Families of transmembrane transporters selective for amino acids and their derivatives

The information presented in this review was initially prepared for presentation at the FASEB meeting on amino acid transport held in Copper Mountain, Colorado, June 26–July 1, 1999 and was updated in January 2000 following the meeting of the Transport Nomenclature Panel of the International Union of Biochemistry and Molecular Biology (IUBMB) in Geneva, November 28–30, 1999. The system of classification described in this review reflects the recommendations of that panel.

References

1. Aleshin V. V., Zakataeva N. P., Livshits V. A. 1999; A new family of amino acid efflux proteins. Trends Biochem Sci 24:133–135 [CrossRef]
   [Google Scholar]
2. Andersson S. G. E., Zomorodipour A., Andersson J. O.7 other authors 1998; The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140 [CrossRef]
   [Google Scholar]
3. Aquila H., Link T. A., Klingenberg T. 1987; Solute carriers involved in energy transfer of mitochondria form a homologous protein family. FEBS Lett 212:1–9 [CrossRef]
   [Google Scholar]
4. Arriza J. L., Kavanaugh M. P., Fairman W. A., Wu Y. N., Murdoch G. H., North R. A., Amara S. G. 1993; Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. J Biol Chem 268:15329–15332
   [Google Scholar]
5. Beckman M. L., Quick M. W. 1998; Neurotransmitter transporters: regulators of function and functional regulation. J Membr Biol 164:1–10 [CrossRef]
   [Google Scholar]
6. Bennett M. J., Marchant A., Green H. G., May S. T., Ward S. P., Millner P. A., Walker A. R., Schulz B., Feldmann K. A. 1996; Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950 [CrossRef]
   [Google Scholar]
7. Berfield J. L., Wang L. C., Reith M. E. A. 1999; Which form of dopamine is the substrate for the human dopamine transporter: the cationic or the uncharged species?. J Biol Chem 274:4876–4882 [CrossRef]
   [Google Scholar]
8. Berg M., Hilbi H., Dimroth P. 1997; Sequence of a gene cluster from Malonomonas rubra encoding components of the malonate decarboxylase Na⁺ pump and evidence for their function. Eur J Biochem 245:103–105 [CrossRef]
   [Google Scholar]
9. Brechtel C. E., King S. C. 1998; 4-aminobutyrate (GABA) transporters from the amine-polyamine-choline superfamily: substrate specificity and ligand recognition profile of the 4-aminobutyrate permease from Bacillus subtilis. Biochem J 333:565–571
   [Google Scholar]
10. Bröer S., Krämer R. 1991a; Lysine excretion by Corynebacterium glutamicum. I. Identification of a specific secretion carrier system. Eur J Biochem 202:131–135 [CrossRef]
    [Google Scholar]
11. Bröer S., Krämer R. 1991b; Lysine excretion by Corynebacterium glutamicum. II. Energetics and mechanism of the transport system. Eur J Biochem 202:137–143 [CrossRef]
    [Google Scholar]
12. Calamita G., Kempf B., Bonhivers M., Bishai W. R., Bremer E., Agre P. 1998; Regulation of the Escherichia coli water channel gene aqpZ. Proc Natl Acad Sci USA 95:3627–3631 [CrossRef]
    [Google Scholar]
13. Chen L. S. K., Lo C. F., Numann R., Cuddy M. 1997; Characterization of the human and rat phospholemman (PLM) cDNAs and localization of the human PLM gene to chromosome 19q13.1. Genomics 41:435–443 [CrossRef]
    [Google Scholar]
14. Chen X.-Z., Zhu T., Smith D. E., Hediger M. A. 1999; Stoichiometry and kinetics of the high-affinity H⁺-coupled peptide transporter PepT2. J Biol Chem 274:2773–2779 [CrossRef]
    [Google Scholar]
15. Chrispeels M. J., Maurel C. 1994; Aquaporins: the molecular basis of facilitated water movement through living plant cells?. Plant Physiol 105:9–13 [CrossRef]
    [Google Scholar]
16. Clark J. A., Amara S. G. 1993; Amino acid neurotransmitter transporters: structure, function, and molecular diversity. Bioessays 15:323–332 [CrossRef]
    [Google Scholar]
17. Closs E. I., Albritton L. M., Kim J. W., Cunningham J. M. 1993; Identification of a low affinity, high capacity transporter of cationic amino acids in mouse liver. J Biol Chem 268:7538–7544
    [Google Scholar]
18. Cosgriff A. J., Pittard A. J. 1997; A topological model for the general aromatic amino acid permease, AroP, of Escherichia coli. J Bacteriol 179:3317–3323
    [Google Scholar]
19. Couriaud C., Ripoche P., Rousselet G. 1998; Cloning and functional characterization of a rat urea transporter expression in the brain. Biochim Biophys Acta 1309:197–199
    [Google Scholar]
20. Covitz K.-M. Y., Amidon G.-L., Sadée W. 1998; Membrane topology of the human dipeptide transporter, hPEPT1, determined by epitope insertions. Biochemistry 37:15214–15221 [CrossRef]
    [Google Scholar]
21. Daniel H. 1996; Function and molecular structure of brush border membrane peptide/H⁺ symporters. J Membr Biol 154:197–203 [CrossRef]
    [Google Scholar]
22. Dean R. M., Rivers R. L., Zeidel M. L., Roberts D. M. 1999; Purification and functional reconstitution of soybean nodulin 26: an aquaporin with water and glycerol transport properties. Biochemistry 38:347–353 [CrossRef]
    [Google Scholar]
23. Deen P. M. T., van Os C. H. 1998; Epithelial aquaporins. Curr Opin Cell Biol 10:435–442 [CrossRef]
    [Google Scholar]
24. Deguchi Y., Yamato I., Anraku Y. 1990; Nucleotide sequence of gltS, the Na⁺/glutamate symport carrier gene of Escherichia coli B. J Biol Chem 265:21704–21708
    [Google Scholar]
25. Didion T., Regenberg B., Jørgensen M. U., Kielland-Brandt M. C., Andersen H. A. 1998; The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae. Mol Microbiol 27:643–650 [CrossRef]
    [Google Scholar]
26. Dierks T., Salentin A., Heberger C., Krämer R. 1990a; The mitochondrial aspartate/glutamate and ADP/ATP carriers switch from obligate counterexchange to unidirectional transport after modification by SH-reagents. Biochim Biophys Acta 1028:268–280 [CrossRef]
    [Google Scholar]
27. Dierks T., Salentin A., Krämer R. 1990b; Pore-like and carrier-like properties of the mitochondrial aspartate/glutamate carrier after modification by SH-reagents: evidence for a preformed channel as a structural requirement of carrier-mediated transport. Biochim Biophys Acta 1028:281–288 [CrossRef]
    [Google Scholar]
28. Dimroth P., Hilbi H. 1997; Enzymatic and genetic basis for bacterial growth on malonate. Mol Microbiol 25:3–10 [CrossRef]
    [Google Scholar]
29. Döring F., Will J., Amasheh S., Clauss W., Ahlbrecht H., Daniel H. 1998; Minimal molecular determinants of substrates for recognition by the intestinal peptide transporter. J Biol Chem 273:23211–23218 [CrossRef]
    [Google Scholar]
30. Echtay K. S., Bienengraeber M., Winkler E., Klingenberg M. 1998; In the uncoupling protein (UCP-1) His-214 is involved in the regulation of purine nucleoside triphosphate but not diphosphate binding. J Biol Chem 273:24368–24374 [CrossRef]
    [Google Scholar]
31. Eichler K., Bourgis F., Buchet A., Kleber H. P., Mandrand-Berthelot M. A. 1994; Molecular characterization of the cai operon necessary for carnitine metabolism in Escherichia coli. Mol Microbiol 13:775–786 [CrossRef]
    [Google Scholar]
32. Engel P., Krämer R., Unden G. 1994; Transport of C₄-dicarboxylates by anaerobically grown Escherichia coli: energetics and mechanism of exchange, uptake and efflux. Eur J Biochem 222:605–614 [CrossRef]
    [Google Scholar]
33. Eskandari S., Loo D. D. F., Dai G., Levy O., Wright E. M., Carrasco N. 1997; Thyroid Na⁺/I⁻ symporter: mechanism, stoichiometry, and specificity. J Biol Chem 272:27230–27238 [CrossRef]
    [Google Scholar]
34. Farcasanu I. C., Mizunuma M., Hirata D., Miyakawa T. 1998; Involvement of histidine permease (Hip1p) in manganese transport in Saccharomyces cerevisiae. Mol Gen Genet 259:541–548 [CrossRef]
    [Google Scholar]
35. Fei Y.-J., Fujita T., Lapp D. F., Ganapathy V., Leibach F. H. 1998; Two oligopeptide transporters from Caenorhabditis elegans: molecular cloning and functional expression. Biochem J 322:565–572
    [Google Scholar]
36. Feirmonte G., Palmieri L., Dolce V., Lasorsa F. M., Palmieri F., Runswick M. J., Walker J. E. 1998; The sequence, bacterial expression, and functional reconstitution of the rat mitochondrial dicarboxylate transporter cloned via distant homologs in yeast and Caenorhabditis elegans. J Biol Chem 273:24754–24759 [CrossRef]
    [Google Scholar]
37. Fekkes P., Driessen A. J. M. 1999; Protein targeting to the bacterial cytoplasmic membrane. Microbiol Mol Biol Rev 63:161–173
    [Google Scholar]
38. Ferguson D. J., Krzycki J. A. 1997; Reconstruction of trimethylamine-dependent coenzyme M methylation with the trimethylamine corrinoid protein and the isozymes of methyltransferase II from Methanosarcina barkeri. J Bacteriol 179:846–852
    [Google Scholar]
39. Fischer W.-N., Kwart M., Hummel S., Frommer W. B. 1995; Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J Biol Chem 270:16315–16320 [CrossRef]
    [Google Scholar]
40. Forward J., Behrendt M. C., Wyborn N. R., Cross R., Kelly D. J. 1997; TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol 179:5482–5493
    [Google Scholar]
41. Foskett J. K. 1998; ClC and CFTR chloride channel gating. Annu Rev Physiol 60:689–717 [CrossRef]
    [Google Scholar]
42. Frommer W. B., Hummel S., Rentsch D. 1994; Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Lett 347:185–189 [CrossRef]
    [Google Scholar]
43. Fuqua C., Winans S. C., Greenberg E. P. 1996; Census and consensus in bacterial ecosystems: the LuxR–LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50:727–751 [CrossRef]
    [Google Scholar]
44. Galli A., Blakely R. D., DeFelice L. J. 1998; Patch-clamp and amperometric recordings from norepinephrine transporters: channels activity and voltage-dependent uptake. Proc Natl Acad Sci USA 13260:13265
    [Google Scholar]
45. Gälweiler L., Guan C., Müller A., Wisman E., Mendgen K., Yephremov A., Palme K. 1998; Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230 [CrossRef]
    [Google Scholar]
46. Glazebrook J., Ichige A., Walker G. C. 1993; A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev 7:1485–1497 [CrossRef]
    [Google Scholar]
47. Golby P., Kelly D. J., Guest J. R., Andrews S. C. 1998; Topological analysis of DcuA, an anaerobic C₄-dicarboxylate transporter of Escherichia coli. J Bacteriol 180:4821–4827
    [Google Scholar]
48. Goss T. J., Schweizer H. P., Datta P. 1988; Molecular characterization of the tdc operon of Escherichia coli K-12. J Bacteriol 170:5352–5359
    [Google Scholar]
49. Hagting A., Kunji E. R. S., Leenhouts K. J., Poolman B., Konings W. N. 1994; The di- and tripeptide transport protein of Lactococcus lactis. J Biol Chem 269:11391–11399
    [Google Scholar]
50. Hagting A., van der Velde J., Poolman B., Konings W. N. 1997; Membrane topology of the di- and tripeptide transport protein of Lactococcus lactis. Biochemistry 36:6777–6785 [CrossRef]
    [Google Scholar]
51. von Heijne G. 1992; Membrane protein structure prediction: hydrophobicity analysis and positive-inside rule. J Mol Biol 225:487–494 [CrossRef]
    [Google Scholar]
52. Heller K. B., Lin E. C. C., Wilson T. H. 1980; Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol 144:274–278
    [Google Scholar]
53. Hoenke S., Schmid M., Dimroth P. 1997; Sequence of a gene cluster from Klebsiella pneumoniae encoding malonate decarboxylase and expression of the enzyme in Escherichia coli. Eur J Biochem 246:530–538 [CrossRef]
    [Google Scholar]
54. Hu L. A., King S. C. 1998a; Functional significance of the ‘signature cysteine’ in helix 8 of the Escherichia coli 4-aminobutyrate transporter from the amine-polyamine-choline superfamily. J Biol Chem 273:20162–20167 [CrossRef]
    [Google Scholar]
55. Hu L. A., King S. C. 1998b; Functional sensitivity of polar surfaces on transmembrane helix 8 and cytoplasmic loop 8–9 of the Escherichia coli GABA (4-aminobutyrate) transporter encoded by gabP: mutagenic analysis of a consensus amphipathic region found in transporters from bacteria to mammals. Biochem J 330:771–776
    [Google Scholar]
56. Hu L. A., King S. C. 1998c; Membrane topology of the Escherichia coli γ-aminobutyrate transporter: implications on the topology and mechanism of prokaryotic and eukaryotic transporters from the APC superfamily. Biochem J 336:69–76
    [Google Scholar]
57. Ichige A., Walker G. C. 1997; Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J Bacteriol 179:209–216
    [Google Scholar]
58. Indiveri C., Iacobazzi V., Giangregorio N., Palmieri F. 1997; The mitochondria carnitine carrier protein: cDNA cloning, primary structure and comparison with other mitochondrial transport proteins. Biochem J 321:713–719
    [Google Scholar]
59. Isnard A. D., Thomas D., Surdin-Kerjan Y. 1996; The study of methionine uptake in Saccharomyces cerevisiae reveals a new family of amino acid permeases. J Mol Biol 262:473–484 [CrossRef]
    [Google Scholar]
60. Jack D. L., Paulsen I. T., Saier M. H. Jr 2000; The APC superfamily of transporters specific for amino acids, polyamines and organocations. Microbiology 146:1797–1814
    [Google Scholar]
61. Jacobs C., Huang L., Bartowsky E., Normark S., Park J. T. 1994; Bacterial cell wall recycling provides cystolic muropeptides as effectors for β-lactamase induction. EMBO J 13:4684–4694
    [Google Scholar]
62. Jacobs M. H. J., van der Heide T., Driessen A. J. M., Konings W. N. 1996; Glutamate transport in Rhodobacter sphaeroides is mediated by a novel binding protein-dependent secondary transport system. Proc Natl Acad Sci USA 93:12786–12790 [CrossRef]
    [Google Scholar]
63. Jung H., Rübenhagen R., Tebbe S., Leifker K., Tholema N., Quick M., Schmid R. 1998; Topology of the Na⁺/proline transporter of Escherichia coli. J Biol Chem 273:26400–26407 [CrossRef]
    [Google Scholar]
64. Kanamori A., Nakayama J., Fukuda M. N., Stallcup W. B., Sasaki K., Fukuda M., Hirabayashi Y. 1997; Expression, cloning, and characterization of a cDNA encoding a novel membrane protein required for the formation of O-acetylated ganglioside: a putative acetyl-CoA transporter. Proc Natl Acad Sci USA 94:2897–2902 [CrossRef]
    [Google Scholar]
65. Kappes R., Kempf B., Bremer E. 1996; Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J Bacteriol 178:5071–5079
    [Google Scholar]
66. Kashiwagi S., Kanamaru K., Mizuno T. 1995; A Synechococcus gene encoding a putative pore-forming intrinsic membrane protein. Biochim Biophys Acta 1237:189–192 [CrossRef]
    [Google Scholar]
67. Kashiwagi K., Shibuya S., Tomitori H., Kuraishi A., Igaragshi K. 1997; Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J Biol Chem 272:6318–6323 [CrossRef]
    [Google Scholar]
68. Kavanaugh M. P. 1998; Neurotransmitter transport: models in flux. Proc Natl Acad Sci USA 95:12737–12738 [CrossRef]
    [Google Scholar]
69. Kempf B., Bremer E. 1998; Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330 [CrossRef]
    [Google Scholar]
70. Kirk K., Strange K. 1998; Functional properties and physiological roles of organic solute channels. Annu Rev Physiol 60:719–739 [CrossRef]
    [Google Scholar]
71. Knutson V. P. 1991; Cellular trafficking and processing of the insulin receptor. FASEB J 5:2130–2138
    [Google Scholar]
72. Koch H.-G., Hengelage T., Neumann-Haefelin C., MacFarlane J., Hoffschulte H. K., Schimz K.-L., Mechler B., Müller M. 1999; In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol Biol Cell 10:2163–2173 [CrossRef]
    [Google Scholar]
73. Kuan J., Saier M. H. Jr 1993; The mitochondrial carrier family of transport proteins: structural, functional and evolutionary relationships. Crit Rev Biochem Mol Biol 28:209–233 [CrossRef]
    [Google Scholar]
74. Lamark T., Kaasen I., Eshoo M. W., Falkenberg P., McDougall J., Strom A. R. 1991; DNA sequence and analysis of the bet genes encoding the osmoregulatory choline-glycine betaine pathway of Escherichia coli. Mol Microbiol 5:1049–1064 [CrossRef]
    [Google Scholar]
75. Leibach F. H., Ganapathy V. 1996; Peptide transporters in the intestine and the kidney. Annu Rev Nutr 16:99–119 [CrossRef]
    [Google Scholar]
76. Li H., Lee S., Jap B. K. 1997; Molecular design of aquaporin-1 water channel as revealed by electron crystallography. Nat Struct Biol 4:263–265 [CrossRef]
    [Google Scholar]
77. Lindquist S., Weston-Hafer K., Schmidt H., Pul C., Korfmann G., Erickson J., Sanders C., Martin H. H., Normark S. 1993; AmpG, a single transducer in chromosomal β-lactamase induction. Mol Microbiol 9:703–715 [CrossRef]
    [Google Scholar]
78. Lubkowitz M. A., Hauser L., Breslav M., Naider F., Becker J. M. 1997; An oligopeptide transport gene from Candida albicans. Microbiology 143:387–396 [CrossRef]
    [Google Scholar]
79. Lubkowitz M. A., Barnes D., Breslav M., Burchfield A., Naider F., Becker J. M. 1998; Schizosaccharomyces pombe isp4 encodes a transporter representing a novel family of oligopeptide transporters. Mol Microbiol 28:729–741
    [Google Scholar]
80. Lucien N., Sidoux-Walter F., Olives B., Moulds J., Le Pennec P.-Y., Cartron J.-P., Bailly P. 1998; Characterization of the gene encoding the human Kidd blood group/urea transporter protein. J Biol Chem 273:12973–12980 [CrossRef]
    [Google Scholar]
81. Luschnig C., Gaxiola R. A., Grisafi P., Fink G. R. 1998; EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187 [CrossRef]
    [Google Scholar]
82. McCammon M. T., Dowds C. A., Orth K., Moomaw C. R., Slaughter C. A., Goodman J. M. 1990; Sorting of peroxisomal membrane protein PMP47 from Candida boidinii into peroxisomal membranes of Saccharomyces cerevisiae. J Biol Chem 265:20098–20105
    [Google Scholar]
83. McIntire S. L., Reimer R. J., Schuske K., Edwards R. H., Jorgensen E. M. 1997; Identification and characterization of the vesicular GABA transporter. Nature 389:870–876 [CrossRef]
    [Google Scholar]
84. Mastroberardino L., Spindler B., Pfeiffer R., Skelly P. J., Loffing J., Shoemaker C. B., Verrey F. 1998; Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature 395:288–291 [CrossRef]
    [Google Scholar]
85. Maurel C., Reizer J., Schroeder J. I., Chrispeels M. J. 1993; The vacuolar membrane protein gamma-TIP creates water-specific channels in Xenopus oocytes. EMBO J 12:2241–2247
    [Google Scholar]
86. Maurel C., Reizer J., Schroeder J. I., Chrispeels M. J., Saier M. H. Jr 1994; Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J Biol Chem 269:11869–11872
    [Google Scholar]
87. Miyamoto K.-I., Shiraga T., Morita K.7 other authors 1996; Sequence, tissue distribution and developmental changes in rat intestinal oligopeptide transporter. Biochim Biophys Acta 1305:34–38 [CrossRef]
    [Google Scholar]
88. Ogawa W., Kim Y. M., Mizushima T., Tsuchiya T. 1998; Cloning and expression of the gene for the Na⁺-coupled serine transporter from Escherichia coli, and characteristics of the transporter. J Bacteriol 180:6749–6752
    [Google Scholar]
89. Olives B., Neau P., Bailly P., Hediger M. A., Rousselet G., Cartron J. P., Ripoche P. 1994; Cloning and functional expression of a urea transporter from human bone marrow cells. J Biol Chem 269:31649–31652
    [Google Scholar]
90. Palacı́n M., Estévez R., Bertran J., Zorzano A. 1998; Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 78:969–1054
    [Google Scholar]
91. Palmieri F. 1994; Mitochondrial carrier proteins. FEBS Lett 346:48–54 [CrossRef]
    [Google Scholar]
92. Palmieri L., Lasorsa F. M., De Palma A., Palmieri F., Runswick M. J., Walker J. E. 1997; Identification of the yeast ACR1 gene product as a succinate-fumarate transporter essential for growth on ethanol or acetate. FEBS Lett 417:114–118 [CrossRef]
    [Google Scholar]
93. Palmieri L., Vozza A., Hönlinger A., Dietmeier K., Palmisano A., Zara V., Palmieri F. 1999; The mitochondrial dicarboxylate carrier is essential for the growth of Saccharomyces cerevisiae on ethanol or acetate as the sole carbon source. Mol Microbiol 31:569–577 [CrossRef]
    [Google Scholar]
94. Pao S. S., Paulsen I. T., Saier M. H. Jr 1998; The major facilitator superfamily. Microbiol Mol Biol Rev 62:1–32
    [Google Scholar]
95. Park J. H., Saier M. H. Jr 1996; Phylogenetic characterization of the MIP family of transmembrane channel proteins. J Membr Biol 153:171–180 [CrossRef]
    [Google Scholar]
96. Park J. T., Raychaudhuri D., Li H., Normark S., Mengin-Lecreulx D. 1998; MppA, a periplasmic binding protein essential for import of the bacterial cell wall peptide l-alanyl-γ-d-glutamyl-meso-diaminopimelate. J Bacteriol 180:1215–1223
    [Google Scholar]
97. Paulsen I. T., Skurray R. A. 1994; The POT family of transport proteins. Trends Biochem Sci 18:404
    [Google Scholar]
98. Paulsen I. T., Sliwinski M. K., Saier M. H. Jr 1998a; Microbial genome analyses: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J Mol Biol 277:573–592 [CrossRef]
    [Google Scholar]
99. Paulsen I. T., Sliwinski M. K., Nelissen B., Goffeau A., Saier M. H. Jr 1998b; Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett 430:116–125 [CrossRef]
    [Google Scholar]
100. Peter H., Weil B., Burkovski A., Krämer R., Morbach S. 1998; Corynebacterium glutamicum is equipped with four secondary carriers for compatible solutes: identification, sequencing, and characterization of the proline/ectoine uptake system, ProP, and the ectoine/proline/glycine betaine carrier, EctP. J Bacteriol 180:6005–6012
     [Google Scholar]
101. Prasad P. D., Wang H., Kekuda R., Fujita T., Fei Y.-J., Devoe L. D., Leibach F. H., Ganapathy V. 1998; Cloning and functional expression of a cDNA encoding a mammalian sodium-dependent vitamin transporter mediating the uptake of pantothenate, biotin, and lipoate. J Biol Chem 273:7501–7506 [CrossRef]
     [Google Scholar]
102. Rabus R., Jack D. L., Kelly D. J., Saier M. H. Jr 1999; TRAP transporters: an ancient family of extracytoplasmic solute receptor-dependent secondary active transporters. Microbiology 145:3431–3445
     [Google Scholar]
103. Reizer J., Finley K., Kakuda D., MacLeod C. L., Reizer A., Saier M. H. Jr 1993a; Mammalian integral membrane receptors are homologous to facilitators and antiporters of yeast, fungi, and eubacteria. Protein Sci 2:20–30
     [Google Scholar]
104. Reizer J., Reizer A., Saier M. H. Jr 1993b; The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution and proposed functional differentiation of the two repeated halves of the proteins. Crit Rev Biochem Mol Biol 28:235–257 [CrossRef]
     [Google Scholar]
105. Reizer J., Michotey V., Reizer A., Saier M. H. Jr 1994; Novel phosphotransferase system genes revealed by bacterial genome analysis: unique, putative fructose- and glucoside-specific systems. Protein Sci 3:440–450
     [Google Scholar]
106. Reizer J., Charbit A., Reizer A., Saier M. H. Jr 1996; Novel phosphotransferase system genes revealed by bacterial genome analysis: operons encoding homologues of sugar-specific permease domains of the phosphotransferase system and pentose catabolic enzymes. Genome Sci Tech 1:53–75 [CrossRef]
     [Google Scholar]
107. Rentsch D., Hirner B., Schmeizer E., Frommer W. B. 1996; Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446 [CrossRef]
     [Google Scholar]
108. Reverchon S., Nasser W., Robert-Baudouy J. 1994; pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi. Mol Microbiol 11:1127–1139 [CrossRef]
     [Google Scholar]
109. 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
     [Google Scholar]
110. Saier M. H. Jr 1996; Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb Comp Genomics 1:129–150
     [Google Scholar]
111. Saier M. H. Jr 1998; Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. In Advances in Microbial Physiology pp. 81–136Edited by Poole R. K. San Diego, CA: Academic Press;
     [Google Scholar]
112. Saier M. H. Jr 1999a; Classification of transmembrane transport systems in living organisms. In Biomembrane Transport pp. 265–276Edited by Van Winkle L. San Diego, CA: Academic Press;
     [Google Scholar]
113. Saier M. H. Jr 1999b; Eukaryotic transmembrane solute transport systems. In International Review of Cytology: a Survey of Cell Biology pp. 61–136Edited by Jeon K. W. San Diego, CA: Academic Press;
     [Google Scholar]
114. Saier M. H. Jr 1999c; Genome archeology leading to the characterization and classification of transport proteins. Curr Opin Microbiol 2:555–561 [CrossRef]
     [Google Scholar]
115. Saier M. H. Jr, Tseng T.-T. 1999; Evolutionary origins of transmembrane transport systems. In Transport of Molecules Across Microbial MembranesSymposium no. 58 Society for General Microbiology; pp. 252–274Edited by Broome-Smith J. K., Baumberg S., Stirling C. J., Ward F. B. Cambridge: Cambridge University Press;
     [Google Scholar]
116. Saier M. H. Jr, Müller M., Werner P. K. 1989; Insertion of proteins into bacterial membranes: mechanism, characteristics, and comparisons with the eucaryotic process. Microbiol Rev 53:333–336
     [Google Scholar]
117. Saier M. H. Jr, Eng B. H., Fard S.15 other authors 1999a; Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta 1422:1–56 [CrossRef]
     [Google Scholar]
118. Saier M. H. Jr, Beatty J. T., Goffeau A.11 other authors 1999b; The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279
     [Google Scholar]
119. Salomón R. A., Farı́as R. N. 1995; The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J Bacteriol 177:3323–3325
     [Google Scholar]
120. Sanchez J. C., Gimenez R., Schneider A., Fessner W. D., Baldoma L., Aguilar J., Badia J. 1994; Activation of a cryptic gene encoding a kinase for l-xylulose opens a new pathway for the utilisation of l-lyxose by Escherichia coli. J Biol Chem 269:29665–29669
     [Google Scholar]
121. Sanders J. W., Leenhouts K., Burghoorn J., Brands J. R., Venema G., Kok J. 1998; A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol 27:299–310 [CrossRef]
     [Google Scholar]
122. Saraste M., Walker J. E. 1982; Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Lett 144:250–254 [CrossRef]
     [Google Scholar]
123. Sarker R. I., Ogawa W., Shimamoto T., Shimamoto T., Tsuchiya T. 1997; Primary structure and properties of the Na⁺/glucose symporter (SglS) of Vibrio parahaemolyticus. J Bacteriol 179:1805–1808
     [Google Scholar]
124. Sarsero J. P., Pittard A. J. 1995; Membrane topology analysis of Escherichia coli K-12 Mtr permease by alkaline phosphatase and β-galactosidase fusions. J Bacteriol 177:297–306
     [Google Scholar]
125. Sarsero J. P., Wookey P. J., Gollnick P., Yanofsky C., Pittard A. J. 1991; A new family of integral membrane proteins involved in transport of aromatic amino acids in Escherichia coli. J Bacteriol 173:3231–3234
     [Google Scholar]
126. Sato H., Tamba M., Ishii T., Bannai S. 1999; Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274:11455–11458 [CrossRef]
     [Google Scholar]
127. Saurin W., Hofnung M., Dassa E. 1999; Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol 48:22–41 [CrossRef]
     [Google Scholar]
128. Schroers A., Burkovski A., Wohlrab H., Krämer R. 1998; The phosphate carrier from yeast mitochondria: dimerization is a prerequisite for function. J Biol Chem 273:14269–14276 [CrossRef]
     [Google Scholar]
129. Shao Z-Q., Lin R. T., Newman E. B. 1994; Sequencing and characterization of the sdaC gene and identification of the sdaCB operon in Escherichia coli K-12. Eur J Biochem 222:901–907 [CrossRef]
     [Google Scholar]
130. Shayakul C., Steel A., Hediger M. A. 1996; Molecular cloning and characterization of the vasopressin-regulated urea transporter of rat kidney collecting ducts. J Clin Invest 98:2580–2587 [CrossRef]
     [Google Scholar]
131. Shukla V. K., Chrispeels M. J. 1998; Aquaporins: their role and regulation in cellular water movement. In NATO-ASI Series, subseries H: Cellular Integration of Signalling Pathways in Plant Development pp. 11–22Edited by Schavio F. L.others New York: Springer;
     [Google Scholar]
132. Six S., Andrews S. C., Unden G., Guest J. R. 1994; Escherichia coli possesses two homologous anaerobic C₄-dicarboxylate membrane transporters (DcuA and DcuB) distinct from the aerobic dicarboxylate transport system (Dct). J Bacteriol 176:6470–6478
     [Google Scholar]
133. Slotboom D. J., Konings W. N., Lolkema J. S. 1999; Structural features of the glutamate transporter family. Microbiol Mol Biol Rev 63:293–307
     [Google Scholar]
134. Sophianopoulou V., Diallinas G. 1995; Amino acid transporters of lower eukaryotes: regulation, structure and topogenesis. FEMS Microbiol Rev 16:53–75 [CrossRef]
     [Google Scholar]
135. Steiner H.-Y., Song W., Zhang L., Naider F., Becker J. M., Stacey G. 1994; An Arabidopsis peptide transporter is a member of a new class of membrane transport proteins. Plant Cell 6:1289–1299 [CrossRef]
     [Google Scholar]
136. Steiner H.-Y., Naider F., Becker J. M. 1995; The PTR family: a new group of peptide transporters. Mol Microbiol 16:825–834 [CrossRef]
     [Google Scholar]
137. Stephens R. S., Kalman S., Lammel C. J., Fan R., Marathe J., Aravind L. 1998; Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754–759 [CrossRef]
     [Google Scholar]
138. Stucky K., Hagting A., Klein J. R., Matern H., Henrich B., Konings W. N., Plapp R. 1995; Cloning and characterization of brnQ, a gene encoding a low-affinity, branched-chain amino acid carrier in Lactobacillus delbruckii subsp. lactis DSM 7290. Mol Gen Genet 249:682–690 [CrossRef]
     [Google Scholar]
139. Sullivan T. D., Strelow L. I., Illingworth C. A., Phillips R. L., Nelson O. E. Jr 1991; Analysis of the maize brittle-1 alleles and a defective suppressor-mutator induced mutable allele. Plant Cell 3:1337–1348 [CrossRef]
     [Google Scholar]
140. Swift S., Throup J. P., Williams P., Salmond G. P. C., Stewart G. S. A. B. 1996; Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem Sci 21:214–219 [CrossRef]
     [Google Scholar]
141. Tauch A., Hermann T., Burkovski A., Krämer R., Pühler A., Kalinowski J. 1998; Isoleucine uptake in Corynebacterium glutamicum ATCC 13032 is directed by the brnQ gene product. Arch Microbiol 169:303–312 [CrossRef]
     [Google Scholar]
142. Tsay Y.-F., Schroeder J. I., Feldmann K. A., Crawford N. M. 1993; The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713 [CrossRef]
     [Google Scholar]
143. Turk E., Wright E. M. 1997; Membrane topology motifs in the SGLT cotransporter family. J Membr Biol 159:1–20 [CrossRef]
     [Google Scholar]
144. Tzagoloff A., Jang J., Glerum D. M., Wu M. 1996; FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J Biol Chem 271:7392–7397 [CrossRef]
     [Google Scholar]
145. Unden G., Bongaerts J. 1997; Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217–234 [CrossRef]
     [Google Scholar]
146. Verrey F., Jack D. L., Paulsen I. T., Saier M. H. Jr, Pfeiffer R. 1999; New glycoprotein-associated amino acid transporters. J Membr Biol 172:181–192 [CrossRef]
     [Google Scholar]
147. Vrljic M., Sahm H., Eggeling L. 1996; A new type of transporter with a new type of cellular function: l-lysine export from Corynebacterium glutamicum. Mol Microbiol 22:815–826 [CrossRef]
     [Google Scholar]
148. Vrljic M., Garg J., Bellman A.7 other authors 1999; The LysE superfamily: topology of the lysine exporter LysE of Corynebacterium glutamicum, a paradigm for a novel superfamily of transmembrane solute translocators. J Mol Microbiol Biotechnol 1:327–336
     [Google Scholar]
149. Walker J. E., Runswick M. J. 1993; The mitochondrial transport protein superfamily. J Bioenerg Biomembr 25:435–446 [CrossRef]
     [Google Scholar]
150. Walshaw D. L., Poole P. S. 1996; The general l-amino acid permease of Rhizobium leguminosarum is an ABC uptake system that also influences efflux of solutes. Mol Microbiol 21:1239–1252 [CrossRef]
     [Google Scholar]
151. Walshaw D. L., Lowthorpe S., East A., Poole P. S. 1997; Distribution of a sub-class of bacterial ABC polar amino acid transporter and identification of an N-terminal region involved in solute specificity. FEBS Lett 414:397–401 [CrossRef]
     [Google Scholar]
152. West I. C. 1997; Ligand conduction and the gated-pore mechanism of transmembrane transport. Biochim Biophys Acta 1331:213–234 [CrossRef]
     [Google Scholar]
153. Wookey P. J., Pittard A. J. 1988; DNA sequence of the gene (tyrP) encoding the tyrosine-specific transport system of Escherichia coli. J Bacteriol 170:4946–4949
     [Google Scholar]
154. Yang B., Verkman A. S. 1998; Urea transporter UT3 functions as an efficient water channel. J Bacteriol 272:9369–9372
     [Google Scholar]
155. Young G. B., Jack D. L., Smith D. W., Saier M. H. Jr 1999; The amino acid/auxin:proton symport permease family. Biochim Biophys Acta 1415:306–322 [CrossRef]
     [Google Scholar]
156. Zakataeva N. P., Aleshin V. V., Tokmakova I. L., Troshin P. V., Livshits V. A. 1999; The novel transmembrane Escherichia coli proteins involved in amino acid efflux. FEBS Lett 452:228–232 [CrossRef]
     [Google Scholar]
157. Zarbiv R., Grunewald M., Kavanaugh M. P., Kanner B. I. 1998; Cysteine scanning of the surroundings of an alkali-ion binding site of the glutamate transporter GLT-1 reveals a conformationally sensitive residue. J Biol Chem 273:14231–14237 [CrossRef]
     [Google Scholar]
158. Zhou J. J., Theodoulou F. L., Muldin I., Ingemarsson B., Miller A. J. 1998; Cloning and functional characterization of a Brassica napus transporter that is able to transport nitrate and histidine. J Biol Chem 273:12017–12023 [CrossRef]
     [Google Scholar]