Induced fit substrate binding to an archeal glutamate transporter homologue

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 30, 2013, Pages 12486-12491

  Ewers, David ^a   Becher, Toni ^a   Machtens, Jan Philipp ^a,b   Weyand, Ingo ^b   Fahlke, Christoph ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Sodium coupled transport; Stopped flow; Uptake

Indexed keywords

AMINO ACID; ASPARTIC ACID; GLUTAMATE TRANSPORTER; SODIUM ION; TRYPTOPHAN;

ARTICLE; CROSS LINKING; FLUORESCENCE; KINETICS; MICELLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

SODIUM-COUPLED TRANSPORT; STOPPED FLOW; UPTAKE;

AMINO ACID TRANSPORT SYSTEM X-AG; ARCHAEA; ISOMERISM; MODELS, MOLECULAR; SPECTROMETRY, FLUORESCENCE; SUBSTRATE SPECIFICITY;

EID: 84880653278     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300772110     Document Type: Article

References (32)

1. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65(1):1-105.
2. Boudker O, Ryan RM, Yernool D, Shimamoto K, Gouaux E (2007) Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445(7126):387-393.
3. Jardetzky O (1966) Simple allosteric model for membrane pumps. Nature 211(5052): 969-970.
4. Klingenberg M (1979) The ADP,ATP shuttle of the mitochondrion. Trends Biochem Sci 4(7):249-252.
5. Reyes N, Ginter C, Boudker O (2009) Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462(7275):880-885.
6. Crisman TJ, Qu S, Kanner BI, Forrest LR (2009) Inward-facing conformation of glutamate transporters as revealed by their inverted-topology structural repeats. Proc Natl Acad Sci USA 106(49):20752-20757.
7. Koshland DE (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44(2):98-104.
8. Klingenberg M (2005) Ligand-protein interaction in biomembrane carriers. The induced transition fit of transport catalysis. Biochemistry 44(24):8563-8570.
9. Mirza O, Guan L, Verner G, Iwata S, Kaback HR (2006) Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J 25(6):1177-1183.
10. Loo TW, Bartlett MC, Clarke DM (2003) Substrate-induced conformational changes in the transmembrane segments of human P-glycoprotein. Direct evidence for the substrate-induced fit mechanism for drug binding. J Biol Chem 278(16):13603-13606.
11. Johnson KA (2008) Role of induced fit in enzyme specificity: A molecular forward/reverse switch. J Biol Chem 283(39):26297-26301.
12. Lakowicz J (2006) Principles of Fluorescence Spectroscopy (Springer US, Boston).
13. Groeneveld M, Slotboom DJ (2010) Na+:aspartate coupling stoichiometry in the glutamate transporter homologue GltPh. Biochemistry 49(17):3511-3513.
14. Fersht AR (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (Freeman, New York).
15. Tsai CJ, Kumar S, Ma B, Nussinov R (1999) Folding funnels, binding funnels, and protein function. Protein Sci 8(6):1181-1190.
16. Strickland S, Palmer G, Massey V (1975) Determination of dissociation constants and specific rate constants of enzyme-substrate (or protein-ligand) interactions from rapid reaction kinetic data. J Biol Chem 250(11):4048-4052.
17. Vogt AD, Di Cera E (2012) Conformational selection or induced fit? A critical appraisal of the kinetic mechanism. Biochemistry 51(30):5894-5902.
18. Ryan RM, Compton ELR, Mindell JA (2009) Functional characterization of a Na+-dependent aspartate transporter from Pyrococcus horikoshii. J Biol Chem 284(26): 17540-17548.
19. Georgieva ER, Borbat PP, Ginter C, Freed JH, Boudker O (2013) Conformational ensemble of the sodium-coupled aspartate transporter. Nat Struct Mol Biol 20(2): 215-221.
20. Hänelt I, Wunnicke D, Bordignon E, Steinhoff HJ, Slotboom DJ (2013) Conformational heterogeneity of the aspartate transporter GltPh. Nat Struct Mol Biol 20(2):210-214.
21. Compton ELR, Taylor EM, Mindell JA (2010) The 3-4 loop of an archaeal glutamate transporter homolog experiences ligand-induced structural changes and is essential for transport. Proc Natl Acad Sci USA 107(29):12840-12845.
22. Jiang J, Shrivastava IH, Watts SD, Bahar I, Amara SG (2011) Large collective motions regulate the functional properties of glutamate transporter trimers. Proc Natl Acad Sci USA 108(37):15141-15146.
23. Shrivastava IH, Jiang J, Amara SG, Bahar I (2008) Time-resolved mechanism of extracellular gate opening and substrate binding in a glutamate transporter. J Biol Chem 283(42):28680-28690.
24. Reyes N, Oh S, Boudker O (2013) Binding thermodynamics of a glutamate transporter homolog. Nat Struct Mol Biol 20(5):634-640.
25. Mim C, Tao Z, Grewer C (2007) Two conformational changes are associated with glutamate translocation by the glutamate transporter EAAC1. Biochemistry 46(31): 9007-9018.
26. Wadiche JI, Kavanaugh MP (1998) Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J Neurosci 18(19):7650-7661.
27. Watzke N, Bamberg E, Grewer C (2001) Early intermediates in the transport cycle of the neuronal excitatory amino acid carrier EAAC1. J Gen Physiol 117(6):547-562.
28. Mim C, Balani P, Rauen T, Grewer C (2005) The glutamate transporter subtypes EAAT4 and EAATs 1-3 transport glutamate with dramatically different kinetics and voltage dependence but share a common uptake mechanism. J Gen Physiol 126(6): 571-589.
29. Bergles DE, Tzingounis AV, Jahr CE (2002) Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters. J Neurosci 22(23):10153-10162.
30. Grewer C, Watzke N, Wiessner M, Rauen T (2000) Glutamate translocation of the neuronal glutamate transporter EAAC1 occurs within milliseconds. Proc Natl Acad Sci USA 97(17):9706-9711.
31. Focke PJ, Moenne-Loccoz P, Larsson HP (2011) Opposite movement of the external gate of a glutamate transporter homolog upon binding cotransported sodium compared with substrate. J Neurosci 31(16):6255-6262.
32. Yernool D, Boudker O, Folta-Stogniew E, Gouaux E (2003) Trimeric subunit stoichiometry of the glutamate transporters from Bacillus caldotenax and Bacillus stearothermophilus. Biochemistry 42(44):12981-12988.