Substrate-driven conformational changes in ClC-ec1 observed by fluorine NMR

EMBO Journal

Volumn 28, Issue 20, 2009, Pages 3090-3102

  Elvington, Shelley M ^a   Liu, Corey W ^b   Maduke, Merritt C ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ChaNnel; Cl; NMR; Transporter

Indexed keywords

ANTIPORTER; CHLORIDE CHANNEL; FLUORINE; MEMBRANE PROTEIN;

ARTICLE; CELL NUCLEUS; CHROMATOGRAPHY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; FLUORINE NUCLEAR MAGNETIC RESONANCE; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; STOICHIOMETRY;

ANTIPORTERS; CHLORIDE CHANNELS; ESCHERICHIA COLI PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY;

ESCHERICHIA COLI;

EID: 70350304561     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.259     Document Type: Article

References (51)

1. Accardi A, Kolmakova-Partensky L, Williams C, Miller C (2004) Ionic currents mediated by a prokaryotic homologue of CLC Cl- channels. J Gen Physiol 123: 109-119
2. Accardi A, Lobet S, Williams C, Miller C, Dutzler R (2006) Synergism between halide binding and proton transport in a CLC-type exchanger. J Mol Biol 362: 691-699
3. Accardi A, Miller C (2004) Secondary active transport mediated by a prokaryotic homologue of ClC Cl-channels. Nature 427: 803-807 (Pubitemid 38297735)
4. Accardi A, Pusch M (2000) Fast and slow gating relaxations in the muscle chloride channel CLC-1. J Gen Physiol 116: 433-444
5. Accardi A, Walden M, Nguitragool W, Jayaram H, Williams C, Miller C (2005) Separate ion pathways in a cl-/h+ exchanger. J Gen Physiol 126: 563-570
6. Ahmad S, Gromiha M, Fawareh H, Sarai A (2004) ASAView: database and tool for solvent accessibility representation in proteins. BMC Bioinformatics 5: 51
7. Bell SP, Curran PK, Choi S, Mindell JA (2006) Site-directed fluorescence studies of a prokaryotic ClC antiporter. Biochemistry 45: 6773-6782
8. Brahm J (1977) Temperature-dependent changes of chloride transport kinetics in human red cells. J Gen Physiol 70: 283-306
9. Bykova EA, Zhang XD, Chen TY, Zheng J (2006) Large movement in the C terminus of CLC-0 chloride channel during slow gating. Nat Struct Mol Biol 13: 1115-1119
10. Danielson MA, Biemann HP, Koshland Jr DE, Falke JJ (1994) Attractant- and disulfide-induced conformational changes in the ligand binding domain of the chemotaxis aspartate receptor: a 19F NMR study. Biochemistry 33: 6100-6109
11. Danielson MA, Falke JJ (1996) Use of 19F NMR to probe protein structure and conformational changes. Annu Rev Biophys Biomol Struct 25: 163-195
12. DeFelice LJ (2004) Transporter structure and mechanism. Trends Neurosci 27: 352-359
13. Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168: 167
14. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R (2002) X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415: 287-294
15. Dutzler R, Campbell EB, MacKinnon R (2003) Gating the selectivity filter in ClC chloride channels. Science 300: 108-112
16. Elvington SM, Maduke M (2008) Thinking outside the crystal: complementary approaches for examining transporter conformational change. Channels (Austin) 2: 373-379
17. Frieden C, Hoeltzli SD, Bann JG (2004) The preparation of 19F-labeled proteins for NMR studies. Methods Enzymol 380: 400-415
18. Gakh YG, Gakh AA, Gronenborn AM (2000) Fluorine as an NMR probe for structural studies of chemical and biological systems. Magn Reson Chem 38: 551-558
19. Gerig J (1994) Fluorine NMR of proteins. Prog NMR Spectrosc 26: 293-370
20. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450: 964-972
21. Hille B (2001) Ion Channels of Excitable Membranes. Sinauer: Sunderland, MA
22. Hong M (2007) Structure, topology, and dynamics of membrane peptides and proteins from solid-state NMR spectroscopy. J Phys Chem B 111: 10340-10351
23. Hull WE, Sykes BD (1975) Fluorotyrosine alkaline phosphatase: internal mobility of individual tyrosines and the role of chemical shift anisotropy as a 19F nuclear spin relaxation mechanism in proteins. J Mol Biol 98: 121-153
24. Hwang PM, Kay LE (2005) Solution structure and dynamics of integral membrane proteins by NMR: a case study involving the enzyme PagP. Methods Enzymol 394: 335-350
25. Jayaram H, Accardi A, Wu F, Williams C, Miller C (2008) Ion permeation through a Cl-selective channel designed from a CLC Cl-/H+ exchanger. Proc Natl Acad Sci USA 105: 11194-11199
26. Jentsch TJ (2008) CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol Biol 43: 3-36
27. Lisal J, Maduke M (2008) The ClC-0 chloride channel is a ?broken? Cl(-)/H(+) antiporter. Nat Struct Mol Biol 15: 805-810
28. Lobet S, Dutzler R (2006) Ion-binding properties of the ClC chloride selectivity filter. EMBO J 25: 24-33
29. Loewen MC, Klein-Seetharaman J, Getmanova EV, Reeves PJ, Schwalbe H, Khorana HG (2001) Solution 19F nuclear Overhauser effects in structural studies of the cytoplasmic domain of mammalian rhodopsin. Proc Natl Acad Sci USA 98: 4888-4892
30. Luck LA, Falke JJ (1991) Open conformation of a substrate-binding cleft: 19F NMR studies of cleft angle in the D-galactose chemo-sensory receptor. Biochemistry 30: 6484-6490
31. Ludewig U, Jentsch TJ, Pusch M (1997) Inward rectification in ClC-0 chloride channels caused by mutations in several protein regions. J Gen Physiol 11 0 : 165-171
32. Luo W, Mani R, Hong M (2007) Side-chain conformation of the M2 transmembrane peptide proton channel of influenza a virus from 19F solid-state NMR. J Phys Chem B 111 : 10825-10832
33. Matulef K, Maduke M (2007) The CLC ?chloride channel? family: revelations from prokaryotes. Mol Membr Biol 24: 342-350
34. Miller C (1982) Open-state substructure of single chloride channels from Torpedo electroplax. Philos Trans R Soc Lond B Biol Sci 299: 401-411
35. Miller C (2006) ClC chloride channels viewed through a transporter lens. Nature 440: 484-489
36. Nguitragool W, Miller C (2007) Inaugural article: CLC Cl/H+ transporters constrained by covalent cross-linking. Proc Natl Acad Sci USA 104: 20659-20665
37. Niemeyer MI, Cid LP, Yusef YR, Briones R, Sepulveda FV (2009) Voltage-dependent and -independent titration of specific residues accounts for complex gating of a ClC chloride channel by extracellular protons. J Physiol 587: 1387-1400
38. O?Hagan D, Harper DB (1999) Fluorine-containing natural products. J Fluor Chem 100: 127-133
39. Osteen JD, Mindell JA (2008) Insights into the ClC-4 transport mechanism from studies of Zn2+ inhibition. Biophys J 95: 4668-4675
40. Oxenoid K, Sonnichsen FD, Sanders CR (2002) Topology and secondary structure of the N-terminal domain of diacylglycerol kinase. Biochemistry 41: 12876-12882
41. Poget SF, Cahill SM, Girvin ME (2007) Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. J Am Chem Soc 129: 2432-2433
42. Prosser RS, Evanics F, Kitevski JL, Patel S (2007) The measurement of immersion depth and topology of membrane proteins by solution state NMR. Biochim Biophys Acta 1768: 3044-3051
43. Pusch M (2004) Structural insights into chloride and proton-mediated gating of CLC chloride channels. Biochemistry 43: 1135-1144 (Pubitemid 38176511)
44. Rozovsky S, Jogl G, Tong L, McDermott AE (2001) Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics. J Mol Biol 310: 271-280
45. Sun ZY, Pratt EA, Simplaceanu V, Ho C (1996) A 19F-NMR study of the equilibrium unfolding of membrane-associated D-lactate dehydrogenase of Escherichia coli. Biochemistry 35: 16502-16509
46. Walden M, Accardi A, Wu F, Xu C, Williams C, Miller C (2007) Uncoupling and turnover in a Cl-/H+ exchange transporter. J Gen Physiol 129: 317-329
47. Wang G (2008) NMR of membrane-associated peptides and proteins. Curr Protein Pept Sci 9: 50-69
48. White SH (2004) The progress of membrane protein structure determination. Protein Sci 13: 1948-1949
49. Witter R, Nozirov F, Sternberg U, Cross TA, Ulrich AS, Fu R (2008) Solid-state 19F NMR spectroscopy reveals that Trp41 participates in the gating mechanism of the M2 proton channel of influenza A virus. J Am Chem Soc 130: 918-924
50. Zdebik AA, Zifarelli G, Bergsdorf EY, Soliani P, Scheel O, Jentsch TJ, Pusch M (2008) Determinants of anion-proton coupling in mammalian endosomal CLC proteins. J Biol Chem 283: 4219-4227
51. Zifarelli G, Murgia AR, Soliani P, Pusch M (2008) Intracellular proton regulation of ClC-0. J Gen Physiol 132: 185-198