TRPV1 structures in distinct conformations reveal activation mechanisms (original) (raw)

References

  1. Basbaum, A. I., Bautista, D. M., Scherrer, G. & Julius, D. Cellular and molecular mechanisms of pain. Cell 139, 267–284 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  2. Baconguis, I. & Gouaux, E. Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 489, 400–405 (2012)
    Article ADS CAS PubMed PubMed Central Google Scholar
  3. Hansen, S. B., Tao, X. & MacKinnon, R. Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477, 495–498 (2011)
    Article ADS CAS PubMed PubMed Central Google Scholar
  4. Hattori, M. & Gouaux, E. Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485, 207–212 (2012)
    Article ADS CAS PubMed PubMed Central Google Scholar
  5. Whorton, M. R. & MacKinnon, R. X-ray structure of the mammalian GIRK2–βγ G-protein complex. Nature 498, 190–197 (2013)
    Article ADS CAS PubMed PubMed Central Google Scholar
  6. Bohlen, C. J. & Julius, D. Receptor-targeting mechanisms of pain-causing toxins: how ow? Toxicon 60, 254–264 (2012)
    Article CAS PubMed PubMed Central Google Scholar
  7. Vriens, J., Appendino, G. & Nilius, B. Pharmacology of vanilloid transient receptor potential cation channels. Mol. Pharmacol. 75, 1262–1279 (2009)
    Article CAS PubMed Google Scholar
  8. Liao, M., Cao, E., Julius, D. & Cheng, Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature http://dx.doi.org/10.1038/nature12823 (this issue)
  9. Catterall, W. A. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67, 915–928 (2010)
    Article CAS PubMed PubMed Central Google Scholar
  10. Long, S. B., Campbell, E. B. & Mackinnon, R. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903–908 (2005)
    Article ADS CAS PubMed Google Scholar
  11. Swartz, K. J. Sensing voltage across lipid membranes. Nature 456, 891–897 (2008)
    Article ADS CAS PubMed PubMed Central Google Scholar
  12. Zhu, S., Darbon, H., Dyason, K., Verdonck, F. & Tytgat, J. Evolutionary origin of inhibitor cystine knot peptides. FASEB J. 17, 1765–1767 (2003)
    Article CAS PubMed Google Scholar
  13. Phillips, L. R. et al. Voltage-sensor activation with a tarantula toxin as cargo. Nature 436, 857–860 (2005)
    Article ADS CAS PubMed Google Scholar
  14. Swartz, K. J. & MacKinnon, R. Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites. Neuron 18, 665–673 (1997)
    Article CAS PubMed Google Scholar
  15. Bohlen, C. J. et al. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 141, 834–845 (2010)
    Article CAS PubMed PubMed Central Google Scholar
  16. Siemens, J. et al. Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 444, 208–212 (2006)
    Article ADS CAS PubMed Google Scholar
  17. Grandl, J. et al. Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nature Neurosci. 13, 708–714 (2010)
    Article CAS PubMed Google Scholar
  18. 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)
    Article CAS PubMed PubMed Central Google Scholar
  19. Yang, F., Cui, Y., Wang, K. & Zheng, J. Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc. Natl Acad. Sci. USA 107, 7083–7088 (2010)
    Article ADS CAS PubMed PubMed Central Google Scholar
  20. Zhou, Y., Morais-Cabral, J. H., Kaufman, A. & MacKinnon, R. Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution. Nature 414, 43–48 (2001)
    Article ADS CAS PubMed Google Scholar
  21. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nature Methods 9, 853–854 (2012)
    Article CAS PubMed PubMed Central Google Scholar
  22. Chou, M. Z., Mtui, T., Gao, Y. D., Kohler, M. & Middleton, R. E. Resiniferatoxin binds to the capsaicin receptor (TRPV1) near the extracellular side of the S4 transmembrane domain. Biochemistry 43, 2501–2511 (2004)
    Article CAS PubMed Google Scholar
  23. Gavva, N. R. et al. Molecular determinants of vanilloid sensitivity in TRPV1. J. Biol. Chem. 279, 20283–20295 (2004)
    Article CAS PubMed Google Scholar
  24. Jordt, S. E. & Julius, D. Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108, 421–430 (2002)
    Article CAS PubMed Google Scholar
  25. Phillips, E., Reeve, A., Bevan, S. & McIntyre, P. Identification of species-specific determinants of the action of the antagonist capsazepine and the agonist PPAHV on TRPV1. J. Biol. Chem. 279, 17165–17172 (2004)
    Article CAS PubMed Google Scholar
  26. Szallasi, A., Blumberg, P. M., Annicelli, L. L., Krause, J. E. & Cortright, D. N. The cloned rat vanilloid receptor VR1 mediates both R-type binding and C-type calcium response in dorsal root ganglion neurons. Mol. Pharmacol. 56, 581–587 (1999)
    Article CAS PubMed Google Scholar
  27. Chung, M. K., Guler, A. D. & Caterina, M. J. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nature Neurosci. 11, 555–564 (2008)
    Article CAS PubMed Google Scholar
  28. Jordt, S. E., Tominaga, M. & Julius, D. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc. Natl Acad. Sci. USA 97, 8134–8139 (2000)
    Article ADS CAS PubMed PubMed Central Google Scholar
  29. Kim, S. E., Patapoutian, A. & Grandl, J. Single residues in the outer pore of TRPV1 and TRPV3 have temperature-dependent conformations. PLoS ONE 8, e59593 (2013)
    Article ADS CAS PubMed PubMed Central Google Scholar
  30. Ryu, S., Liu, B., Yao, J., Fu, Q. & Qin, F. Uncoupling proton activation of vanilloid receptor TRPV1. J. Neurosci. 27, 12797–12807 (2007)
    Article CAS PubMed PubMed Central Google Scholar
  31. Yeh, B. I., Kim, Y. K., Jabbar, W. & Huang, C. L. Conformational changes of pore helix coupled to gating of TRPV5 by protons. EMBO J. 24, 3224–3234 (2005)
    Article CAS PubMed PubMed Central Google Scholar
  32. Bernèche, S. & Roux, B. A gate in the selectivity filter of potassium channels. Structure 13, 591–600 (2005)
    Article PubMed CAS Google Scholar
  33. Cuello, L. G., Jogini, V., Cortes, D. M. & Perozo, E. Structural mechanism of C-type inactivation in K+ channels. Nature 466, 203–208 (2010)
    Article ADS CAS PubMed PubMed Central Google Scholar
  34. Hoshi, T. & Armstrong, C. M. C-type inactivation of voltage-gated K+ channels: pore constriction or dilation? J. Gen. Physiol. 141, 151–160 (2013)
    Article CAS PubMed PubMed Central Google Scholar
  35. Hui, K., Liu, B. & Qin, F. Capsaicin activation of the pain receptor, VR1: multiple open states from both partial and full binding. Biophys. J. 84, 2957–2968 (2003)
    Article ADS CAS PubMed PubMed Central Google Scholar
  36. Liu, B., Hui, K. & Qin, F. Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys. J. 85, 2988–3006 (2003)
    Article ADS CAS PubMed PubMed Central Google Scholar
  37. Tominaga, M. et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531–543 (1998)
    Article CAS PubMed Google Scholar
  38. Jiang, Y. et al. The open pore conformation of potassium channels. Nature 417, 523–526 (2002)
    Article ADS CAS PubMed Google Scholar
  39. Latorre, R., Zaelzer, C. & Brauchi, S. Structure–functional intimacies of transient receptor potential channels. Q. Rev. Biophys. 42, 201–246 (2009)
    Article CAS PubMed Google Scholar
  40. Dai, J. et al. TRPV4-pathy, a novel channelopathy affecting diverse systems. J. Hum. Genet. 55, 400–402 (2010)
    Article PubMed Google Scholar
  41. Lin, Z. et al. Exome sequencing reveals mutations in TRPV3 as a cause of Olmsted syndrome. Am. J. Hum. Genet. 90, 558–564 (2012)
    Article CAS PubMed PubMed Central Google Scholar
  42. Latorre, R., Vargas, G., Orta, G. & Brauchi, S. in TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades Frontiers in Neuroscience (eds Liedtke, W. B. & Heller, S. ). (2007)
  43. Matta, J. A. & Ahern, G. P. Voltage is a partial activator of rat thermosensitive TRP channels. J. Physiol. (Lond.) 585, 469–482 (2007)
    Article CAS Google Scholar
  44. Nilius, B. et al. Gating of TRP channels: a voltage connection? J. Physiol. (Lond.) 567, 35–44 (2005)
    Article CAS Google Scholar
  45. Loukin, S., Su, Z., Zhou, X. & Kung, C. Forward genetic analysis reveals multiple gating mechanisms of TRPV4. J. Biol. Chem. 285, 19884–19890 (2010)
    Article CAS PubMed PubMed Central Google Scholar
  46. 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)
    Article CAS PubMed PubMed Central Google Scholar
  47. van der Stelt, M. & Di Marzo, V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur. J. Biochem. 271, 1827–1834 (2004)
    Article CAS PubMed Google Scholar
  48. Brauchi, S., Orta, G., Salazar, M., Rosenmann, E. & Latorre, R. A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J. Neurosci. 26, 4835–4840 (2006)
    Article CAS PubMed PubMed Central Google Scholar
  49. Papakosta, M. et al. The chimeric approach reveals that differences in the TRPV1 pore domain determine species-specific sensitivity to block of heat activation. J. Biol. Chem. 286, 39663–39672 (2011)
    Article CAS PubMed PubMed Central Google Scholar
  50. Yao, J., Liu, B. & Qin, F. Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc. Natl Acad. Sci. USA 108, 11109–11114 (2011)
    Article ADS CAS PubMed PubMed Central Google Scholar
  51. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012)
    Article CAS PubMed PubMed Central Google Scholar
  52. Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004)
    Article CAS PubMed Google Scholar
  53. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004)
    Article CAS PubMed Google Scholar
  54. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010)
    Article CAS PubMed PubMed Central Google Scholar
  55. 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,–376 (1996)
    Article Google Scholar
  56. Takahashi, H. et al. Solution structure of hanatoxin1, a gating modifier of voltage-dependent K+ channels: common surface features of gating modifier toxins. J. Mol. Biol. 297, 771–780 (2000)
    Article CAS PubMed Google Scholar

Download references