Structure of the voltage-gated calcium channel Cav1.1 at 3.6 Å resolution

Nature

Volumn 537, Issue 7619, 2016, Pages 191-196

  Wu, Jianping ^a   Yan, Zhen ^a   Li, Zhangqiang ^a   Qian, Xingyang ^a   Lu, Shan ^b   Dong, Mengqiu ^b   Zhou, Qiang ^a   Yan, Nieng ^a  

^a TSINGHUA UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV1.1; CALCIUM CHANNEL L TYPE; PROTEIN BINDING; PROTEIN SUBUNIT;

BIOCHEMISTRY; CALCIUM; CELLS AND CELL COMPONENTS; CHEMICAL BONDING; ELECTRICAL CONDUCTIVITY; LAGOMORPH; MOLECULAR ANALYSIS; MUSCLE; SENSORY SYSTEM; SKELETON;

ALPHA CHAIN; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYOELECTRON MICROSCOPY; DISULFIDE BOND; EXCITATION CONTRACTION COUPLING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; EXTRACELLULAR SPACE; HUMAN; ION TRANSPORT; METABOLISM; MOLECULAR MODEL; PROTEIN SUBUNIT; RABBIT; ULTRASTRUCTURE;

MAMMALIA; ORYCTOLAGUS CUNICULUS;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM CHANNELS, L-TYPE; CRYOELECTRON MICROSCOPY; EXTRACELLULAR SPACE; HUMANS; ION TRANSPORT; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RABBITS;

EID: 84986575661     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19321     Document Type: Article

References (70)

1. Clapham, D. E. Calcium signaling. Cell 131, 1047-1058 (2007).
2. Zamponi, G. W., Striessnig, J., Koschak, A., Dolphin, A. C. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol. Rev. 67, 821-870 (2015).
3. Catterall, W. A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3, a003947 (2011).
4. Nowycky, M. C., Fox, A. P., Tsien, R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316, 440-443 (1985).
5. Ertel, E. A. et al. Nomenclature of voltage-gated calcium channels. Neuron 25, 533-535 (2000).
6. Hille, B. Ion Channels of Excitable Membranes, 814 (Sinauer, 2001).
7. Kang, M. G., Campbell, K. P. Subunit of voltage-activated calcium channels. J. Biol. Chem. 278, 21315-21318 (2003).
8. Davies, A. et al. Functional biology of the 2 subunits of voltage-gated calcium channels. Trends Pharmacol. Sci. 28, 220-228 (2007).
9. Buraei, Z., Yang, J. The-subunit of voltage-gated Ca2+ channels. Physiol. Rev. 90, 1461-1506 (2010).
10. Kohlhardt, M., Fleckenstein, A. Inhibition of the slow inward current by nifedipine in mammalian ventricular myocardium. Naunyn Schmiedebergs Arch. Pharmacol. 298, 267-272 (1977).
11. Fleckenstein, A. History of calcium antagonists. Circ. Res. 52, I3-I16 (1983).
12. Tanabe, T. et al. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature 328, 313-318 (1987).
13. Bannister, R. A., Beam, K. G. Ca(V)1.1: The atypical prototypical voltage-gated Ca2+ channel. Biochim. Biophys. Acta 1828, 1587-1597 (2013).
14. Rios, E., Brum, G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325, 717-720 (1987).
15. Tanabe, T., Beam, K. G., Powell, J. A., Numa, S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336, 134-139 (1988).
16. Block, B. A., Imagawa, T., Campbell, K. P., Franzini-Armstrong, C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 107, 2587-2600 (1988).
17. Adams, B. A., Tanabe, T., Mikami, A., Numa, S., Beam, K. G. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature 346, 569-572 (1990).
18. Takekura, H., Bennett, L., Tanabe, T., Beam, K. G., Franzini-Armstrong, C. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys. J. 67, 793-803 (1994).
19. Wu, J.et al. Structure of the voltage-gated calcium channel Cav1.1 complex. Science 350, 2395 (2015).
20. Simske, J. S. Claudins reign: the claudin/EMP/PMP22/channel protein family in C. elegans. Tissue Barriers 1, e25502 (2013).
21. Davies, A. et al. The 2-subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function. Proc. Natl Acad. Sci. USA 107, 1654-1659 (2010).
22. Cantí, C. et al. The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of 2-subunits is key to trafficking voltage-gated Ca2+ channels. Proc. Natl Acad. Sci. USA 102, 11230-11235 (2005).
23. Yang, J., Ellinor, P. T., Sather, W. A., Zhang, J. F., Tsien, R. W. Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature 366, 158-161 (1993).
24. Ellinor, P. T., Yang, J., Sather, W. A., Zhang, J. F., Tsien, R. W. Ca2+ channel selectivity at a single locus for high-affinity Ca2+ interactions. Neuron 15, 1121-1132 (1995).
25. Cloues, R. K., Cibulsky, S. M., Sather, W. A. Ion interactions in the high-affinity binding locus of a voltage-gated Ca2+ channel. J. Gen. Physiol. 116, 569-586 (2000).
26. Tang, L. et al. Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature 505, 56-61 (2014).
27. Payandeh, J., Scheuer, T., Zheng, N., Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011).
28. Zhang, X. et al. Crystal structure of an orthologue of the NaChBac voltagegated sodium channel. Nature 486, 130-134 (2012).
29. Ahuja, S.et al. Structural basis of Nav1.7 inhibition by an isoform-selective small-molecule antagonist. Science 350, 5464 (2015).
30. Armstrong, C. M., Bezanilla, F. Currents related to movement of the gating particles of the sodium channels. Nature 242, 459-461 (1973).
31. Noda, M. et al. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312, 121-127 (1984).
32. Tao, X., Lee, A., Limapichat, W., Dougherty, D. A., MacKinnon, R. A gating charge transfer center in voltage sensors. Science 328, 67-73 (2010).
33. Ronache, Z. et al. The auxiliary-subunit 1 of the skeletal muscle L-type Ca2+ channel is an endogenous Ca2+ antagonist. Proc. Natl Acad. Sci. USA 104, 17885-17890 (2007).
34. Almagor, L. et al. The role of a voltage-dependent Ca2+ channel intracellular linker: a structure-function analysis. J. Neurosci. 32, 7602-7613 (2012).
35. Yan, Z. et al. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 517, 50-55 (2015).
36. Zalk, R. et al. Structure of a mammalian ryanodine receptor. Nature 517, 44-49 (2015).
37. Efremov, R. G., Leitner, A., Aebersold, R., Raunser, S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517, 39-43 (2015).
38. Gregg, R. G. et al. Absence of the subunit (cchb1) of the skeletal muscle dihydropyridine receptor alters expression of the 1 subunit and eliminates excitation-contraction coupling. Proc. Natl Acad. Sci. USA 93, 13961-13966 (1996).
39. Cheng, W., Altafaj, X., Ronjat, M., Coronado, R. Interaction between the dihydropyridine receptor Ca2+ channel-subunit and ryanodine receptor type 1 strengthens excitation-contraction coupling. Proc. Natl Acad. Sci. USA 102, 19225-19230 (2005).
40. Schredelseker, J. et al. The 1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle. Proc. Natl Acad. Sci. USA 102, 17219-17224 (2005).
41. Stotz, S. C., Jarvis, S. E., Zamponi, G. W. Functional roles of cytoplasmic loops and pore lining transmembrane helices in the voltage-dependent inactivation of HVA calcium channels.J. Physiol. (Lond.) 554, 263-273 (2004).
42. Wang, C., Chung, B. C., Yan, H., Lee, S. Y., Pitt, G. S. Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin. Structure 20, 1167-1176 (2012).
43. Wang, C. et al. Structural analyses of Ca2+/CaM interaction with NaV channel C-termini reveal mechanisms of calcium-dependent regulation. Nature Commun. 5, 4896 (2014).
44. Lee, K. S., Marban, E., Tsien, R. W. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium. J. Physiol. (Lond.) 364, 395-411 (1985).
45. Zühlke, R. D., Pitt, G. S., Deisseroth, K., Tsien, R. W., Reuter, H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399, 159-162 (1999).
46. Armstrong, C.M., Bezanilla, F. Inactivation of the sodium channel. II. Gating current experiments. J Gen. Physiol. 70, 567-90 (1977).
47. Rohl, C.A. et al. Solution structure of the sodium channel inactivation gate. Biochemistry 38, 855-61 (1999).
48. DeLano, W. L. The PyMOL Molecular Graphics System (2002).
49. Smart, O. S., Neduvelil, J. G., Wang, X., Wallace, B. A., Sansom, M. S. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14, 354-376 (1996).
50. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
51. Yuan, Z. F. et al. pParse: a method for accurate determination of monoisotopic peaks in high-resolution mass spectra. Proteomics 12, 226-235 (2012).
52. Lu, S. et al. Mapping native disulfide bonds at a proteome scale. Nature Methods 12, 329-331 (2015).
53. 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).
54. 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).
55. Mindell, J. A., Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
56. Scheres, S. H. W. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
57. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
58. Gong, X. et al. Structural insights into the Niemann-Pick C1 (NPC1)-mediated cholesterol transfer and Ebola infection. Cell 165, 1467-1478 (2016).
59. Rosenthal, P. B., Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721-745 (2003).
60. Kucukelbir, A., Sigworth, F. J., Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
61. Emsley, P., Lohkamp, B., Scott, W. G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
62. DiMaio, F., Tyka, M. D., Baker, M. L., Chiu, W., Baker, D. Refinement of protein structures into low-resolution density maps using Rosetta. J. Mol. Biol. 392, 181-190 (2009).
63. Song, Y. et al. High-resolution comparative modeling with RosettaCM. Structure 21, 1735-1742 (2013).
64. DiMaio, F. et al. Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement. Nature Methods 12, 361-365 (2015).
65. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
66. Murshudov, G. N., Vagin, A. A., Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255 (1997).
67. Nicholls, R. A., Fischer, M., McNicholas, S., Murshudov, G. N. Conformationindependent structural comparison of macromolecules with ProSMART. Acta Crystallogr. D 70, 2487-2499 (2014).
68. Amunts, A. et al. Structure of the yeast mitochondrial large ribosomal-subunit. Science 343, 1485-1489 (2014).
69. Guo, J. et al. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531, 196-201 (2016).
70. Kintzer, A. F., Stroud, R. M. Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana. Nature 531, 258-264 (2016).