Structure, function and evolution of solute transporters in prokaryotes and eukaryotes.

In both prokaryotes and eukaryotes, transport systems of organic solutes can be classified as passive transporters, such as channels and facilitated transporters, and active transporters, which utilize diverse energy-coupling mechanisms. In the past decade, our understanding of the biochemistry and molecular biology of transporters from Escherichia coli has progressed significantly, whereas the analysis of mammalian transporters has initially been limited by the ability to purify membrane proteins. The recent development of methods to detect the activity of recombinant proteins in individual cells, however, has led to the cloning of several novel mammalian transporter cDNAs. One of the most useful expression cloning systems is Xenopus oocytes in conjunction with uptake studies and electrophysiological experiments. Overall, the sequence information and the functional data derived from many transporters has revealed unifying designs, similar energy-coupling mechanisms and common evolutionary origins. Here, I will provide a general survey of the known transport systems in bacteria, yeast, plants, insects and vertebrates and illustrate the different types of transport systems in mammals by discussing transporters recently studied in our laboratory.

[1]  H. Nikaido,et al.  Prevention of drug access to bacterial targets: permeability barriers and active efflux. , 1994, Science.

[2]  H. Nikaido,et al.  Lipopolysaccharide structure required for in vitro trimerization of Escherichia coli OmpF porin , 1991, Journal of bacteriology.

[3]  R. Robey,et al.  Cloning of a Na(+)- and Cl(-)-dependent betaine transporter that is regulated by hypertonicity. , 1992, The Journal of biological chemistry.

[4]  D. Eisenberg,et al.  A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter , 1992, Cell.

[5]  P. Overvoorde,et al.  Topographical analysis of the plasma membrane-associated sucrose binding protein from soybean. , 1994, The Journal of biological chemistry.

[6]  S. Udenfriend,et al.  Expression cloning of a Na(+)-independent neutral amino acid transporter from rat kidney. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Sauer,et al.  The hexose carrier from Chlorella , 1989, FEBS letters.

[8]  Yoshikatsu Kanai,et al.  The elusive transporters with a high affinity for glutamate , 1993, Trends in Neurosciences.

[9]  P. Dawson,et al.  Expression cloning and characterization of the hamster ileal sodium-dependent bile acid transporter. , 1994, The Journal of biological chemistry.

[10]  M. Hediger,et al.  Cloning and characterization of an extracellular Ca2+-sensing receptor from bovine parathyroid , 1993, Nature.

[11]  J. Ferretti,et al.  A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. , 1992, The Journal of biological chemistry.

[12]  S. Weremowicz,et al.  Assignment of the gene coding for the human high-affinity glutamate transporter EAAC1 to 9p24: potential role in dicarboxylic aminoaciduria and neurodegenerative disorders. , 1994, Genomics.

[13]  S. Jackowski,et al.  Cloning, sequence, and expression of the pantothenate permease (panF) gene of Escherichia coli , 1990, Journal of bacteriology.

[14]  Y. Hirata,et al.  Cloning and expression of apical membrane water channel of rat kidney collecting tubule , 1993, Nature.

[15]  R. Star,et al.  The vasopressin-regulated urea transporter in renal inner medullary collecting duct. , 1990, The American journal of physiology.

[16]  J. Pandit,et al.  Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein with and without a ligand. , 1994, The Journal of biological chemistry.

[17]  A. Driessen,et al.  Energy transduction and transport processes in thermophilic bacteria , 1992, Journal of bioenergetics and biomembranes.

[18]  L. Reuss,et al.  Relationships between rhodamine 123 transport, cell volume, and ion-channel function of P-glycoprotein. , 1994, The Journal of biological chemistry.

[19]  N. Nelson,et al.  Cloning and expression of a cDNA encoding the transporter of taurine and beta-alanine in mouse brain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Blakely,et al.  Cloning and expression of a functional serotonin transporter from rat brain , 1991, Nature.

[21]  E. Seeberg,et al.  Cloning and expression of a rat brain L-glutamate transporter , 1992, Nature.

[22]  P. Agre,et al.  Aquaporin CHIP: the archetypal molecular water channel. , 1993, The American journal of physiology.

[23]  Klein THE INSECT V-ATPase, A PLASMA MEMBRANE PROTON PUMP ENERGIZING SECONDARY ACTIVE TRANSPORT: IMMUNOLOGICAL EVIDENCE FOR THE OCCURRENCE OF A V-ATPase IN INSECT ION-TRANSPORTING EPITHELIA. , 1992, The Journal of experimental biology.

[24]  Peter Agre,et al.  Appearance of Water Channels in Xenopus Oocytes Expressing Red Cell CHIP28 Protein , 1992, Science.

[25]  B. Kanner Sodium-coupled neurotransmitter transport: structure, function and regulation. , 1994, The Journal of experimental biology.

[26]  J. Hanrahan,et al.  The molecular basis of chloride transport in shark rectal gland. , 1994, The Journal of experimental biology.

[27]  G. Uhl,et al.  Cloning and expression of a cocaine-sensitive dopamine transporter complementary DNA. , 1991, Science.

[28]  M. Hediger,et al.  Cloning and characterization of the vasopressin-regulated urea transporter , 1993, Nature.

[29]  J. McNamara,et al.  Cloning and expression of a novel Na(+)-dependent neutral amino acid transporter structurally related to mammalian Na+/glutamate cotransporters. , 1993, The Journal of biological chemistry.

[30]  D. Bedwell,et al.  A mitochondrial porin cDNA predicts the existence of multiple human porins. , 1993, The Journal of biological chemistry.

[31]  M. Palacín,et al.  Expression cloning of a cDNA from rabbit kidney cortex that induces a single transport system for cystine and dibasic and neutral amino acids. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[32]  H. Betz,et al.  Primary structure and functional expression of a choline transporter expressed in the rat nervous system , 1992, FEBS letters.

[33]  Günter J. Hämmerling,et al.  Selectivity of MHC-encoded peptide transporters from human, mouse and rat , 1994, Nature.

[34]  N. Sauer,et al.  cDNA cloning of a eucaryotic H+-cotransporter , 1989 .

[35]  B. Erni,et al.  The mannose transporter of Escherichia coli. Structure and function of the IIABMan subunit. , 1993, The Journal of biological chemistry.

[36]  A. Pühler,et al.  Identification and sequence analysis of the Rhizobium meliloti dctA gene encoding the C4-dicarboxylate carrier , 1989, Journal of bacteriology.

[37]  V. Franceschi,et al.  A 62-kD sucrose binding protein is expressed and localized in tissues actively engaged in sucrose transport. , 1992, The Plant cell.

[38]  M. Azuma,et al.  K+/H+ antiport in the tobacco hornworm midgut: the K(+)-transporting component of the K+ pump. , 1994, The Journal of experimental biology.

[39]  R. North,et al.  Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. , 1993, The Journal of biological chemistry.

[40]  G. Saidel,et al.  Effects of dietary protein restriction and glucocorticoid administration on urea excretion in rats. , 1975, Kidney international.

[41]  M. Hediger,et al.  A new family of neurotransmitter transporters: the high‐affinity glutamate transporters , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[42]  S. Roseman,et al.  The bacterial phosphoenolpyruvate: glycose phosphotransferase system. , 1990, Annual review of biochemistry.

[43]  T. Mohandas,et al.  Cloning and chromosomal localization of a human kidney cDNA involved in cystine, dibasic, and neutral amino acid transport. , 1993, The Journal of clinical investigation.

[44]  S. Michaelis,et al.  Effects of nucleotide binding fold mutations on STE6, a yeast ABC protein. , 1993, Society of General Physiologists series.

[45]  C. Kong,et al.  Cloning and expression of a mammalian Na+/amino acid cotransporter with sequence similarity to Na+/glucose cotransporters. , 1993, The Journal of biological chemistry.

[46]  M. Esmann,et al.  The Na,K-ATPase , 1992, Journal of bioenergetics and biomembranes.

[47]  H. Nikaido,et al.  Porins and specific diffusion channels in bacterial outer membranes. , 1994, The Journal of biological chemistry.

[48]  D. Bush Proton-Coupled Sugar and Amino Acid Transporters in Plants , 1993 .

[49]  S. Baldwin,et al.  Mammalian and bacterial sugar transport proteins are homologous , 1987, Nature.

[50]  O. Rosen,et al.  Evidence that facilitative glucose transporters may fold as beta-barrels. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[51]  M. Hediger,et al.  Primary structure and functional characterization of a high-affinity glutamate transporter , 1992, Nature.

[52]  Terri L. Gilbert,et al.  The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins , 1993, Neuron.

[53]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[54]  H. Lodish,et al.  Sequence and structure of a human glucose transporter. , 1985, Science.

[55]  M. Hediger,et al.  Cloning of a rat kidney cDNA that stimulates dibasic and neutral amino acid transport and has sequence similarity to glucosidases. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  T. Pourcher,et al.  The melibiose permease of Escherichia coli: importance of the NH2-terminal domains for cation recognition by the Na+/sugar cotransporter. , 1993, Society of General Physiologists series.

[57]  S. Mundlos,et al.  Glucose/galactose malabsorption caused by a defect in the Na+/glucose cotransporter , 1991, Nature.

[58]  J. Weissenbach,et al.  Localization of a gene causing cystinuria to chromosome 2p , 1994, Nature Genetics.

[59]  M. Knepper The aquaporin family of molecular water channels. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[60]  T. Caspari,et al.  Hexose/H+ symporters in lower and higher plants. , 1994, The Journal of experimental biology.

[61]  M. Hediger,et al.  Molecular physiology of sodium-glucose cotransporters. , 1994, Physiological reviews.

[62]  W. Frommer,et al.  Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. , 1992, The EMBO journal.

[63]  Randy D. Blakely,et al.  Expression cloning of a cocaine-and antidepressant-sensitive human noradrenaline transporter , 1991, Nature.

[64]  L. Reuss,et al.  Unidirectional fluxes of rhodamine 123 in multidrug-resistant cells: evidence against direct drug extrusion from the plasma membrane. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[65]  M. Hediger,et al.  The high affinity Na+/glucose cotransporter. Re-evaluation of function and distribution of expression. , 1994, The Journal of biological chemistry.

[66]  V. Sacchi,et al.  Amino acid transport systems in intestinal brush-border membranes from lepidopteran larvae. , 1989, The American journal of physiology.

[67]  J A McCammon,et al.  Hinge-bending in L-arabinose-binding protein. The "Venus's-flytrap" model. , 1982, The Journal of biological chemistry.

[68]  E. Wright,et al.  Cloning of a human kidney cDNA with similarity to the sodium-glucose cotransporter. , 1992, The American journal of physiology.

[69]  T. Branchek,et al.  Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors , 1992, Neuron.

[70]  T. Branchek,et al.  Cloning and expression of a high affinity taurine transporter from rat brain. , 1992, Molecular pharmacology.

[71]  David Attwell,et al.  The glial cell glutamate uptake carrier countertransports pH-changing anions , 1992, Nature.

[72]  R. Edwards The transport of neurotransmitters into synaptic vesicles , 1992, Current Biology.

[73]  E. Lin,et al.  Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli , 1980, Journal of bacteriology.

[74]  H. Lester,et al.  Cloning and expression of a rat brain GABA transporter. , 1990, Science.

[75]  J. Rosenbusch,et al.  Crystallization of porin using short chain phospholipids. , 1989, Journal of molecular biology.

[76]  E. Wright,et al.  Cloning and functional expression of a mammalian Na+/nucleoside cotransporter. A member of the SGLT family. , 1992, The Journal of biological chemistry.

[77]  M. Saier,et al.  Transport proteins in bacteria: common themes in their design. , 1992, Science.

[78]  X. Estivill,et al.  Cystinuria caused by mutations in rBAT, a gene involved in the transport of cystine , 1994, Nature Genetics.

[79]  R. Dalbey Positively charged residues are important determinants of membrane protein topology. , 1990, Trends in biochemical sciences.

[80]  S. Udenfriend,et al.  Characterization of the rat neutral and basic amino acid transporter utilizing anti-peptide antibodies. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[81]  G. W. Frimpter Cystinuria , 1890, The Hospital.

[82]  Y. Anraku,et al.  Molecular cloning of gltS and gltP, which encode glutamate carriers of Escherichia coli B , 1989, Journal of bacteriology.

[83]  N. Tsukagoshi,et al.  cDNA sequence for rkST1, a novel member of the sodium ion-dependent glucose cotransporter family. , 1994, Biochimica et biophysica acta.

[84]  S. Freundlieb,et al.  Facilitated diffusion of p-nitrophenyl-alpha-D-maltohexaoside through the outer membrane of Escherichia coli. Characterization of LamB as a specific and saturable channel for maltooligosaccharides. , 1988, The Journal of biological chemistry.

[85]  P. Meier,et al.  Functional expression cloning and characterization of the hepatocyte Na+/bile acid cotransport system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Y. Anraku,et al.  Nucleotide sequence of gltS, the Na+/glutamate symport carrier gene of Escherichia coli B. , 1990, The Journal of biological chemistry.

[87]  R. Blakely,et al.  Molecular cloning and expression of a high affinity l-proline transporter expressed in putative glutamatergic pathways of rat brain , 1992, Neuron.

[88]  P. Maloney,et al.  The evolution of membrane carriers. , 1993, Society of General Physiologists series.

[89]  B. Hoffman,et al.  Expression cloning of a reserpine-sensitive vesicular monoamine transporter. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[90]  L. Kühn,et al.  Stimulation of system y(+)-like amino acid transport by the heavy chain of human 4F2 surface antigen in Xenopus laevis oocytes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[91]  N. Crawford,et al.  The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter , 1993, Cell.

[92]  M H Saier,et al.  The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships. , 1993, Critical reviews in biochemistry and molecular biology.

[93]  E. Wright,et al.  Expression cloning and cDNA sequencing of the Na+/glucose co-transporter , 1987, Nature.

[94]  D. Bush,et al.  Electrogenicity, pH-Dependence, and Stoichiometry of the Proton-Sucrose Symport. , 1990, Plant physiology.

[95]  A. Bel,et al.  Strategies of Phloem Loading , 1993 .

[96]  M. G. Wolfersberger,et al.  Cation-dependent leucine, alanine, and phenylalanine uptake at pH 10 in brush-border membrane vesicles from larval Manduca sexta midgut. , 1993, Biochimica et biophysica acta.

[97]  H. Nikaido,et al.  Specificity of diffusion channels produced by lambda phage receptor protein of Escherichia coli. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[98]  D. Eisenberg,et al.  Analysis of membrane and surface protein sequences with the hydrophobic moment plot. , 1984, Journal of molecular biology.

[99]  W. Saenger,et al.  Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance. , 1994, Science.

[100]  S. Amara,et al.  Cloning and expression of a cocaine-sensitive rat dopamine transporter. , 1991, Science.

[101]  M. Palacín,et al.  A new family of proteins (rBAT and 4F2hc) involved in cationic and zwitterionic amino acid transport: a tale of two proteins in search of a transport function. , 1994, The Journal of experimental biology.

[102]  B. Poolman,et al.  Revised nucleotide sequence of the gltP gene, which encodes the proton-glutamate-aspartate transport protein of Escherichia coli K-12 , 1992, Journal of bacteriology.

[103]  W. Frommer,et al.  Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. , 1994, The EMBO journal.

[104]  T. Chiou,et al.  Cloning a plant amino acid transporter by functional complementation of a yeast amino acid transport mutant. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[105]  T. Storck,et al.  Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[106]  P. Roepe,et al.  The lac permease of Escherichia coli: site-directed mutagenesis studies on the mechanism of beta-galactoside/H+ symport. , 1990, Research in microbiology.

[107]  K. H. Langer,et al.  Urinary Concentration and Dilution , 1969 .

[108]  D. Housman,et al.  Cloning and characterization of a second member of the mouse mdr gene family , 1988, Molecular and cellular biology.

[109]  M. Knepper,et al.  Concentration dependence of urea and thiourea transport in rat inner medullary collecting duct. , 1990, The American journal of physiology.

[110]  W. S. Lee,et al.  Molecular cloning, primary structure, and characterization of two members of the mammalian electroneutral sodium-(potassium)-chloride cotransporter family expressed in kidney. , 1994, The Journal of biological chemistry.

[111]  G. Rummel,et al.  Crystal structures explain functional properties of two E. coli porins , 1992, Nature.

[112]  M. Hediger,et al.  The human kidney low affinity Na+/glucose cotransporter SGLT2. Delineation of the major renal reabsorptive mechanism for D-glucose. , 1994, The Journal of clinical investigation.

[113]  M. Romero,et al.  Expression cloning of a mammalian proton-coupled oligopeptide transporter , 1994, Nature.

[114]  M. Knepper,et al.  Urea gradient-associated fluid absorption with sigma urea = 1 in rat terminal collecting duct. , 1990, American Journal of Physiology.

[115]  P. Lachmann,et al.  Membrane defence against complement lysis: The structure and biological properties of CD59 , 1993, Immunologic research.

[116]  M. Hediger,et al.  The 4F2 antigen heavy chain induces uptake of neutral and dibasic amino acids in Xenopus oocytes. , 1992, The Journal of biological chemistry.

[117]  A. Yamauchi,et al.  Cloning of the cDNa for a Na+/myo-inositol cotransporter, a hypertonicity stress protein. , 1992, The Journal of biological chemistry.

[118]  M. Hediger,et al.  The neuronal and epithelial human high affinity glutamate transporter. Insights into structure and mechanism of transport. , 1994, The Journal of biological chemistry.

[119]  X. Estivill,et al.  Expression cloning of a human renal cDNA that induces high affinity transport of L-cystine shared with dibasic amino acids in Xenopus oocytes. , 1993, The Journal of biological chemistry.