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Structural snapshots of TRPV1 reveal mechanism of polymodal functionality.

Zhang K, Julius D, Cheng Y
Cell 184 5138-5150.e12 (2021)
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Cited: 48 times
EuropePMC logo PMID: 34496225

Abstract

Many transient receptor potential (TRP) channels respond to diverse stimuli and conditionally conduct small and large cations. Such functional plasticity is presumably enabled by a uniquely dynamic ion selectivity filter that is regulated by physiological agents. What is currently missing is a "photo series" of intermediate structural states that directly address this hypothesis and reveal specific mechanisms behind such dynamic channel regulation. Here, we exploit cryoelectron microscopy (cryo-EM) to visualize conformational transitions of the capsaicin receptor, TRPV1, as a model to understand how dynamic transitions of the selectivity filter in response to algogenic agents, including protons, vanilloid agonists, and peptide toxins, permit permeation by small and large organic cations. These structures also reveal mechanisms governing ligand binding substates, as well as allosteric coupling between key sites that are proximal to the selectivity filter and cytoplasmic gate. These insights suggest a general framework for understanding how TRP channels function as polymodal signal integrators.

Reviews - 7l2t mentioned but not cited (2)

  1. Ligand-Binding Sites in Vanilloid-Subtype TRP Channels. Yelshanskaya MV, Sobolevsky AI. Front Pharmacol 13 900623 (2022)
  2. Cryo-EM Analyses Permit Visualization of Structural Polymorphism of Biological Macromolecules. Chang WH, Huang SH, Lin HH, Chung SC, Tu IP. Front Bioinform 1 788308 (2021)

Articles - 7l2t mentioned but not cited (2)

  1. Structural snapshots of TRPV1 reveal mechanism of polymodal functionality. Zhang K, Julius D, Cheng Y. Cell 184 5138-5150.e12 (2021)
  2. A step-by-step protocol for capturing conformational snapshots of ligand gated ion channels by single-particle cryo-EM. Zhang K, Julius D, Cheng Y. STAR Protoc 3 101732 (2022)


Reviews citing this publication (16)

  1. Druggable Lipid Binding Sites in Pentameric Ligand-Gated Ion Channels and Transient Receptor Potential Channels. Cheng WWL, Arcario MJ, Petroff JT. Front Physiol 12 798102 (2021)
  2. Ionic channels in nerve membranes, 50 years on. Hille B. Prog Biophys Mol Biol 169-170 12-20 (2022)
  3. Nobel somatosensations and pain. Reeh PW, Fischer MJM. Pflugers Arch 474 405-420 (2022)
  4. "ThermoTRP" Channel Expression in Cancers: Implications for Diagnosis and Prognosis (Practical Approach by a Pathologist). Szallasi A. Int J Mol Sci 24 9098 (2023)
  5. Carcinogenesis and Metastasis: Focus on TRPV1-Positive Neurons and Immune Cells. Erin N, Szallasi A. Biomolecules 13 983 (2023)
  6. Druggability of Voltage-Gated Sodium Channels-Exploring Old and New Drug Receptor Sites. Wisedchaisri G, Gamal El-Din TM. Front Pharmacol 13 858348 (2022)
  7. Inferiority complex: why do sensory ion channels multimerize? Gamper N, Shah S. Biochem Soc Trans 50 213-222 (2022)
  8. Mechanotransduction in the urothelium: ATP signalling and mechanoreceptors. Li X, Hu J, Yin P, Liu L, Chen Y. Heliyon 9 e19427 (2023)
  9. New Horizons in Structural Biology of Membrane Proteins: Experimental Evaluation of the Role of Conformational Dynamics and Intrinsic Flexibility. Puthenveetil R, Christenson ET, Vinogradova O. Membranes (Basel) 12 227 (2022)
  10. Progress in the Structural Basis of thermoTRP Channel Polymodal Gating. Fernández-Ballester G, Fernández-Carvajal A, Ferrer-Montiel A. Int J Mol Sci 24 743 (2023)
  11. Research focus and thematic trends of transient receptor potential vanilloid member 1 research: a bibliometric analysis of the global publications (1990-2023). Liu X, Zhang M, He C, Jia S, Xiang R, Xu Y, Zhao M. Naunyn Schmiedebergs Arch Pharmacol (2023)
  12. Sensory TRP Channels in Three Dimensions. Diver MM, Lin King JV, Julius D, Cheng Y. Annu Rev Biochem 91 629-649 (2022)
  13. Structural Plasticity of the Selectivity Filter in Cation Channels. Hendriks K, Öster C, Lange A. Front Physiol 12 792958 (2021)
  14. TRP (transient receptor potential) ion channel family: structures, biological functions and therapeutic interventions for diseases. Zhang M, Ma Y, Ye X, Zhang N, Pan L, Wang B. Signal Transduct Target Ther 8 261 (2023)
  15. TRP channels: a journey towards a molecular understanding of pain. Rosenbaum T, Morales-Lázaro SL, Islas LD. Nat Rev Neurosci 23 596-610 (2022)
  16. The interaction of TRPV1 and lipids: Insights into lipid metabolism. Abdalla SS, Harb AA, Almasri IM, Bustanji YK. Front Physiol 13 1066023 (2022)

Articles citing this publication (28)

  1. TRPV1, a novel biomarker associated with lung cancer via excluding immune infiltration. Gao R, Meng M, Zhou X, Yu M, Li Z, Li J, Wang X, Song Y, Wang H, He J. MedComm (2020) 3 e139 (2022)
  2. A pentameric TRPV3 channel with a dilated pore. Lansky S, Betancourt JM, Zhang J, Jiang Y, Kim ED, Paknejad N, Nimigean CM, Yuan P, Scheuring S. Nature 621 206-214 (2023)
  3. Applications of Cryo-EM in small molecule and biologics drug design. Lees JA, Dias JM, Han S. Biochem Soc Trans 49 2627-2638 (2021)
  4. Modulation of TRPV2 by endogenous and exogenous ligands: A computational study. Feng S, Pumroy RA, Protopopova AD, Moiseenkova-Bell VY, Im W. Protein Sci 32 e4490 (2023)
  5. Opening of capsaicin receptor TRPV1 is stabilized equally by its four subunits. Li S, Nguyen PT, Vu S, Yarov-Yarovoy V, Zheng J. J Biol Chem 299 104828 (2023)
  6. Structural basis of TRPV3 inhibition by an antagonist. Fan J, Hu L, Yue Z, Liao D, Guo F, Ke H, Jiang D, Yang Y, Lei X. Nat Chem Biol 19 81-90 (2023)
  7. Vanilloid-dependent TRPV1 opening trajectory from cryoEM ensemble analysis. Kwon DH, Zhang F, Fedor JG, Suo Y, Lee SY. Nat Commun 13 2874 (2022)
  8. Anti-Inflammatory Effect of Beta-Caryophyllene Mediated by the Involvement of TRPV1, BDNF and trkB in the Rat Cerebral Cortex after Hypoperfusion/Reperfusion. Serra MP, Boi M, Carta A, Murru E, Carta G, Banni S, Quartu M. Int J Mol Sci 23 3633 (2022)
  9. Cannabidiol sensitizes TRPV2 channels to activation by 2-APB. Gochman A, Tan XF, Bae C, Chen H, Swartz KJ, Jara-Oseguera A. Elife 12 e86166 (2023)
  10. Classifying liganded states in heterogeneous single-particle cryo-EM datasets. Arnold WR, Asarnow D, Cheng Y. Microscopy (Oxf) 71 i23-i29 (2022)
  11. Gating intermediates reveal inhibitory role of the voltage sensor in a cyclic nucleotide-modulated ion channel. Gao X, Schmidpeter PAM, Berka V, Durham RJ, Fan C, Jayaraman V, Nimigean CM. Nat Commun 13 6919 (2022)
  12. Genetically-encoded BRET probes shed light on ligand bias-induced variable ion selectivity in TRPV1 and P2X5/7. Chappe YL, Pierredon S, Joushomme A, Molle P, Garenne A, Canovi A, Barbeau S, Poulletier De Gannes F, Hurtier A, Lagroye I, Ducret T, Quignard JF, Compan V, Percherancier Y. Proc Natl Acad Sci U S A 119 e2205207119 (2022)
  13. Human TRPV1 structure and inhibition by the analgesic SB-366791. Neuberger A, Oda M, Nikolaev YA, Nadezhdin KD, Gracheva EO, Bagriantsev SN, Sobolevsky AI. Nat Commun 14 2451 (2023)
  14. In Silico Drug Repurposing Framework Predicts Repaglinide, Agomelatine and Protokylol as TRPV1 Modulators with Analgesic Activity. Andrei C, Mihai DP, Zanfirescu A, Nitulescu GM, Negres S. Pharmaceutics 14 2563 (2022)
  15. Molecular details of ruthenium red pore block in TRPV channels. Pumroy RA, De Jesús-Pérez JJ, Protopopova AD, Rocereta JA, Fluck EC, Fricke T, Lee BH, Rohacs T, Leffler A, Moiseenkova-Bell V. EMBO Rep (2024)
  16. Mutagenesis studies of TRPV1 subunit interfaces informed by genomic variant analysis. Mott TM, Ibarra JS, Kandula N, Senning EN. Biophys J 122 322-332 (2023)
  17. Pepper Fruit Extracts Show Anti-Proliferative Activity against Tumor Cells Altering Their NADPH-Generating Dehydrogenase and Catalase Profiles. Rodríguez-Ruiz M, Ramos MC, Campos MJ, Díaz-Sánchez I, Cautain B, Mackenzie TA, Vicente F, Corpas FJ, Palma JM. Antioxidants (Basel) 12 1461 (2023)
  18. Permeant cations modulate pore dynamics and gating of TRPV1 ion channels. García-Ávila M, Tello-Marmolejo J, Rosenbaum T, Islas LD. J Gen Physiol 156 e202313422 (2024)
  19. Structural Mechanism of Ionic Conductivity of the TRPV1 Channel. Trofimov YA, Minakov AS, Krylov NA, Efremov RG. Dokl Biochem Biophys 508 1-5 (2023)
  20. Structural and functional analysis of human pannexin 2 channel. He Z, Zhao Y, Rau MJ, Fitzpatrick JAJ, Sah R, Hu H, Yuan P. Nat Commun 14 1712 (2023)
  21. Structural insights into TRPV2 activation by small molecules. Pumroy RA, Protopopova AD, Fricke TC, Lange IU, Haug FM, Nguyen PT, Gallo PN, Sousa BB, Bernardes GJL, Yarov-Yarovoy V, Leffler A, Moiseenkova-Bell VY. Nat Commun 13 2334 (2022)
  22. Structural mechanisms of TRPV2 modulation by endogenous and exogenous ligands. Su N, Zhen W, Zhang H, Xu L, Jin Y, Chen X, Zhao C, Wang Q, Wang X, Li S, Wen H, Yang W, Guo J, Yang F. Nat Chem Biol 19 72-80 (2023)
  23. Structure of human TRPV4 in complex with GTPase RhoA. Nadezhdin KD, Talyzina IA, Parthasarathy A, Neuberger A, Zhang DX, Sobolevsky AI. Nat Commun 14 3733 (2023)
  24. TRPV1 and Piezo: the 2021 Nobel Prize in Physiology or Medicine. Cheng Y. IUCrJ 9 4-5 (2022)
  25. Temperature sensitive contact modes allosterically gate TRPV3. Burns D, Venditti V, Potoyan DA. PLoS Comput Biol 19 e1011545 (2023)
  26. The capsaicin binding affinity of wildtype and mutant TRPV1 ion channels. Li S, Zheng J. J Biol Chem 299 105268 (2023)
  27. The past and future of transient receptor potential: A scientometric analysis. Jiang N, Pan C, Zhang S, Cheng B, Dong C. Medicine (Baltimore) 101 e30317 (2022)
  28. The role of TRPV2 as a regulator on the osteoclast differentiation during orthodontic tooth movement in rats. Shigemi S, Sato T, Sakamoto M, Yajima T, Honda T, Tsumaki H, Deguchi T, Ichikawa H, Fukunaga T, Mizoguchi I. Sci Rep 13 13718 (2023)


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