Unlocking the molecular secrets of sodium-coupled transporters

Nature

Volumn 459, Issue 7245, 2009, Pages 347-355

  Krishnamurthy, Harini ^a   Piscitelli, Chayne L ^a   Gouaux, Eric ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOMIPRAMINE; DESIPRAMINE; GLUCOSE TRANSPORTER; IMIPRAMINE; LEUCINE; SCAFFOLD PROTEIN; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM ION; TRICYCLIC ANTIDEPRESSANT AGENT;

CELL ORGANELLE; DISEASE TREATMENT; MOLECULAR ANALYSIS;

BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; COMPETITIVE INHIBITION; CONFORMATIONAL TRANSITION; CONSERVATION BIOLOGY; CRYSTAL STRUCTURE; ENERGY; ENZYME SUBSTRATE; ESCHERICHIA COLI; HYDROGEN BOND; ISOMERIZATION; LIGAND BINDING; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; NONHUMAN; ORTHOLOGY; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; REVIEW; SODIUM TRANSPORT; SOLUTE;

ANIMALS; BINDING SITES; HUMANS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; SODIUM;

EID: 66249098083     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08143     Document Type: Review

References (67)

1. Quick, M. W. (ed.) Transmembrane Transporters (Wiley-Liss, 2002).
2. Roux, M. J. & Supplisson, S. Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383 (2000).
3. Chakrabarti, A. C. & Deamer, D. W. Permeability of lipid bilayers to amino acids and phosphate. Biochim. Biophys. Acta 1111, 171-177 (1992).
4. Supplisson, S. & Roux, M. J. Why glycine transporters have different stoichiometries. FEBS Lett. 529, 93-101 (2002).
5. Sobczak, I. & Lolkema, J. S. Structural and mechanistic diversity of secondary transporters. Curr. Opin. Microbiol. 8, 161-167 (2005).
6. Wright, E. M. & Turk, E. The sodium/glucose cotransport family SLC5. Pflügers Arch. 447, 510-518 (2004).
7. Hebert, S. C., Mount, D. B. & Gamba, G. Molecular physiology of cation-coupled Cl-cotransport: the SLC12 family. Pflügers Arch. 447, 580-593 (2004).
8. Sonders, M. S., Quick, M. & Javitch, J. A. How did the neurotransmitter cross the bilayer? A closer view. Curr. Opin. Neurobiol. 15, 296-304 (2005).
9. Gamba, G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev. 85, 423-493 (2005).
10. Murphy, D. L., Lerner, A., Rudnick, G. & Lesch, K. P. Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Mol. Interv. 4, 109-123 (2004).
11. Busch, W. & Saier, M. H. Jr The transporter classification (TC) system, 2002. Crit. Rev. Biochem. Mol. Biol. 37, 287-337 (2002).
12. Hediger, M. A. et al. The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins. Pflügers Arch. 447, 465-468 (2004).
13. Saier, M. H. Jr A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354-411 (2000).
14. Saier, M. H. Jr, Tran, C. V. & Barabote, R. D. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 34, D181-D186 (2006).
15. Mitchell, P. A general theory of membrane transport from studies of bacteria. Nature 180, 134-136 (1957).
16. Mitchell, P. in Advances in Enzymology and Related Areas of Molecular Biology (ed. Nord, F. F.) 33-87 (Interscience, 1967).
17. Patlak, C. S. 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, 209-235 (1957).
18. Vidaver, G. A. Inhibition of parallel flux and augmentation of counter flux shown by transport models not involving a mobile carrier. J. Theor. Biol. 10, 301-306 (1966).
19. Jardetzky, O. Simple allosteric model for membrane pumps. Nature 211, 969-970 (1966).
20. Murakami, S., Nakashima, R., Yamashita, E. & Yamaguchi, A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419, 587-593 (2002).
21. Huang, Y., Lemieux, M. J., Song, J., Auer, M. & Wang, D. N. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301, 616-620 (2003).
22. Abramson, J. et al. Structure and mechanism of the lactose permease of Escherichia coli. Science 301, 610-615 (2003).
23. Yernool, D., Boudker, O., Jin, Y. & Gouaux, E. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818 (2004).
24. + antiporter and insights into mechanism of action and regulation by pH. Nature 435, 1197-1202 (2005).
25. Yamashita, A., Singh, S. K., Kawate, T. , Jin, Y. & Gouaux, E. Crystal structure of a bacterial homologue of Na+/C l--dependent neurotransmitter transporters. Nature 437, 215-223 (2005).
26. Screpanti, E. & Hunte, C. Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261-267 (2007).
27. Faham, S. et al. The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321, 810-814 (2008).
28. Weyand, S. et al. Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322, 709-713 (2008).
29. +-glucose cotransporters: SLC5. Physiology 19, 370-376 (2004).
30. Chen, N. H., Reith, M. E. & Quick, M. W. Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflügers Arch. 447, 519-531 (2004).
31. Barker, E. L., Moore, K. R., Rakhshan, F. & Blakely, R. D. Transmembrane domain I contributes to the permeation pathway for serotonin and ions in the serotonin transporter. J. Neurosci. 19, 4705-4717 (1999).
32. Rudnick, G. Serotonin transporters - structure and function. J. Membr. Biol. 213, 101-110 (2006).
33. Kanner, B. I. & Zomot, E. Sodium-coupled neurotransmitter transporters. Chem. Rev. 108, 1654-1668 (2008).
34. Ben-Yona, A. & Kanner, B. I. Transmembrane domain 8 of the γ-aminobutyric acid transporter GAT-1 lines a cytoplasmic accessibility pathway into its binding pocket. J. Biol. Chem. 284, 9727-9732 (2009).
35. Slotboom, D. J., Lolkema, J. S. & Konings, W. N. Membrane topology of the C-terminal half of the neuronal, glial, and bacterial glutamate transporter family. J. Biol. Chem. 271, 31317-31321 (1996).
36. Grunewald, M., Bendahan, A. & Kanner, B. I. Biotinylation of single cysteine mutants of the glutamate transporter GLT-1 from rat brain reveals its unusual topology. Neuron 21, 623-632 (1998).
37. Seal, R. P. & Amara, S. G. A reentrant loop domain in the glutamate carrier EAAT1 participates in substrate binding and translocation. Neuron 21, 1487-1498 (1998).
38. Toyoshima, C., Nakasako, M., Nomura, H. & Ogawa, H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405, 647-655 (2000).
39. Dutzler, R., Campbell, E. B., Cadene, M., Chait, B. T. & MacKinnon, R. X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature 415, 287-294 (2002).
40. Singh, S. K., Piscitelli, C. L., Yamashita, A. & Gouaux, E. A competitive inhibitor traps LeuT in an open-to-out conformation. Science 322, 1655-1661 (2008).
41. Shi, L., Quick, M., Zhao, Y., Weinstein, H. & Javitch, J. A. The mechanism of a neurotransmitter:sodium symporter-inward release of Na+ and substrate is triggered by a substrate in a second binding site. Mol. Cell 30, 667-677 (2008).
42. Celik, L., Schiott, B. & Tajkhorshid, E. Substrate binding and formation of an occluded state in the leucine transporter. Biophys. J. 94, 1600-1612 (2008).
43. +/proline transporter PutP of Escherichia coli in ligand binding and transport. J. Biol. Chem. 283, 4921-4929 (2008).
44. - symporter play a role in its Na+ dependence and are critical for transport activity. J. Biol. Chem. 282, 25290-25298 (2007).
45. Zhou, Y., Zomot, E. & Kanner, B. I. Identification of a lithium interaction site in the GABA transporter GAT-1. J. Biol. Chem. 281, 22092-22099 (2006).
46. + binding sites with two different mechanisms. J. Mol. Biol. 377, 804-818 (2008).
47. +-dependent leucine transporter LeuT. Biophys. J. 95, 4613-4621 (2008).
48. Talvenheimo, J., Fishkes, H., Nelson, P. J. & Rudnick, G. The serotonin transporter-imipramine "receptor". J. Biol. Chem. 258, 6115-6119 (1983).
49. Gu, H. H., Wall, S. & Rudnick, G. Ion coupling stoichiometry for the norepinephrine transporter in membrane vesicles from stably transfected cells. J. Biol. Chem. 271, 6911- 6916 (1996).
50. Keynan, S. & Kanner, B. I. γ-Aminobutyric acid transport in reconstituted preparations from rat brain: coupled sodium and chloride fluxes. Biochemistry 27, 12-17 (1988).
51. +-to-sugar stoichiometry of SGLT3. Am. J. Physiol. Renal Physiol. 280, F278-F282 (2001).
52. +/glucose cotransporter (SGLT1) currents and fluxes. J. Membr. Biol. 162, 101-106 (1998).
53. Eskandari, S. et al. Thyroid Na+/I- symporter. Mechanism, stoichiometry, and specificity. J. Biol. Chem. 272, 27230-27238 (1997).
54. Forrest, L. R., Tavoulari, S., Zhang, Y. W., Rudnick, G. & Honig, G. Identification of a chloride ion binding site in Na+/C l- -dependent transporters. Proc. Natl Acad. Sci. USA 104, 12761-12766 (2007).
55. Zomot, E. et al. Mechanism of chloride interaction with neurotransmitter:sodium symporters. Nature 449, 726-730 (2007).
56. Singh, S., Yamashita, A. & Gouaux, E. Antidepressant binding site in a bacterial homologue of neurotransmitter transporters. Nature 448, 952-956 (2007).
57. Boudker, O., Ryan, R., Yernool, D., Shimamoto, K. & Gouaux, E. Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445, 387-393 (2007).
58. Kavanaugh, M. P., Bendahan, A., Zerangue, N., Zhang, Y. & Kanner, B. I. Mutation of an amino acid residue influencing potassium coupling in the glutamate transporter GLT-1 induces obligate exchange. J. Biol. Chem. 272, 1703-1708 (1997).
59. Keyes, S. R. & Rudnick, G. Coupling of transmembrane proton gradients to platelet serotonin transport. J. Biol. Chem. 257, 1172-1176 (1982).
60. Forrest, L. R. et al. Mechanism for alternating access in neurotransmitter transporters. Proc. Natl Acad. Sci. USA 105, 10338-10343 (2008).
61. Jacobs, M. T., Zhang, Y. W., Campbell, S. D. & Rudnick, G. Ibogaine, a noncompetitive inhibitor of serotonin transport, acts by stabilizing the cytoplasm-facing state of the transporter. J. Biol. Chem. 282, 29441-29447 (2007).
62. Zhang, Y.-W. & Rudnick, G. The cytoplasmic substrate permeation pathway of serotonin transporter. J. Biol. Chem. 281, 36213-36220 (2006).
63. Zhang, Y. W. & Rudnick, G. Cysteine-scanning mutagenesis of serotonin transporter intracellular loop 2 suggests an α-helical conformation. J. Biol. Chem. 280, 30807-30813 (2005).
64. Zhou, Z. et al. LeuT-desipramine structure reveals how antidepressants block neurotransmitter uptake. Science 317, 1390-1393 (2007).
65. Apparsundaram, S., Stockdale, D. J., Henningsen, R. A., Milla, M. E. & Martin, R. S. Antidepressants targeting the serotonin reuptake transporter act via a competitive mechanism. J. Pharmacol. Exp. Ther. 327, 982-990 (2008).
66. Hirayama, B. A., Diez-Sampedro, A. & Wright, E. M. Common mechanisms of inhibition for the Na+/glucose (hSGLT1) and Na+/C l-/GABA (hGAT1) cotransporters. Br. J. Pharmacol. 134, 484-495 (2001).
67. Hayward, S. & Berendsen, H. J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30, 144-154 (1998).