Insights into transport mechanism from LeuT engineered to transport tryptophan

EMBO Journal

Volumn 31, Issue 1, 2012, Pages 228-235

  Piscitelli, Chayne L ^a,b   Gouaux, Eric ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

crystallography; LeuT; mechanism; transporter; tryptophan

Indexed keywords

COTRANSPORTER; LEUT PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ARTICLE; BINDING SITE; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; LEUCINE; MOLECULAR SEQUENCE DATA; PLASMA MEMBRANE NEUROTRANSMITTER TRANSPORT PROTEINS; PROTEIN ENGINEERING; SEQUENCE ALIGNMENT; TRYPTOPHAN;

BACTERIA (MICROORGANISMS);

EID: 84855351908     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.353     Document Type: Article

References (45)

1. Abramson J, Wright EM (2009) Structure and function of Na(f)-symporters with inverted repeats. Curr Opin Struct Biol 19: 425-432
2. Adams PD, Grosse-Kunstleve RW, Hung LW, Loerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D 58: 1948-1954 (Pubitemid 35337293)
3. Amara SG, Kuhar MJ (1993) Neurotransmitter transporters: recent progress. Annu Rev Neurosci 16: 73-93 (Pubitemid 23074001)
4. Andersen J, Kristensen AS, Bang-Andersen B, Stromgaard K (2009) Recent advances in the understanding of the interaction of antidepressant drugs with serotonin and norepinephrine transporters. Chem Commun (Camb) 3677-3692
5. Androutsellis-Theotokis A, Goldberg NR, Ueda K, Beppu T, Beckman ML, Das S, Javitch JA, Rudnick G (2003) Characterization of a functional bacterial homologue of sodium-dependent neurotransmitter transporters. J Biol Chem 278: 12703-12709 (Pubitemid 36800031)
6. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201 (Pubitemid 43205406)
7. Asquith RS, Rivett DE (1971) Studies on the photooxidation of tryptophan. Biochim Biophys Acta 252: 111-116
8. Beuming T, Shi L, Javitch JA, Weinstein H (2006) A comprehensive structure-based alignment of prokaryotic and eukaryotic neuro-transmitter/Na+ symporters (NSS) aids in the use of the LeuT structure to probe NSS structure and function. Mol Pharmacol 70: 1630-1642
9. Celik L, Schiott B, Tajkhorshid E (2008) Substrate binding and formation of an occluded state in the leucine transporter. Biophys J 94: 1600-1612
10. Claxton DP, Quick M, Shi L, de Carvalho FD, Weinstein H, Javitch JA, McHaourab HS (2010) Ion/substrate-dependent conforma-tional dynamics of a bacterial homolog of neurotransmitter:so-dium symporters. Nat Struct Mol Biol 17: 822-829
11. Collaborative Computational Project N (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763
12. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WBr, Snoeyink J, Richardson JS, Richardson DC (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383
13. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132 (Pubitemid 41742764)
14. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics, Chapter 5, Unit 5 6
15. Faham S, Watanabe A, Besserer GM, Cascio D, Specht A, Hirayama BA, Wright EM, Abramson J (2008) The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321: 810-814
16. Forrest LR, Kramer R, Ziegler C (2010) The structural basis of secondary active transport mechanisms. Biochim Biophys Acta 1807: 167-188
17. Forrest LR, Zhang YW, Jacobs MT, Gesmonde J, Xie L, Honig BH, Rudnick G (2008) Mechanism for alternating access in neuro-transmitter transporters. Proc Natl Acad Sci USA 105 : 10338-10343
18. Iversen LL (1971) Role of transmitter uptake mechanisms in synap-tic neurotransmission. Br J Pharmacol 41 : 571-591
19. Kaplan RS, Pedersen PL (1985) Determination of microgram quantities of protein in the presence of milligram levels of lipid with amido black 10B. Anal Biochem 150: 97-104 (Pubitemid 16258402)
20. Kerwin BA, Remmele Jr RL (2007) Protect from light: photodegra-dation and protein biologics. J Pharm Sci 96: 1468-1479 (Pubitemid 46953763)
21. Kniazeff J, Shi L, Loland CJ, Javitch JA, Weinstein H, Gether U (2008) An intracellular interaction network regulates conforma-tional transitions in the dopamine transporter. J Biol Chem 283: 17691-17701
22. Krishnamurthy H, Piscitelli CL, Gouaux E (2009) Unlocking the molecular secrets of sodium-coupled transporters. Nature 459: 347-355
23. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macro-molecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255 (Pubitemid 27235885)
24. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326 (Pubitemid 27085611)
25. Perez C, Koshy C, Ressl S, Nicklisch S, Kramer R, Ziegler C (2011) Substrate specificity and ion coupling in the Na+/betaine sym-porter BetP. EMBO J 30: 1221-1229
26. Piscitelli CL, Krishnamurthy H, Gouaux E (2010) Neurotransmitter/sodium symporter orthologue LeuT has a single high-affinity substrate site. Nature 468: 1129-1132
27. Quick M, Winther AM, Shi L, Nissen P, Weinstein H, Javitch JA (2009) Binding of an octyl glucoside molecule in the second substrate (S2) site of LeuT establishes an inhibitor-bound con formation. Proc Natl Acad Sci USA 106: 5563-5568
28. Ressl S, Terwisscha van Scheltinga AC, Vonrhein C, Ott V, Ziegler C (2009) Molecular basis of transport and regulation in the Na(f)/betaine symporter BetP. Nature 458: 47-52
29. Rudnick G, Clark J (1993) From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochim Biophys Acta 1144: 249-263 (Pubitemid 23290252)
30. Shaikh SA, Tajkhorshid E (2010) Modeling and dynamics of the inward-facing state of a Na+/Cl-dependent neurotransmitter transporter homologue. PLoS Comput Biol 6: e1000905
31. Shi L, Quick M, Zhao Y, Weinstein H, Javitch JA (2008) The mechanism of a neurotransmitter:sodium symporter-inward re-lease of Na+ and substrate is triggered by substrate in a second binding site. Mol Cell 30: 667-677 (Pubitemid 351815131)
32. Shimamura T, Weyand S, Beckstein O, Rutherford NG, Hadden JM, Sharples D, Sansom MS, Iwata S, Henderson PJ, Cameron AD (2010) Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1. Science 328: 470-473
33. Singh SK, Piscitelli CL, Yamashita A, Gouaux E (2008) A competitive inhibitor traps LeuT in an open-to-out conformation. Science 322: 1655-1661
34. Singh SK, Yamashita A, Gouaux E (2007) Antidepressant binding site in a bacterial homologue of neurotransmitter transporters. Nature 448: 952-956 (Pubitemid 47312772)
35. Vagin AA, Steiner RA, Lebedev AA, Potterton L, McNicholas S, Long F, Murshudov GN (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr D Biol Crystallogr 60: 2184-2195 (Pubitemid 41742770)
36. Vagin AA, Teplayakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30: 1022-1025
37. Watanabe A, Choe S, Chaptal V, Rosenberg JM, Wright EM, Grabe M, Abramson J (2010) The mechanism of sodium and substrate release from the binding pocket of vSGLT. Nature 468: 988-991
38. Weyand S, Shimamura T, Beckstein O, Sansom MS, Iwata S, Henderson PJ, Cameron AD (2010) The alternating access mechanism of transport as observed in the sodium-hydantoin transporter Mhp1. J Synchrotron Radiat 18: 20-23
39. Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O'Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PC, Iwata S, Henderson PJ, Cameron AD (2008) Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322: 709-713
40. Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E (2005) Crystal structure of a bacterial homologue of Na+/Cl-dependent neuro-transmitter transporters. Nature 437: 215-223 (Pubitemid 41294479)
41. Zahniser NR, Doolen S (2001) Chronic and acute regulation of Na+/Cl-dependent neurotransmitter transporters: drugs, substrates, presynaptic receptors, and signaling systems. Pharmacol Ther 92: 21-55 (Pubitemid 34032021)
42. Zhao Y, Terry D, Shi L, Weinstein H, Blanchard SC, Javitch JA (2010) Single-molecule dynamics of gating in a neurotransmitter transporter homologue. Nature 465: 188-193
43. Zhao Y, Terry DS, Shi L, Quick M, Weinstein H, Blanchard SC, Javitch JA (2011) Substrate-modulated gating dynamics in a Na+-coupled neurotransmitter transporter homologue. Nature 474: 109-113
44. Zhou Z, Zhen J, Karpowich NK, Goetz RM, Law CJ, Reith ME, Wang DN (2007) LeuT-desipramine structure reveals how antidepressants block neurotransmitter reuptake. Science 317: 1390-1393 (Pubitemid 47417479)
45. Zhou Z, Zhen J, Karpowich NK, Law CJ, Reith ME, Wang DN (2009) Antidepressant specificity of serotonin transporter suggested by three LeuT-SSRI structures. Nat Struct Mol Biol 16: 652-657