The structural basis of secondary active transport mechanisms

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 2, 2011, Pages 167-188

  Forrest, Lucy R ^a   Krämer, Reinhard ^b   Ziegler, Christine ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Carrier; Coupling; Modeling; Protein conformation; Protein structure; Secondary active transport

Indexed keywords

CARRIER PROTEIN;

ARTICLE; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; ELECTROCHEMISTRY; MEMBRANE TRANSPORT; MOLECULAR MECHANICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SOLUTE;

BIOLOGICAL TRANSPORT, ACTIVE; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTONS;

EID: 78650297251     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.10.014     Document Type: Review

References (166)

1. W.F. Widdas Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer J. Physiol. 118 1952 23 39
2. P. Mitchell A general theory of membrane transport from studies of bacteria Nature 180 1957 134 136
3. O. Jardetzky Simple allosteric model for membrane pumps Nature 211 1966 969 970
4. G.A. Vidaver Inhibition of parallel flux and augmentation of counter flux shown by transport models not involving a mobile carrier J. Theor. Biol. 10 1966 301 306
5. C.S. Patlak Contributions to the theory of active transport: II. The gate type non-carrier mechanism and generalizations concerning tracer flow, efficiency, and measurement of energy expenditure Bull. Math. Biophys. 19 1957 209 235
6. W.D. Stein, and B. Honig Models for the active transport of cations..the steady-state analysis Mol. Cell. Biochem. 15 1977 27 44
7. M. Klingenberg A.N. Martonosi, The enzymes of biological membranes: membrane transport vol. 3 1976 Plenum Publ. Corp. New York 383 438
8. W.D. Stein Transport and diffusion across cell membranes 1986 Academic Press Orlando, Fl
9. R.M. Krupka Role of substrate binding forces in exchange-only transport systems: II. Implications for the mechanism of the anion exchanger of red cells J. Membr. Biol. 109 1989 159 171
10. I.C. West Ligand conduction and the gated-pore mechanism of transmembrane transport Biochim. Biophys. Acta 1331 1997 213 234
11. R.M. Krupka Coupling mechanisms in active transport Biochim. Biophys. Acta 1183 1993 105 113
12. A.R. Fersht Enzyme structure and mechanism 1977 Freeman San Francisco
13. W.P. Jencks The utilization of binding energy in coupled vectorial processes Adv. Enzymol. Relat. Areas Mol. Biol. 51 1980 75 106
14. M. Klingenberg Ligand-protein interaction in biomembrane carriers. The induced transition fit of transport catalysis Biochemistry 44 2005 8563 8570
15. M. Klingenberg Transport catalysis Biochim. Biophys. Acta 1757 2006 1229 1236
16. W.P. Jencks Utilization of binding energy and coupling rules for active transport and other coupled vectorial processes Methods Enzymol. 171 1989 145 164
17. C.J. Law, P.C. Maloney, and D.N. Wang Ins and outs of major facilitator superfamily antiporters Annu. Rev. Microbiol. 62 2008 289 305
18. H. Krishnamurthy, C.L. Piscitelli, and E. Gouaux Unlocking the molecular secrets of sodium-coupled transporters Nature 459 2009 347 355
19. L.R. Forrest, and G. Rudnick The rocking bundle: a mechanism for ion-coupled solute flux by symmetrical transporters Physiology 24 2009 377 386
20. +-symporters with inverted repeats Curr. Opin. Struct. Biol. 19 2009 425 432
21. T. Shimamura, S. Weyand, O. Beckstein, N.G. Rutherford, J.M. Hadden, D. Sharples, M.S.P. Sansom, S. Iwata, P.J.F. Henderson, and A.D. Cameron Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1 Science 328 2010 470 473
22. O. Boudker, and G. Verdon Structural perspectives on secondary active transporters Trends Pharm. Sci. 31 2010 418 426
23. C. Tanford Mechanism of free energy coupling in active transport Annu. Rev. Biochem. 52 1983 379 409
24. M. Klingenberg The ADP, ATP shuttle of the mitochondrion Trends Biochem. Sci. 4 1979 249 252
25. B. Hille Ion channels of excitable membranes 3rd. ed 2001 Sinauer Ass
26. R.M. Krupka Expression of substrate specificity in facilitated transport systems J. Membr. Biol. 117 1990 69 78
27. E. Gouaux The molecular logic of sodium-coupled neurotransmitter transporters Philos. T R Soc. B 364 2009 149 154
28. L. Guan, and H.R. Kaback Lessons from lactose permease Annu. Rev. Bioph. Biom. 35 2006 67 91
29. M. Sobczak, and J.S. Lolkema Structural and mechanistic diversity of secondary transporters Curr. Opin. Microbiol. 8 2005 161 167
30. E. Padan, L. Kozachkov, K. Herz, and A. Rimon NhaA crystal structure: functional-structural insights J. Exp. Biol. 212 2009 1593 1603
31. H. Nury, C. Dahout-Gonzalez, V. Trezeguet, G.J.M. Lauquin, G. Brandolin, and E. Pebay-Peyroula Relations between structure and function of the mitochondrial ADP/ATP carrier Annu. Rev. Biochem. 75 2006 713 741 (Pubitemid 44118050)
32. E. Pebay-Peyroula, and G. Brandolin Nucleotide exchange in mitochondria: insight at a molecular level Curr. Opin. Struct. Biol. 14 2004 420 425
33. M.J. Lemieux, Y.F. Huang, and D.N. Wang The structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily Curr. Opin. Struct. Biol. 14 2004 405 412
34. J. Abramson, S. Iwata, and H.R. Kaback Lactose permease as a paradigm for membrane transport proteins Mol. Membr. Biol. 21 2004 227 236
35. W. Busch, and M.H. Saier The transporter classification (TC) system Crit. Rev. Biochem. Mol. 37 2002 287 337
36. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trezeguet, G.J.M. Lauquin, and R. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
37. E.R. Kunji, and P.G. Crichton Mitochondrial carriers function as monomers Biochim. Biophys. Acta BBA Bioenerg. 1797 2010 817 831
38. M. Klingenberg Wanderings in bioenergetics and biomembranes Biochim. Biophys. Acta BBA Bioenerg. 1797 2010 579 594
39. H. Nury, C. Dahout-Gonzalez, V. Trezeguet, G. Lauquin, G. Brandolin, and E. Pebay-Peyroula Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers FEBS Lett. 579 2005 6031 6036
40. D.R. Nelson, C.M. Felix, and J.M. Swanson Highly conserved charge-pair networks in the mitochondrial carrier family J. Mol. Biol. 277 1998 285 308
41. A.J. Robinson, C. Overy, and E.R.S. Kunji The mechanism of transport by mitochondrial carriers based on analysis of symmetry Proc. Natl Acad. Sci. USA 105 2008 17766 17771
42. E.R.S. Kunji, and A.J. Robinson The conserved substrate binding site of mitochondrial carriers Biochim. Biophys. Acta BBA Bioenerg. 1757 2006 1237 1248
43. Y. Wang, and E. Tajkhorshid Electrostatic funneling of substrate in mitochondrial inner membrane carriers Proc. Natl Acad. Sci. USA 105 2008 9598 9603
44. A.J. Robinson, and E.R.S. Kunji Mitochondrial carriers in the cytoplasmic state have a common substrate binding site Proc. Natl Acad. Sci. USA 103 2006 2617 2622
45. W.W. Cleland Kinetics of enzyme-catalyzed reactions with 2 or more substrates or products Biochim. Biophys. Acta BBA Bioenerg. 67 1963 104 137
46. F. Palmieri Mitochondrial carrier proteins FEBS Lett. 346 1994 48 54
47. F. Dehez, E. Pebay-Peyroula, and C. Chipot Binding of ADP in the mitochondrial ADP/ATP carrier is driven by an electrostatic funnel J. Am. Chem. Soc. 130 2008 12725 12733
48. S.S. Pao, I.T. Paulsen, and M.H. Saier Jr. Major Facilitator Superfamily Microbiol. Mol. Biol. Rev. 62 1998 1 34
49. Y. Huang, M.J. Lemieux, J. Song, M. Auer, and D.-N. Wang Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli Science 301 2003 616 620
50. Y. Yin, X. He, P. Szewczyk, T. Nguyen, and G. Chang Structure of the multidrug transporter EmrD from Escherichia coli Science 312 2006 741 744
51. J. Abramson, I. Smirnova, V. Kasho, G. Verner, H.R. Kaback, and S. Iwata Structure and mechanism of the lactose permease of Escherichia coli Science 301 2003 610 615
52. L. Guan, O. Mirza, G. Verner, S. Iwata, and H.R. Kaback Structural determination of wild-type lactose permease Proc. Natl. Acad. Sci. USA 104 2007 15294 15298
53. + symport in LacY EMBO J. 25 2006 1177 1183
54. S. Dang, L. Sun, Y. Huang, F. Lu, Y. Liu, H. Gong, J. Wang, and N. Yan Structure of a fucose transporter in an outward-open conformation Nature 467 2010 734 738
55. W. Nie, F.E. Sabetfard, and H.R. Kaback The Cys154 - > Gly mutation in LacY causes constitutive opening of the hydrophilic periplasmic pathway J. Mol. Biol. 379 2008 695 703
56. I.N. Smirnova, and H.R. Kaback A mutation in the lactose permease of Escherichia coli that decreases conformational flexibility and increases protein stability Biochemistry 42 2003 3025 3031
57. Y. Yin, M.Ø. Jensen, E. Tajkhorshid, and K. Schulten Sugar binding and protein conformational changes in lactose permease Biophys. J. 91 2006 3972 3985
58. J.B. Klauda, and B.R. Brooks Sugar binding in lactose permease: anomeric state of a disaccharide influences binding structure J. Mol. Biol. 367 2007 1523 1534
59. J. Holyoake, and M.S.P. Sansom Conformational change in an MFS protein: MD simulations of LacY Structure 15 2007 873 884
60. T. Hirai, and S. Subramaniam Structure and transport mechanism of the bacterial oxalate transporter OxlT Biophys. J. 87 2004 3600 3607
61. Y.L. Nie, and H.R. Kaback Sugar binding induces the same global conformational change in purified LacY as in the native bacterial membrane Proc. Natl Acad. Sci. USA 107 2010 9903 9908
62. Y.G. Zhou, Y.L. Nie, and H.R. Kaback Residues gating the periplasmic pathway of LacY J. Mol. Biol. 394 2009 219 225
63. Y. Nie, Y.G. Zhou, and H.R. Kaback Clogging the periplasmic pathway in LacY Biochemistry 48 2009 738 743
64. Z.Y. Liu, M.G. Madej, and H.R. Kaback Helix dynamics in LacY: helices II and IV J. Mol. Biol. 396 2010 617 626
65. Y. Nie, N. Ermolova, and H.R. Kaback Site-directed alkylation of LacY: effect of the proton electrochemical gradient J. Mol. Biol. 374 2007 356 364
66. H.R. Kaback, R. Dunten, S. Frillingos, P. Venkatesan, I. Kwaw, W. Zhang, and N. Ermolova Site-directed alkylation and the alternating access model for LacY Proc. Natl Acad. Sci. USA 104 2007 491 494
67. D.S. Majumdar, I. Smirnova, V. Kasho, E. Nir, X.X. Kong, S. Weiss, and H.R. Kaback Single-molecule FRET reveals sugar-induced conformational dynamics in LacY Proc. Natl Acad. Sci. USA 104 2007 12640 12645
68. I.N. Smirnova, V.N. Kasho, and H.R. Kaback Direct sugar binding to LacY measured by resonance energy transfer Biochemistry 45 2006 15279 15287
69. I. Smirnova, V. Kasho, J.Y. Choe, C. Altenbach, W.L. Hubbell, and H.R. Kaback Sugar binding induces an outward facing conformation of LacY Proc. Natl Acad. Sci. USA 104 2007 16504 16509
70. I. Smirnova, V. Kasho, J. Sugihara, and H.R. Kaback Probing of the rates of alternating access in LacY with Trp fluorescence Proc. Natl Acad. Sci. USA 106 2009 21561 21566
71. + translocation site define the pKa for sugar binding to LacY Biochemistry 48 2009 8852 8860
72. I.N. Smirnova, V. Kasho, and H.R. Kaback Protonation and sugar binding to LacY Proc. Natl Acad. Sci. USA 105 2008 8896 8901
73. Y. Zhou, L. Guan, J.A. Freites, and H.R. Kaback Opening and closing of the periplasmic gate in lactose permease Proc. Natl Acad. Sci. USA 105 2008 3774 3778
74. G. Enkavi, and E. Tajkhorshid Simulation of spontaneous substrate binding revealing the binding pathway and mechanism and initial conformational response of GlpT Biochemistry 49 2010 1105 1114
75. D. Yernool, O. Boudker, Y. Jin, and E. Gouaux Structure of a glutamate transporter homologue from Pyrococcus horikoshii Nature 431 2004 811 818
76. O. Boudker, R.M. Ryan, D. Yernool, K. Shimamoto, and E. Gouaux Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter Nature 445 2007 387 393
77. N. Reyes, C. Ginter, and O. Boudker Transport mechanism of a bacterial homologue of glutamate transporters Nature 462 2009 880 885
78. T. Crisman, S. Qu, B.I. Kanner, and L.R. Forrest Inward-facing conformation of glutamate transporters as revealed by their inverted-topology structural repeats Proc. Natl Acad. Sci. USA 106 2009 20752 20757
79. I.H. Shrivastava, J. Jiang, S.G. Amara, and I. Bahar Time-resolved mechanism of extracellular gate opening and substrate binding in a glutamate transporter J. Biol. Chem. 283 2008 28680 28690
80. Z. Huang, and E. Tajkhorshid Dynamics of the extracellular gate and ion-substrate coupling in the glutamate transporter Biophys. J. 95 2008 2292 2300
81. H.P. Larsson, A.V. Tzingounis, H.P. Koch, and M.P. Kavanaugh Fluorometric measurements of conformational changes in glutamate transporters Proc. Natl Acad. Sci. USA 101 2004 3951 3956
82. A. Yamashita, S.K. Singh, T. Kawate, Y. Jin, and E. Gouaux Crystal structure of a bacterial homologue of Na+/Cl- dependent neurotransmitter transporters Nature 437 2005 215 223
83. +/sugar symport Science 321 2008 810 814
84. S. Weyand, T. Shimamura, S. Yajima, S.I. Suzuki, O. Mirza, K. Krusong, E.P. Carpenter, N.G. Rutherford, J.M. Hadden, J. O'Reilly, P. Ma, M. Saidijam, S.G. Patching, R.J. Hope, H.T. Norbertczak, P.C.J. Roach, S. Iwata, P.J.F. Henderson, and A.D. Cameron Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter Science 322 2008 709 713
85. +/betaine symporter BetP Nature 458 2009 47 52
86. L. Tang, L. Bai, W.-H. Wang, and T. Jiang Crystal structure of the carnitine transporter and insights into the antiport mechanism Nat. Struct. Mol. Biol. 17 2010 492 496
87. +-independent transport in the carnitine/butyrobetaine antiporter CaiT Nature 467 2010 233 237
88. +-independent amino acid transporter Science 325 2009 1010 1014
89. Y. Fang, H. Jayaram, T. Shane, L. Kolmakova-Partensky, F. Wu, C. Williams, Y. Xiong, and C. Miller Structure of a prokaryotic virtual proton pump at 3.2 Å resolution Nature 460 2009 1040 1043
90. X. Gao, L. Zhou, X. Jiao, F. Lu, C. Yan, X. Zeng, J. Wang, and Y. Shi Mechanism of substrate recognition and transport by an amino acid antiporter Nature 463 2010 828 832
91. E. Screpanti, and C. Hunte Discontinuous membrane helices in transport proteins and their correlation with function J. Struct. Biol. 159 2007 261 267
92. X. Gao, F. Lu, L. Zhou, S. Dang, L. Sun, X. Li, J. Wang, and Y. Shi Structure and mechanism of an amino acid antiporter Science 324 2009 1565 1568
93. S.K. Singh, C.L. Piscitelli, A. Yamashita, and E. Gouaux A competitive inhibitor traps LeuT in an open-to-out conformation Science 322 2008 1655 1661
94. S.K. Singh, A. Yamashita, and E. Gouaux Antidepressant binding site in a bacterial homologue of neurotransmitter transporters Nature 448 2007 952 956
95. M. Quick, A.-M. Lund Winther, L. Shi, P. Nissen, H. Weinstein, and J.A. Javitch Binding of an octylglucoside detergent molecule in the second substrate (S2) site of LeuT establishes an inhibitor-bound conformation Proc. Natl Acad. Sci. USA 106 2009 5563 5568
96. Z. Zhou, J. Zhen, N.K. Karpowich, R.M. Goetz, C.J. Law, M.E.A. Reith, and D.-N. Wang LeuT-desipramine structure reveals how antidepressants block neurotransmitter reuptake Science 317 2007 1390 1393
97. Z. Zhou, J. Zhen, N.K. Karpowich, C.J. Law, M.E.A. Reith, and D.N. Wang Antidepressant specificity of serotonin transporter suggested by three LeuT-SSRI structures Nat. Struct. Mol. Biol. 16 2009 652 U696
98. L. Shi, M. Quick, Y. Zhao, H. Weinstein, and J.A. Javitch The mechanism of a neurotransmitter:sodium symporter-Inward release of Na + and substrate is triggered by substrate in a second binding site Mol. Cell 30 2008 667 677
99. Y. Zhao, D. Terry, L. Shi, H. Weinstein, S.C. Blanchard, and J.A. Javitch Single-molecule dynamics of gating in a neurotransmitter transporter homologue Nature 465 2010 188 193
100. L.R. Forrest, Y.-W. Zhang, M.T. Jacobs, J. Gesmonde, L. Xie, B. Honig, and G. Rudnick A mechanism for alternating access in neurotransmitter transporters Proc. Natl Acad. Sci. USA 105 2008 10338 10343
101. + antiporter Trends Biochem. Sci. 33 2008 435 443
102. + antiporter and insights into mechanism of action and regulation by pH Nature 435 2005 1197 1202
103. + antiporting Science 317 2007 799 803
104. E. Olkhova, E. Padan, and H. Michel The influence of protonation states on the dynamics of the NhaA antiporter from Escherichia coli Biophys. J. 92 2007 3784 3791
105. Y.-J. Chen, O. Pornillos, S. Lieu, C. Ma, A.P. Chen, and G. Chang X-ray structure of EmrE supports dual topology model Proc. Natl Acad. Sci. USA 104 2007 18999 19004
106. S. Schuldiner EmrE, a model for studying evolution and mechanism of ion-coupled transporters Biochim. Biophys. Acta BBA Bioenerg. 1794 2009 748 762
107. S. Schuldiner When biochemistry meets structural biology: the cautionary tale of EmrE Trends Biochem. Sci. 32 2007 252 258
108. I. Ubarretxena-Belandia, J.M. Baldwin, S. Schuldiner, and C.G. Tate Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer EMBO J. 22 2003 6175 6181
109. S.J. Fleishman, S.E. Harrington, A. Enosh, D. Halperin, C.G. Tate, and N. Ben-Tal Quasi-symmetry in the Cryo-EM structure of EmrE provides the key to modeling its transmembrane domain J. Mol. Biol. 364 2006 54 67
110. S. Steiner-Mordoch, M. Soskine, D. Solomon, D. Rotem, A. Gold, M. Yechieli, Y. Adam, and S. Schuldiner Parallel topology of genetically fused EmrE homodimers EMBO J. 27 2008 17 26
111. V. Agarwal, U. Fink, S. Schuldiner, and B. Reif MAS solid-state NMR studies on the multidrug transporter EmrE Biochim. Biophys. Acta BBA Bioenerg. 1768 2007 3036 3043
112. I. Nasie, S. Steiner-Mordoch, A. Gold, and S. Schuldiner Topologically random insertion of EmrE supports a pathway for evolution of inverted repeats in ion-coupled transporters J. Biol. Chem. 285 2010 15234 15244
113. T. Eicher, L. Brandstatter, and K.M. Pos Structural and functional aspects of the multidrug efflux pump AcrB Biol. Chem. 390 2009 693 699
114. K.M. Pos Drug transport mechanism of the AcrB efflux pump Biochim. Biophys. Acta BBA Bioenerg. 1794 2009 782 793
115. S. Murakami Multidrug efflux transporter, AcrB-the pumping mechanism Curr. Opin. Struct. Biol. 18 2008 459 465
116. M.A. Seeger, A. Schiefner, T. Eicher, F. Verrey, K. Diederichs, and K.M. Pos Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism Science 313 2006 1295 1298
117. S. Murakami, R. Nakashima, E. Yamashita, T. Matsumoto, and A. Yamaguchi Crystal structures of a multidrug transporter reveal a functionally rotating mechanism Nature 443 2006 173 179
118. - channels Nature 427 2004 803 807 (Pubitemid 38297735)
119. C. Miller CIC chloride channels viewed through a transporter lens Nature 440 2006 484 489
120. R. Dutzler, E.B. Campbell, M. Cadene, B.T. Chait, and R. MacKinnon X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity Nature 415 2002 287 294
121. + exchanger Philos. T R Soc. B 364 2009 175 180
122. -/H+ exchanger Proc. Natl Acad. Sci. USA 105 2008 11194 11199
123. R. Kramer, and M. Klingenberg Electrophoretic control of reconstituted adenine nucleotide translocation Biochemistry 21 1982 1082 1089
124. B. Poolman Precursor/product antiport in bacteria Mol. Microbiol. 4 1990 1629 1636
125. G.F. LeFevre, and G.F. McGinnis Tracer exchange vs. net uptake of glucose through human red cell surface. New evidence for carrier-mediated diffusion J. Gen. Physiol. 1960 87 103
126. +/glucose cotransporter Annu. Rev. Physiol. 55 1993 575 589
127. +/glucose cotransporter: I. Voltage-clamp studies J. Membr. Biol. 125 1992 49 62
128. M. Sahin-Tóth, A. Karlin, and H.R. Kaback Unraveling the mechanism of the lactose permease of Escherichia coli Proc. Natl Acad. Sci. USA 97 2000 10729 10732
129. H.R. Kaback, M. Sahin-Toth, and A.B. Weinglass The kamikaze approach to membrane transport Nat. Rev. Mol. Cell Biol. 2 2001 610 620
130. S.C. King, and T.H. Wilson Towards an understanding of the structural basis of 'forbidden' transport pathways in the Escherichia coli lactose carrier: mutations probing the energy barriers to uncoupled transport Mol. Microbiol. 4 1990 1433 1438
131. R.J. Brooker An analysis of lactose permease "sugar specificity" mutations which also affect the coupling between proton and lactose transport. I. Val177 and Val177/Asn319 permeases facilitate proton uniport and sugar uniport J. Biol. Chem. 266 1991 4131 4138
132. J.S. Lolkema, and B. Poolman Uncoupling in secondary transport proteins. A mechanistic explanation for mutants of lac permease with an uncoupled phenotype J. Biol. Chem. 270 1995 12670 12676
133. +/lactose coupling by ionic interactions in the lactose permease of Escherichia coli J. Membr. Biol. 198 2004 135 146
134. G.J. Kaczorowski, and H.R. Kaback Mechanism of lactose translocation in membrane vesicles from Escherichia coli. 1. Effect of pH on efflux, exchange, and counterflow Biochemistry 18 1979 3691 3697
135. + Biochemistry 18 1979 3697 3704
136. D.E. Robertson, G.J. Kaczorowski, M.L. Garcia, and H.R. Kaback Active transport in membrane vesicles from Escherichia coli: the electrochemical proton gradient alters the distribution of the lac carrier between two different kinetic states Biochemistry 19 1980 5692 5702
137. J.J. Garcia-Celma, J. Ploch, I. Smirnova, H.R. Kaback, and K. Fendler Delineating electrogenic reactions during lactose/H(+) symport Biochemistry 49 2010 6115 6121
138. J.J. Garcia-Celma, I.N. Smirnova, H.R. Kaback, and K. Fendler Electrophysiological characterization of LacY Proc. Natl Acad. Sci. USA 106 2009 7373 7378
139. M. Klingenberg Transport viewed as a catalytic process Biochimie 89 2007 1042 1048
140. Y. Zhou, E. Zomot, and B.I. Kanner Identification of a lithium interaction site in the γ-aminobutyric acid (GABA) transporter GAT-1 J. Biol. Chem. 281 2006 22092 22099
141. K.M.Y. Penado, G. Rudnick, and M.M. Stephan Critical amino acid residues in transmembrane span 7 of the serotonin transporter identified by random mutagenesis J. Biol. Chem. 273 1998 28098 28106
142. S.A. Mari, A. Soragna, M. Castagna, E. Bossi, A. Peres, and V.F. Sacchi Aspartate 338 contributes to the cationic specificity and to driver-amino acid coupling in the insect cotransporter KAAT1 Cell. Mol. Life Sci. 61 2004 243 256
143. S. Mager, N. Kleinberger-Doron, G.I. Keshet, N. Davidson, B.I. Kanner, and H.A. Lester Ion binding and permeation at the GABA transporter GAT1 J. Neurosci. 16 1996 5405 5414
144. + binding sites with two different mechanisms J. Mol. Biol. 377 2008 804 818
145. +-dependent leucine transporter LeuT Biophys. J. 95 2008 4613 4621
146. L. Celik, B. Schiott, and E. Tajkhorshid Substrate binding and formation of an occluded state in the leucine transporter Biophys. J. 94 2007 1600 1612
147. + dependence and are critical for transport activity J. Biol. Chem. 282 2007 25290 25298
148. Y. Zhou, E.R. Bennett, and B.I. Kanner The aqueous accessibility in the external half of transmembrane domain I of the GABA transporter GAT-1 is modulated by its ligands J. Biol. Chem. 279 2004 13800 13808
149. J. Li, and E. Tajkhorshid Ion-releasing state of a secondary membrane transporter Biophys. J. 97 2009 L29 L31
150. L.R. Forrest, S. Tavoulari, Y.-W. Zhang, G. Rudnick, and B. Honig Identification of a chloride ion binding site in Na+/Cl- dependent transporters Proc. Natl Acad. Sci. USA 104 2007 12761 12766
151. E. Zomot, A. Bendahan, M. Quick, Y. Zhao, J.A. Javitch, and B.I. Kanner Mechanism of chloride interaction with neurotransmitter:sodium symporters Nature 449 2007 726 730
152. Z. Tao, A. Gameiro, and C. Grewer Thallium ions can replace both sodium and potassium ions in the glutamate transporter Excitatory Amino Acid Carrier 1 Biochemistry 47 2008 12923 12930
153. S. Teichman, S. Qu, and B.I. Kanner The equivalent of a thallium binding residue from an archeal homolog controls cation interactions in brain glutamate transporters Proc. Natl Acad. Sci. USA 106 2009 14297 14302
154. H.P. Larsson, X. Wang, B. Lev, I. Baconguis, D.A. Caplan, N.P. Vyleta, H.P. Koch, A. Diez-Sampedro, and S.Y. Noskov Evidence for a third sodium-binding site in glutamate transporters suggests an ion-substrate coupling model Proc. Natl Acad. Sci. USA 107 2010 13912 13917
155. Z. Tao, N. Rosental, B.I. Kanner, A. Gameiro, J. Mwaura, and C. Grewer Mechanism of cation binding to the glutamate transporter EAAC1 probed with mutation of the conserved amino acid residue T101 J. Biol. Chem. 285 2010 17725 17733
156. D.C. Holley, and M.P. Kavanaugh Interactions of alkali cations with glutamate transporters Philos. T R Soc. B 364 2009 155 161
157. + site and the sequence of extracellular binding events in the glutamate transporter Biophys. J. 99 2010 1416 1425
158. D. Menaker, A. Bendahan, and B.I. Kanner The substrate specificity of a neuronal glutamate transporter is determined by the nature of the coupling ion J. Neurochem. 99 2006 20 28
159. J.I. Wadiche, and M.P. Kavanaugh Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel J. Neurosci. 18 1998 7650 7661
160. N. Watzke, E. Bamberg, and C. Grewer Early intermediates in the transport cycle of the neuronal excitatory amino acid carrier EAAC1 J. Gen. Physiol. 117 2001 547 562
161. P.J. Franco, and R.J. Brooker Functional roles of Glu-269 and Glu-325 within the lactose permease of Escherichia coli J. Biol. Chem. 269 1994 7379 7386
162. M.L. Ujwal, M. Sahin-Toth, B. Persson, and H.R. Kaback Role of glutamate-269 in the lactose permease of Escherichia coli Mol. Membr. Biol. 11 1994 9 16
163. + antiporter Biophys. J. 97 2009 121 131
164. + exchanger J. Gen. Physiol. 133 2009 131 138
165. M.J. Roux, and S. Supplisson Neuronal and glial glycine transporters have different stoichiometries Neuron 25 2000 373 383
166. S. Murakami, R. Nakashima, E. Yamashita, and A. Yamaguchi Crystal structure of bacterial multidrug efflux transporter AcrB Nature 419 2002 587 593