Structure of the TRPV1 ion channel determined by electron cryo-microscopy

Nature

Volumn 504, Issue 7478, 2013, Pages 107-112

  Liao, Maofu ^a   Cao, Erhu ^b   Julius, David ^a   Cheng, Yifan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; VANILLOID RECEPTOR 1;

CRYSTALLIZATION; CYTOPLASM; ELECTRON MICROSCOPY; ION EXCHANGE; MEMBRANE; PROTEIN; SIGNAL;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTALLIZATION; CYTOPLASM; FILTER; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ANIMALS; ANKYRIN REPEAT; CRYOELECTRON MICROSCOPY; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RATS; TRPV CATION CHANNELS;

EID: 84889607320     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12822     Document Type: Article

References (56)

1. Ramsey, I. S., Delling, M. & Clapham, D. E. An introduction to TRP channels. Annu. Rev. Physiol. 68, 619-647 (2006).
2. Venkatachalam, K. & Montell, C. TRP channels. Annu. Rev. Biochem. 76, 387-417 (2007).
3. Nilius, B. & Owsianik, G. Transient receptor potential channelopathies. Pflugers Arch. 460, 437-450 (2010).
4. Nilius, B. et al. Gating of TRPchannels: a voltage connection? J. Physiol. (Lond.) 567, 35-44 (2005).
5. Long, S. B., Campbell, E. B. & Mackinnon, R. Crystal structure of a mammalian voltage-dependent Shaker family K1 channel. Science 309, 897-903 (2005).
6. Long, S. B., Tao, X., Campbell, E. B. & MacKinnon, R. Atomic structure of a voltagedependent K1 channel in a lipid membrane-like environment. Nature 450, 376-382 (2007).
7. Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011).
8. Zhang, X. et al. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486, 130-134 (2012).
9. Caterina, M. J. et al.The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824 (1997).
10. Cao, E., Cordero-Morales, J. F., Liu, B., Qin, F. & Julius, D. TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 77, 667-679 (2013).
11. Yao, J., Liu, B.& Qin, F. Kinetic and energetic analysis of thermally activated TRPV1 channels. Biophys. J. 99, 1743-1753 (2010).
12. Brederson, J. D., Kym, P. R.&Szallasi, A. Targeting TRP channels for pain relief. Eur. J. Pharmacol. 716, 61-76 (2013).
13. Julius, D. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29, 355-384 (2013).
14. Bai, X. C., Fernandez, I. S., McMullan, G. & Scheres, S. H. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife 2, e00461 (2013).
15. Li, X. et al. Electron counting and beam-induced motion correction enable nearatomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
16. Yu, X., Jin, L. & Zhou, Z. H. 3.88A? structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 453, 415-419 (2008).
17. Zhang, X., Jin, L., Fang, Q., Hui, W. H. & Zhou, Z. H. 3.3A? cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 141, 472-482 (2010).
18. Mio, K. et al. The TRPC3 channel has a large internal chamber surrounded by signal sensing antennas. J. Mol. Biol. 367, 373-383 (2007).
19. Moiseenkova-Bell, V. Y., Stanciu, L. A., Serysheva, I. I., Tobe, B. J. & Wensel, T. G. Structure of TRPV1 channel revealed by electron cryomicroscopy. Proc. Natl Acad. Sci. USA 105, 7451-7455 (2008).
20. Shigematsu, H., Sokabe, T., Danev, R., Tominaga, M. & Nagayama, K. A 3.5-nm structure of rat TRPV4 cation channel revealed by Zernike phase-contrast cryoelectron microscopy. J. Biol. Chem. 285, 11210-11218 (2010).
21. Chung, M. K., Guler, A. D. & Caterina, M. J. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nature Neurosci. 11, 555-564 (2008).
22. Myers, B. R., Bohlen, C. J.&Julius, D. A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron 58, 362-373 (2008).
23. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nature Methods 9, 853-854 (2012).
24. Lishko, P. V., Procko, E., Jin, X., Phelps, C. B. & Gaudet, R. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54, 905-918 (2007).
25. Catterall, W. A. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67, 915-928 (2010).
26. Swartz, K. J. Sensing voltage across lipid membranes. Nature 456, 891-897 (2008).
27. Boukalova, S., Marsakova, L., Teisinger, J. & Vlachova, V. Conserved residues within the putative S4-S5 region serve distinct functions among thermosensitive vanilloid transient receptor potential (TRPV) channels. J. Biol. Chem. 285, 41455-41462 (2010).
28. Boukalova, S., Teisinger, J.&Vlachova, V. Protons stabilize the closedconformation of gain-of-function mutants of the TRPV1 channel. Biochim. Biophys. Acta 1833, 520-528 (2013).
29. Cao, E., Liao, M., Cheng, Y. & Julius, D. TRPV1 structures in distinct conformations revealmechanisms of activation. Nature http://dx.doi.org/10.1038/nature12823 (this issue).
30. Latorre, R., Zaelzer, C. & Brauchi, S. Structure-functional intimacies of transient receptor potential channels. Q. Rev. Biophys. 42, 201-246 (2009).
31. Lin, Z. et al. Exome sequencing reveals mutations in TRPV3 as a cause of Olmsted syndrome. Am. J. Hum. Genet. 90, 558-564 (2012).
32. Long, S. B., Campbell, E. B. & Mackinnon, R. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903-908 (2005).
33. Loukin, S., Su, Z. & Kung, C. Increased basal activity is a key determinant in the severity of human skeletal dysplasia caused by TRPV4 mutations. PLoS ONE 6, e19533 (2011).
34. Owsianik, G., Talavera, K., Voets, T. & Nilius, B. Permeation and selectivity of TRP channels. Annu. Rev. Physiol. 68, 685-717 (2006).
35. Susankova, K., Ettrich, R., Vyklicky, L., Teisinger, J.&Vlachova, V. Contribution of the putative inner-pore region to the gating of the transient receptor potential vanilloid subtype 1 channel (TRPV1). J. Neurosci. 27, 7578-7585 (2007).
36. Voets, T., Janssens, A., Droogmans, G. & Nilius, B. Outer pore architecture of a Ca21-selective TRP channel. J. Biol. Chem. 279, 15223-15230 (2004).
37. Binshtok, A. M., Bean, B. P. & Woolf, C. J. Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449, 607-610 (2007).
38. Salazar, H. et al. Structural determinants of gating in the TRPV1 channel. Nature Struct. Mol. Biol. 16, 704-710 (2009).
39. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K1 conduction and selectivity. Science 280, 69-77 (1998).
40. Gaudet, R. A primer on ankyrin repeat function in TRP channels and beyond. Mol. Biosyst. 4, 372-379 (2008).
41. Inanobe, A., Matsuura, T., Nakagawa, A. & Kurachi, Y. Structural diversity in the cytoplasmic region of G protein-gated inward rectifier K1 channels. Channels (Austin) 1, 39-45 (2007).
42. Nishida, M. & MacKinnon, R. Structural basis of inward rectification: cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8A? resolution. Cell 111, 957-965 (2002).
43. Inada, H., Procko, E., Sotomayor, M. & Gaudet, R. Structural and biochemical consequences of disease-causing mutations in the ankyrin repeat domain of the human TRPV4 channel. Biochemistry 51, 6195-6206 (2012).
44. Booth, D. S., Avila-Sakar, A. & Cheng, Y. Visualizing proteins and macromolecular complexes by negative stainEM: fromgrid preparation to image acquisition. J. Vis. Exp. 58, 3227 (2011).
45. Dukkipati, A., Park, H. H.,Waghray, D., Fischer, S.&Garcia, K. C. BacMamsystemfor high-level expression of recombinant soluble and membrane glycoproteins for structural studies. Protein Expr. Purif. 62, 160-170 (2008).
46. Reeves, P. J., Callewaert, N.,Contreras, R.&Khorana, H. G. Structure and functionin rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N- acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl Acad. Sci. USA 99, 13419-13424 (2002).
47. Althoff, T., Mills, D. J., Popot, J. L. & Kuhlbrandt, W. Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J. 30, 4652-4664 (2011).
48. Popot, J. L. et al. Amphipols from A to Z. Annu. Rev. Biophys. 40, 379-408 (2011).
49. Mindell, J. A.&Grigorieff, N. Accurate determinationof local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
50. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
51. Grigorieff, N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157, 117-125 (2007).
52. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
53. Pettersen, E. F. et al.UCSFChimera- A visualization systemfor exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
55. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
56. 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, 354-360 (1996).