. R. Kaback. 1979. Mechanism of lactose translocation in membrane vesicles from Escherichia coli. 1. Effect of pH on efflux, exchange, and counterflow. Biochemistry 18:3691-3697.
44. King, S. C., and T. H. Wilson. 1990. Identification of valine 177 as a mutation altering specificity for transport of sugars by the Escherichia coli lactose carrier. Enhanced specificity for sucrose and maltose. J. Biol. Chem. 265:9638-9644.
45. Kuan, G., E. Dassa, W. Saurin, M. Hofnung, and M. H. Saier, Jr. 1995. Phylogenetic analyses of the ATP-binding constituents of bacterial extracy-toplasmic receptor-dependent ABC-type nutrient uptake permeases. Res. Microbiol. 146:271-278.
46. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
47. 45a.Le, T., and M. H. Saier, Jr. Unpublished programs.
48. Maiden, M. C. J., E. O. Davis, S. A. Baldwin, D. C. M. Moore, and P. J. F. Henderson. 1987. Mammalian and bacterial sugar transport proteins are homologous. Nature 325:641-643.
49. Maiden, M. C. J., M. C. Jones-Mortimer, and P. J. F. Hendersen. 1988. The cloning, DNA sequence, and over express ion of the gene araE coding for arabinose-proton symport in Escherichia coli K12. J. Biol. Chem. 263:8003-8010.
50. Maloney, P. C. 1990. Microbes and membrane biology. FEMS Microbiol. Rev. 87:91-102.
51. Maloney, P. C. 1992. The molecular and cell biology of anion transport by bacteria. Bioessays 14:757-762.
52. Maloney, P. C., S. V. Ambudkar, V. Anantharam, L. A. Sonna, and A. Varadhachary. 1990. Anion-exchange mechanisms in bacteria. Microbiol. Rev. 54:1-17.
53. Marger, M. D., and M. H. Saier, Jr. 1993. A major superfamily of transmembrane facilitators catalyzing uniport, symport and antiport. Trends Biochem. Sci. 18:13-20.
54. Martinez, J., S. Steenbergen, and E. Vimr. 1995. Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain. J. Bacteriol. 177:6005-6010.
55. Mitchell, P. 1967. Translocations through natural membranes. Adv. Enzymol. 29:33-87.
56. Mitchell, P. 1967. Proton-translocation phosphorylation in mitochondria, chloroplasts and bacteria: natural fuel cells and solar cells. Fed. Proc. 26:1370-1379.
57. Neidle, E. L., C. Hartnett L. N. Ornston, A. Bairoch, M. Rekik, and S. Harayama, 1991. Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases. J. Bacteriol. 173:5385-5395.
58. Olsen, S. G., and R. J. Brooker. 1989. Analysis of the structural specificity of the lactose permease toward sugars. J. Biol. Chem. 264:15982-15987.
59. Olsen, S. G., K. M. Greene, and R. J. Brooker. 1993. Lactose permease mutants which transport (malto-)oligosaccharides. J. Bacteriol. 175:6269-6275.
60. Olson, A.L., and J. E. Pessin. 1996. Structure, function, and regulation of the mammalian facilitative glucose transporter gene family. Annu. Rev. Nutr. 16:235-256.
61. Paulsen, I. T., A. M. Beness, and M. H. Saier, Jr. 1997. Computer-based analyses of the protein constituents of transport systems catalyzing export of complex carbohydrates in bacteria. Microbiology 143:2685-2699.
62. Paulsen, I. T., M. H. Brown, and R. A. Skurray. 1996. Proton-dependent multidrug efflux pumps. Microbiol. Rev. 60:575-608.
63. + symporter. J. Bacteriol. 180:498-504.
64. Paulsen, I. T., and R. A. Skurray. 1994. The POT family of transport proteins. Trends Biochem. Sci. 18:404.
65. Paulsen, I. T., M. K. Sliwinski, and M. H. Saier, Jr. Microbial genome analyses: Global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J. Mol. Biol., in press.
66. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
67. +/lactate cotransporter(MCT1). Biochem. J. 320:817-824.
68. Rai, R., F. S. Genbauffe, and T. G. Cooper 1988. Structure and transcription of the allantoate permease gene (DAL5) from Saccharomyces cerevisiae. J. Bacteriol. 170:266-271.
69. Reizer, J., A. Reizer, and M. H. Saier, Jr. 1994. A functional superfamily of sodium/solute symporters. Biochim. Biophys. Acta 1197:133-166.
70. Rowe, J. J., T. Ubbink-Kok, D. Molenaar, W. N. Konings, and A. J. Driessen. 1994. NarK is a nitrite-extrusion system involved in anaerobic nitrate respiration by Escherichia coli. Mol. Microbiol. 12:579-586.
71. Ruan, Z. S., V. Anantharam, I. T. Crawford, S. V. Ambudkar, S. Y. Rhee, M. J. Allison, and P. C. Maloney. 1992. Identification, purification, and reconstitution of OxlT, the oxalate:formate antiport protein of Oxalobacter formigenes. J. Biol. Chem. 267:10537-10543.
72. Rubin, R. A., S. B. Levy, R. L. Heinrikson, and F. J. Kézdy. 1990. Gene duplication in the evolution of the two complementing domains of Gram-negative bacterial tetracycline efflux proteins. Gene 87:7-13.
73. Saier, M. H., Jr. 1994. Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol. Rev. 58:71-93.
74. Saier, M. H., Jr. 1996. Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb. Comp. Genomics 1:129-150.
75. 72a.Saier, M. H., Jr. Unpublished data.
76. 72b.Saier, M. H., Jr. Unpublished data.
77. Saier, M. H., Jr. Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. Adv. Microb. Physiol., in press.
78. Saier, M. H., Jr., I. T. Paulsen, M. K. Sliwinski, S. S. Pao, R. A. Skurray, and H. Nikaido. Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J., in press.
79. 74a.Saier, M. H., Jr., et al. Unpublished data.
80. Seol, W., and A. J. Shatkin. 1991. Escherichia coli kgtP encodes an α-keto-glutarate transporter. Proc. Natl. Acad. Sci. USA 88:3802-3806.
81. Seol, W., and A. J. Shatkin. 1993. Membrane topology model of Escherichia coli α-ketoglutarate permease by PhoA fusion analysis. J. Bacteriol. 175:565-567.
82. Siewe, R. M., B. Weil, A. Burkovski, B. J. Eikmanns, M. Eikmanns, and R. Krämer. 1996. Functional and genetic characterization of the (methyl)ammonium uptake carrier of Corynebacterium glutamicum. J. Biol. Chem. 271:5398-5403.
83. Steiner, H.-Y., F. Naider, and J. M. Becker. 1995. The PTR family: a new group of peptide transporters. Mol. Microbiol. 16:825-834.
84. Sung, Y.-C., and J. A. Fuchs. 1988. Characterization of the cyn operon in Escherichia coli K12. J. Biol. Chem. 263:14769-14775.
85. Tamai, I., H. Takanaga, H. Maeda, Y. Sai, T. Ogihara, H. Higashida, and A. Tsuji. 1995. Participation of a proton-cotransporter, MCT1, in the intestinal transport of monocarboxylic acids. Biochem. Biophys. Res. Commun. 214:482-489.
86. Unkles, S. E., K. L. Hawker, C. Grieve, E. I. Campbell, P. Montague, and J. R. Kinghorn. 1991. crnA encodes a nitrate transporter in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 88:204-208 (Errata, 88:4564, 1991, and 92:3076, 1995.)
87. Varela, M. F., and T. H. Wilson. 1996. Molecular biology of the lactose carrier of Escherichia coli. Biochim. Biophys. Acta 1276:21-34.
88. von Heijne, G. 1992. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225:487-494.
89. Werner, A., M. L. Moore, N. Mantei, J. Biber, G. Semenza, and H. Murer. 1991. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex. Proc. Natl. Acad. Sci. USA 88:9608-9612.
90. Westh Hansen, S. E., N. Jensen, and A. Munch-Petersen. 1987. Studies on the sequence and structure of the Escherichia coli K-12 nupG gene, encoding a nucleoside-transport system. Eur. J. Biochem. 168:385-391.
91. Williams, P. A., and L. E. Shaw. 1997. mucK, a gene in Acinetobacter calcoaceticus ADP1 (BD413), encodes the ability to grow an exogenous cis,cis-muconate as the sole carbon source. J. Bacteriol. 179:5935-5942.
92. + antiporter of Escherichia coli. J. Biochem. 115:958-964.
93. 66, in tetracycline transport. J. Biol. Chem. 265:15525-15530.
94. + antiporter of Escherichia coli encoded by a transposon, Tn10. The role of a conserved sequence motif, GXXXXRXGRR, in a putative cytoplasmic loop between helices 2 and 3. J. Biol. Chem. 267:19155-19162.
95. Yan, R.-T., and P. C. Maloney. 1993. Identification of a residue in the translocation pathway of a membrane carrier. Cell 75:37-44.
96. Yan, R.-T., and P. C. Maloney. 1995. Residues in the pathway through a membrane transporter. Proc. Natl. Acad. Sci. USA 92:5973-5976.