Structure, Dynamics and Implied Gating Mechanism of a Human Cyclic Nucleotide-Gated Channel

PLoS Computational Biology

Volumn 10, Issue 12, 2014, Pages

  Gofman, Yana ^a,e   Schärfe, Charlotta ^b,c   Marks, Debora S ^c   Haliloglu, Turkan ^d   Ben Tal, Nir ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BOGAZICI UNIVERSITY   (Turkey)

^e STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE; CYCLIC NUCLEOTIDE BINDING DOMAIN; GATED CHANNELS; GATING MECHANISMS; ION CHANNEL; SENSOR DOMAINS; STRUCTURE DYNAMICS; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE DOMAIN; VOLTAGE SENSOR;

NUCLEOTIDES;

BACTERIAL PROTEIN; CYCLIC NUCLEOTIDE GATED CHANNEL; KIRBAC CHANNEL; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; CYCLIC NUCLEOTIDE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL;

ALLOSTERISM; ARTICLE; CHANNEL GATING; CYTOSOL; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; ANIMAL; BIOLOGY; CHEMISTRY; HUMAN; METABOLISM; MOUSE; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS);

ANIMALS; COMPUTATIONAL BIOLOGY; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; HUMANS; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MICE; MOLECULAR DYNAMICS SIMULATION; NUCLEOTIDES, CYCLIC; PROTEIN STRUCTURE, TERTIARY;

EID: 84919668874     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003976     Document Type: Article

References (79)

1. Matulef K, Zagotta WN, (2003) Cyclic nucleotide-gated ion channels. Annu Rev Cell Dev Biol 19: 23–44.
2. Yu FH, Catterall WA, (2004) The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004: re15.
3. Biel M, Michalakis S, (2007) Function and dysfunction of CNG channels: insights from channelopathies and mouse models. Mol Neurobiol 35: 266–277.
4. Wang Z, Jiang Y, Lu L, Huang R, Hou Q, et al. (2007) Molecular mechanisms of cyclic nucleotide-gated ion channel gating. J Genet Genomics 34: 477–485.
5. Craven KB, Zagotta WN, (2006) CNG and HCN channels: two peas, one pod. Annu Rev Physiol 68: 375–401.
6. Kaupp UB, Seifert R, (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82: 769–824.
7. Peng C, Rich ED, Varnum MD, (2004) Subunit configuration of heteromeric cone cyclic nucleotide-gated channels. Neuron 42: 401–410.
8. Ding XQ, Matveev A, Singh A, Komori N, Matsumoto H, (2012) Biochemical characterization of cone cyclic nucleotide-gated (CNG) channel using the infrared fluorescence detection system. Adv Exp Med Biol 723: 769–775.
9. Reuter P, Koeppen K, Ladewig T, Kohl S, Baumann B, et al. (2008) Mutations in CNGA3 impair trafficking or function of cone cyclic nucleotide-gated channels, resulting in achromatopsia. Hum Mutat 29: 1228–1236.
10. Clayton GM, Altieri S, Heginbotham L, Unger VM, Morais-Cabral JH, (2008) Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel. Proc Natl Acad Sci USA 105: 1511–1515.
11. Clayton GM, Silverman WR, Heginbotham L, Morais-Cabral JH, (2004) Structural basis of ligand activation in a cyclic nucleotide regulated potassium channel. Cell 119: 615–627.
12. Altieri SL, Clayton GM, Silverman WR, Olivares AO, De la Cruz EM, et al. (2008) Structural and energetic analysis of activation by a cyclic nucleotide binding domain. J Mol Biol 381: 655–669.
13. Schunke S, Stoldt M, Novak K, Kaupp UB, Willbold D, (2009) Solution structure of the Mesorhizobium loti K1 channel cyclic nucleotide-binding domain in complex with cAMP. EMBO Rep 10: 729–735.
14. Schunke S, Stoldt M, Lecher J, Kaupp UB, Willbold D, (2011) Structural insights into conformational changes of a cyclic nucleotide-binding domain in solution from Mesorhizobium loti K1 channel. Proc Natl Acad Sci USA 108: 6121–6126.
15. Zagotta WN, Olivier NB, Black KD, Young EC, Olson R, et al. (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425: 200–205.
16. Flynn GE, Black KD, Islas LD, Sankaran B, Zagotta WN, (2007) Structure and rearrangements in the carboxy-terminal region of SpIH channels. Structure 15: 671–682.
17. Craven KB, Olivier NB, Zagotta WN, (2008) C-terminal movement during gating in cyclic nucleotide-modulated channels. J Biol Chem 283: 14728–14738.
18. Taraska JW, Puljung MC, Olivier NB, Flynn GE, Zagotta WN, (2009) Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nat Methods 6: 532–537.
19. Xu X, Vysotskaya ZV, Liu Q, Zhou L, (2010) Structural basis for the cAMP-dependent gating in the human HCN4 channel. J Biol Chem 285: 37082–37091.
20. Lolicato M, Nardini M, Gazzarrini S, Moller S, Bertinetti D, et al. (2011) Tetramerization dynamics of C-terminal domain underlies isoform-specific cAMP gating in hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 286: 44811–44820.
21. Cukkemane A, Seifert R, Kaupp UB, (2011) Cooperative and uncooperative cyclic-nucleotide-gated ion channels. Trends Biochem Sci 36: 55–64.
22. Richards MJ, Gordon SE, (2000) Cooperativity and cooperation in cyclic nucleotide-gated ion channels. Biochemistry 39: 14003–14011.
23. Karpen JW, Ruiz M, (2002) Ion channels: does each subunit do something on its own? Trends Biochem Sci 27: 402–409.
24. Karpen JW, Zimmerman AL, Stryer L, Baylor DA, (1988) Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc Natl Acad Sci USA 85: 1287–1291.
25. Tibbs GR, Goulding EH, Siegelbaum SA, (1997) Allosteric activation and tuning of ligand efficacy in cyclic-nucleotide-gated channels. Nature 386: 612–615.
26. Monod J, Wyman J, Changeux JP, (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88–118.
27. Liu DT, Tibbs GR, Paoletti P, Siegelbaum SA, (1998) Constraining ligand-binding site stoichiometry suggests that a cyclic nucleotide-gated channel is composed of two functional dimers. Neuron 21: 235–248.
28. Craven KB, Zagotta WN, (2004) Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels. J Gen Physiol 124: 663–677.
29. Kalman M, Ben-Tal N, (2010) Quality assessment of protein model-structures using evolutionary conservation. Bioinformatics 26: 1299–1307.
30. Hopf TA, Colwell LJ, Sheridan R, Rost B, Sander C, et al. (2012) Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149: 1607–1621.
31. Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, et al. (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6: e28766.
32. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 108: E1293–1301.
33. Marks DS, Hopf TA, Sander C, (2012) Protein structure prediction from sequence variation. Nat Biotechnol 30: 1072–1080.
34. Taylor WR, Hamilton RS, Sadowski MI, (2013) Prediction of contacts from correlated sequence substitutions. Curr Opin Struct Biol 23: 473–479.
35. Haliloglu T, Bahar I, Erman B, (1997) Gaussian dynamics of folded proteins. Phys Rev Lett 79: 3090.
36. Bahar I, Rader AJ, (2005) Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 15: 586–592.
37. Bahar I, Lezon TR, Bakan A, Shrivastava IH, (2010) Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins. Chem Rev 110: 1463–1497.
38. Giorgetti A, Nair AV, Codega P, Torre V, Carloni P, (2005) Structural basis of gating of CNG channels. FEBS Lett 579: 1968–1972.
39. Flynn GE, Johnson JP, JrZagotta WN, (2001) Cyclic nucleotide-gated channels: shedding light on the opening of a channel pore. Nat Rev Neurosci 2: 643–651.
40. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529–533.
41. Bahar I, (2010) On the functional significance of soft modes predicted by coarse-grained models for membrane proteins. J Gen Physiol 135: 563–573.
42. Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, et al. (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90: 291–366.
43. Bavro VN, De Zorzi R, Schmidt MR, Muniz JR, Zubcevic L, et al. (2012) Structure of a KirBac potassium channel with an open bundle crossing indicates a mechanism of channel gating. Nat Struct Mol Biol 19: 158–163.
44. Clarke OB, Caputo AT, Hill AP, Vandenberg JI, Smith BJ, et al. (2010) Domain reorientation and rotation of an intracellular assembly regulate conduction in Kir potassium channels. Cell 141: 1018–1029.
45. Smart OS, Goodfellow JM, Wallace BA, (1993) The pore dimensions of gramicidin A. Biophys J. 65: 2455–2460.
46. Swartz KJ, (2004) Towards a structural view of gating in potassium channels. Nat Rev Neurosci 5: 905–916.
47. Shrivastava IH, Bahar I, (2006) Common mechanism of pore opening shared by five different potassium channels. Biophys J 90: 3929–3940.
48. Haliloglu T, Ben-Tal N, (2008) Cooperative transition between open and closed conformations in potassium channels. PLoS Comput Biol 4: e1000164.
49. Gofman Y, Shats S, Attali B, Haliloglu T, Ben-Tal N, (2012) How does KCNE1 regulate the Kv7.1 potassium channel? Model-structure, mutations, and dynamics of the Kv7.1-KCNE1 complex. Structure 20: 1343–1352.
50. Valadie H, Lacapcre JJ, Sanejouand YH, Etchebest C, (2003) Dynamical properties of the MscL of Escherichia coli: a normal mode analysis. J Mol Biol 332: 657–674.
51. Zhu F, Hummer G, (2010) Pore opening and closing of a pentameric ligand-gated ion channel. Proc Natl Acad Sci U S A 107: 19814–19819.
52. Yeheskel A, Haliloglu T, Ben-Tal N, (2010) Independent and cooperative motions of the Kv1.2 channel: voltage sensing and gating. Biophys J 98: 2179–2188.
53. Schushan M, Ben-Tal N (2010) Modeling and Validation of Transmembrane Protein Structures. In: Rangwala H, Karypis G, editors.Introduction to Protein Structure Prediction.New Jersey: John Wiley & Sons. pp. 369–401.
54. Mazzolini M, Marchesi A, Giorgetti A, Torre V, (2010) Gating in CNGA1 channels. Pflugers Arch 459: 547–555.
55. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, et al. (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80: 505–515.
56. Bahar I, Atilgan AR, Erman B, (1997) Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des 2: 173–181.
57. Emekli U, Schneidman-Duhovny D, Wolfson HJ, Nussinov R, Haliloglu T, (2008) HingeProt: automated prediction of hinges in protein structures. Proteins 70: 1219–1227.
58. Sadowski MI, Maksimiak K, Taylor WR, (2011) Direct correlation analysis improves fold recognition. Computational Biology and Chemistry 35: 323–332.
59. Tanaka N, Delemotte L, Klein ML, Komaromy AM, Tanaka JC, (2014) A cyclic nucleotide-gated channel mutation associated with canine daylight blindness provides insight into a role for the S2 segment tri-Asp motif in channel biogenesis. PLoS One 9: e88768.
60. Faillace MP, Bernabeu RO, Korenbrot JI, (2004) Cellular processing of cone photoreceptor cyclic GMP-gated ion channels: a role for the S4 structural motif. J Biol Chem 279: 22643–22653.
61. Goldenberg O, Erez E, Nimrod G, Ben-Tal N, (2009) The ConSurf-DB: pre-calculated evolutionary conservation profiles of protein structures. Nucleic Acids Res 37: D323–327.
62. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
63. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195–202.
64. Nugent T, Jones DT, (2009) Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 10: 159.
65. Tusnady GE, Simon I, (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283: 489–506.
66. Hildebrand A, Remmert M, Biegert A, Soding J, (2009) Fast and accurate automatic structure prediction with HHpred. Proteins 77: 128–132.
67. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A, (2005) FFAS03: a server for profile—profile sequence alignments. Nucleic Acids Res 33: W284–288.
68. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31: 365–370.
69. Biegert A, Soding J, (2009) Sequence context-specific profiles for homology searching. Proc Natl Acad Sci USA 106: 3770–3775.
70. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5 6.
71. Wang C, Bradley P, Baker D, (2007) Protein-protein docking with backbone flexibility. J Mol Biol 373: 503–519.
72. Canutescu AA, Dunbrack RL, Jr (2003) Cyclic coordinate descent: a robotics algorithm for protein loop closure. Protein Sci 12: 963–972.
73. Eddy SR, (2011) Accelerated Profile HMM Searches. PLoS Comput Biol 7: e1002195.
74. The UniProt Consortium, (2013) Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res 41: D43–47.
75. Ekeberg M, Lövkvist C, Lan Y, Weigt M, Aurell E, (2013) Improved contact prediction in proteins: Using pseudolikelihoods to infer Potts models. Physical Review E 87: 012707.
76. Kessel A, Ben-Tal N (2002) Free energy determinants of peptide association with lipid bilayers. In: Sidney A. Simon TJM, editor.Current Topics in Membranes: Academic Press. pp. 205–253.
77. Flynn GE, Zagotta WN, (2001) Conformational changes in S6 coupled to the opening of cyclic nucleotide-gated channels. Neuron 30: 689–698.
78. Flynn GE, Zagotta WN, (2003) A cysteine scan of the inner vestibule of cyclic nucleotide-gated channels reveals architecture and rearrangement of the pore. J Gen Physiol 121: 563–582.
79. Mazzolini M, Anselmi C, Torre V, (2009) The analysis of desensitizing CNGA1 channels reveals molecular interactions essential for normal gating. J Gen Physiol 133: 375–386.