Structure of a eukaryotic cyclic-nucleotide-gated channel

Nature

Volumn 542, Issue 7639, 2017, Pages 60-65

  Li, Minghui ^a   Zhou, Xiaoyuan ^b   Wang, Shu ^c,d,e   Michailidis, Ioannis ^a   Gong, Ye ^c,d   Su, Deyuan ^c,d,e   Li, Huan ^c,d,e   Li, Xueming ^b   Yang, Jian ^a,c,d  

^a Howard Hughes Medical Institute   (United States)

^b TSINGHUA UNIVERSITY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d KUNMING INSTITUTE OF ZOOLOGY   (China)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARBONYL DERIVATIVE; CARBOXYLIC ACID; CYCLIC NUCLEOTIDE; CYCLIC NUCLEOTIDE GATED CHANNEL; GLUTAMIC ACID; PROTEIN S6; CAENORHABDITIS ELEGANS PROTEIN; CYCLIC GMP; ION CHANNEL; TAX-4 PROTEIN, C ELEGANS;

CARBOXYLIC ACID; CHEMICAL BINDING; ELECTRON MICROSCOPY; EUKARYOTE; FILTER; OLFACTION; SENSOR;

ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ELECTRIC POTENTIAL; EUKARYOTE; FILTER; ION PERMEABILITY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ELECTRIC CONDUCTIVITY; METABOLISM; MOLECULAR MODEL; ULTRASTRUCTURE;

CAENORHABDITIS ELEGANS; EUKARYOTA;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CRYOELECTRON MICROSCOPY; CYCLIC GMP; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ELECTRIC CONDUCTIVITY; GLUTAMIC ACID; ION CHANNEL GATING; ION CHANNELS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN DOMAINS;

EID: 85016153637     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20819     Document Type: Article

References (57)

1. Kaupp, U. B. & Seifert, R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769-824 (2002).
2. Zagotta, W. N. & Siegelbaum, S. A. Structure and function of cyclic nucleotidegated channels. Annu. Rev. Neurosci. 19, 235-263 (1996).
3. Varnum, M. D. & Dai, G. in The Handbook of Ion Channels (eds Zheng, J. & Trudeau, M. C.) 361-382 (CRC, 2015).
4. Fesenko, E. E., Kolesnikov, S. S. & Lyubarsky, A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310-313 (1985).
5. Yau, K. W. & Baylor, D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu. Rev. Neurosci. 12, 289-327 (1989).
6. Nakamura, T. & Gold, G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325, 442-444 (1987).
7. Kaupp, U. B. et al. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342, 762-766 (1989).
8. Dhallan, R. S., Yau, K. W., Schrader, K. A. & Reed, R. R. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347, 184-187 (1990).
9. Gordon, S. E. & Zagotta, W. N. A histidine residue associated with the gate of the cyclic nucleotide-activated channels in rod photoreceptors. Neuron 14, 177-183 (1995).
10. Gordon, S. E. & Zagotta, W. N. Localization of regions affecting an allosteric transition in cyclic nucleotide-activated channels. Neuron 14, 857-864 (1995).
11. Brown, R. L., Snow, S. D. & Haley, T. L. Movement of gating machinery during the activation of rod cyclic nucleotide-gated channels. Biophys. J. 75, 825-833 (1998).
12. Zong, X., Zucker, H., Hofmann, F. & Biel, M. Three amino acids in the C-linker are major determinants of gating in cyclic nucleotide-gated channels. EMBO J. 17, 353-362 (1998).
13. Zhou, L., Olivier, N. B., Yao, H., Young, E. C. & Siegelbaum, S. A. A conserved tripeptide in CNG and HCN channels regulates ligand gating by controlling C-terminal oligomerization. Neuron 44, 823-834 (2004).
14. Paoletti, P., Young, E. C. & Siegelbaum, S. A. C-Linker of cyclic nucleotide-gated channels controls coupling of ligand binding to channel gating. J. Gen. Physiol. 113, 17-34 (1999).
15. Long, S. B., Campbell, E. B. & Mackinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309, 897-903 (2005).
16. Long, S. B., Campbell, E. B. & Mackinnon, R. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903-908 (2005).
17. Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011).
18. Wu, J. et al. Structure of the voltage-gated calcium channel Cav1.1 complex. Science 350, aad2395 (2015).
19. Liao, M., Cao, E., Julius, D. & Cheng, Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107-112 (2013).
20. Paulsen, C. E., Armache, J. P., Gao, Y., Cheng, Y. & Julius, D. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520, 511-517 (2015).
21. Komatsu, H., Mori, I., Rhee, J. S., Akaike, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707-718 (1996).
22. Komatsu, H. et al. Functional reconstitution of a heteromeric cyclic nucleotidegated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821, 160-168 (1999).
23. Long, S. B., Tao, X., Campbell, E. B. & MacKinnon, R. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450, 376-382 (2007).
24. Arcangeletti, M., Marchesi, A., Mazzolini, M. & Torre, V. Multiple mechanisms underlying rectification in retinal cyclic nucleotide-gated (CNGA1) channels. Physiol. Rep. 1, e00148 (2013).
25. Flynn, G. E. & Zagotta, W. N. Conformational changes in S6 coupled to the opening of cyclic nucleotide-gated channels. Neuron 30, 689-698 (2001).
26. Contreras, J. E. & Holmgren, M. Access of quaternary ammonium blockers to the internal pore of cyclic nucleotide-gated channels: implications for the location of the gate. J. Gen. Physiol. 127, 481-494 (2006).
27. Contreras, J. E., Srikumar, D. & Holmgren, M. Gating at the selectivity filter in cyclic nucleotide-gated channels. Proc. Natl Acad. Sci. USA 105, 3310-3314 (2008).
28. Goulding, E. H., Tibbs, G. R., Liu, D. & Siegelbaum, S. A. Role of H5 domain in determining pore diameter and ion permeation through cyclic nucleotidegated channels. Nature 364, 61-64 (1993).
29. Eismann, E., Muller, F., Heinemann, S. H. & Kaupp, U. B. A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. Proc. Natl Acad. Sci. USA 91, 1109-1113 (1994).
30. Root, M. J. & MacKinnon, R. Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel. Neuron 11, 459-466 (1993).
31. Morrill, J. A. & MacKinnon, R. Isolation of a single carboxyl-carboxylate proton binding site in the pore of a cyclic nucleotide-gated channel. J. Gen. Physiol. 114, 71-83 (1999).
32. Derebe, M. G. et al. Tuning the ion selectivity of tetrameric cation channels by changing the number of ion binding sites. Proc. Natl Acad. Sci. USA 108, 598-602 (2011).
33. Derebe, M. G., Zeng, W., Li, Y., Alam, A. & Jiang, Y. Structural studies of ion permeation and Ca2+ blockage of a bacterial channel mimicking the cyclic nucleotide-gated channel pore. Proc. Natl Acad. Sci. USA 108, 592-597 (2011).
34. Napolitano, L. M. et al. A structural, functional, and computational analysis suggests pore flexibility as the base for the poor selectivity of CNG channels. Proc. Natl Acad. Sci. USA 112, E3619-E3628 (2015).
35. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69-77 (1998).
36. Zagotta, W. N. et al. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425, 200-205 (2003).
37. Saponaro, A. et al. Structural basis for the mutual antagonism of cAMP and TRIP8b in regulating HCN channel function. Proc. Natl Acad. Sci. USA 111, 14577-14582 (2014).
38. Schunke, S. & Stoldt, M. Structural snapshot of cyclic nucleotide binding domains from cyclic nucleotide-sensitive ion channels. Biol. Chem. 394, 1439-1451 (2013).
39. Xu, X., Vysotskaya, Z. V., Liu, Q. & Zhou, L. Structural basis for the cAMPdependent gating in the human HCN4 channel. J. Biol. Chem. 285, 37082-37091 (2010).
40. Lolicato, M. et al. Tetramerization dynamics of C-terminal domain underlies isoform-specific cAMP gating in hyperpolarization-activated cyclic nucleotidegated channels. J. Biol. Chem. 286, 44811-44820 (2011).
41. Taraska, J. W., Puljung, M. C., Olivier, N. B., Flynn, G. E. & Zagotta, W. N. Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nature Methods 6, 532-537 (2009).
42. Altieri, S. L. et al. Structural and energetic analysis of activation by a cyclic nucleotide binding domain. J. Mol. Biol. 381, 655-669 (2008).
43. Puljung, M. C. & Zagotta, W. N. A secondary structural transition in the C-helix promotes gating of cyclic nucleotide-regulated ion channels. J. Biol. Chem. 288, 12944-12956 (2013).
44. Puljung, M. C., DeBerg, H. A., Zagotta, W. N. & Stoll, S. Double electron-electron resonance reveals cAMP-induced conformational change in HCN channels. Proc. Natl Acad. Sci. USA 111, 9816-9821 (2014).
45. Zhou, L. & Siegelbaum, S. A. Gating of HCN channels by cyclic nucleotides: residue contacts that underlie ligand binding, selectivity, and efficacy. Structure 15, 655-670 (2007).
46. Nair, A. V., Nguyen, C. H. & Mazzolini, M. Conformational rearrangements in the S6 domain and C-linker during gating in CNGA1 channels. Eur. Biophys. J. 38, 993-1002 (2009).
47. Saotome, K., Singh, A. K., Yelshanskaya, M. V. & Sobolevsky, A. I. Crystal structure of the epithelial calcium channel TRPV6. Nature 534, 506-511 (2016).
48. Whicher, J. R. & MacKinnon, R. Structure of the voltage-gated K+ channel Eag1 reveals an alternative voltage sensing mechanism. Science 353, 664-669 (2016).
49. Li, X., Zheng, S., Agard, D. A. & Cheng, Y. Asynchronous data acquisition and on-the-fly analysis of dose fractionated cryoEM images by UCSFImage. J. Struct. Biol. 192, 174-178 (2015).
50. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
51. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
52. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
53. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
54. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
55. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
56. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
57. Amunts, A. et al. Structure of the yeast mitochondrial large ribosomal subunit. Science 343, 1485-1489 (2014).