Genetic code expansion, an emerging tool in the Ca
CRAC channels
Ca2+ ion channels
structure/function relationship
unnatural amino acids
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
02 May 2024
02 May 2024
Historique:
received:
18
01
2024
accepted:
15
04
2024
medline:
2
5
2024
pubmed:
2
5
2024
entrez:
2
5
2024
Statut:
aheadofprint
Résumé
Various methods for characterizing binding forces as well as for monitoring and remote control of ion channels are still emerging. A recent innovation is the direct incorporation of unnatural amino acids (UAAs) with corresponding biophysical or biochemical properties, which are integrated using genetic code expansion technology. Minimal changes to natural amino acids, which are achieved by chemical synthesis of corresponding UAAs, are valuable tools to provide insight into the contributions of physicochemical properties of side chains in binding events. To gain unique control over the conformational changes or function of ion channels, a series of light-sensitive, chemically reactive and posttranslationally modified UAAs have been developed and utilized. Here, we present the existing UAA tools, their mode of action, their potential and limitations as well as their previous applications to Ca
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Austrian Science Fund (FWF)
ID : FWF 32851
Organisme : Austrian Science Fund (FWF)
ID : FWF 35900
Organisme : Austrian Science Fund (FWF)
ID : FWF 36202
Informations de copyright
© 2024 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Ahern, C. A., Eastwood, A. L., Dougherty, D. A., & Horn, R. (2008). Electrostatic contributions of aromatic residues in the local anesthetic receptor of voltage‐gated sodium channels. Circulation Research, 102(1), 86–94.
Ahern, C. A., & Kobertz, W. R. (2009). Chemical tools for K + channel biology †. Biochemistry, 48(3), 517–526.
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., & Walter, P. (2002). Ion Channels and the Electrical Properties of Membranes (4th edn). Garland Science. https://www.ncbi.nlm.nih.gov/books/NBK26910/
Ambrogelly, A., Palioura, S., & Söll, D. (2007). Natural expansion of the genetic code. Nature Chemical Biology, 3(1), 29–35.
Aydin, Y., Böttke, T., Lam, J. H., Ernicke, S., Fortmann, A., Tretbar, M., Zarzycka, B., Gurevich, V. V., Katritch, V., & Coin, I. (2023). Structural details of a Class B GPCR‐arrestin complex revealed by genetically encoded crosslinkers in living cells. Nature Communications, 14(1), 1151.
Aydin, Y., & Coin, I. (2023). Genetically encoded crosslinkers to address protein–protein interactions. Protein Science, 32(5), e4637.
Banghart, M. R., Volgraf, M., & Trauner, D. (2006). Engineering light‐gated ion channels. Biochemistry, 45(51), 15129–15141.
Batool, M., Ahmad, B., & Choi, S. (2019). A structure‐based drug discovery paradigm. International Journal of Molecular Sciences, 20(11), 2783.
Beene, D. L., Brandt, G. S., Zhong, W., Zacharias, N. M., Lester, H. A., & Dougherty, D. A. (2002). Cation−π interactions in ligand recognition by serotonergic (5‐HT 3A) and nicotinic acetylcholine receptors: The anomalous binding properties of nicotine. Biochemistry, 41(32), 10262–10269.
Beene, D. L., Dougherty, D. A., & Lester, H. A. (2003). Unnatural amino acid mutagenesis in mapping ion channel function. Current Opinion in Neurobiology, 13(3), 264–270.
Beene, D. L., Price, K. L., Lester, H. A., Dougherty, D. A., & Lummis, S. C. R. (2004). Tyrosine residues that control binding and gating in the 5‐hydroxytryptamine 3 receptor revealed by unnatural amino acid mutagenesis. The Journal of Neuroscience, 24(41), 9097–9104.
Benemei, S., Patacchini, R., Trevisani, M., & Geppetti, P. (2015). TRP channels. Current Opinion in Pharmacology, 22, 18–23.
Berridge, M. J., Bootman, M. D., & Lipp, P. (1998). Calcium–a life and death signal. Nature, 395(6703), 645–648.
Berridge, M. J., Lipp, P., & Bootman, M. D. (2000). The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology, 1(1), 11–21.
Bianco, A., Townsley, F. M., Greiss, S., Lang, K., & Chin, J. W. (2012). Expanding the genetic code of Drosophila melanogaster. Nature Chemical Biology, 8(9), 748–750.
Böttke, T., Ernicke, S., Serfling, R., Ihling, C., Burda, E., Gurevich, V. V., Sinz, A., & Coin, I. (2020). Exploring GPCR‐arrestin interfaces with genetically encoded crosslinkers. European Molecular Biology Organization Reports, 21(11), e50437.
Brauchi, S., & Orio, P. (2011). Voltage sensing in thermo‐TRP channels. Advances in Experimental Medicine and Biology, 704, 517–530.
Brauchi, S. E., & Steinberg, X. P. (2021). Studying ion channel conformation dynamics by encoding coumarin as unnatural amino acid. Methods in Enzymology, 653, 239–266.
Braun, N., Lynagh, T., Yu, R., Biggin, P. C., & Pless, S. A. (2016). Role of an absolutely conserved tryptophan pair in the extracellular domain of cys‐loop receptors. Acute Coronary Syndrome Chemical Neuroscience, 7(3), 339–348.
Butorac, C., Krizova, A., & Derler, I. (2020). Review: Structure and activation mechanisms of CRAC channels. Advances in Experimental Medicine and Biology, 1131, 547–604.
Cao, E., Liao, M., Cheng, Y., & Julius, D. (2013). TRPV1 structures in distinct conformations reveal activation mechanisms. Nature, 504(7478), 113–118.
Cashin, A. L., Torrice, M. M., McMenimen, K. A., Lester, H. A., & Dougherty, D. A. (2007). Chemical‐scale studies on the role of a conserved aspartate in preorganizing the agonist binding site of the nicotinic acetylcholine receptor. Biochemistry, 46(3), 630–639.
Celie, P. H. N., van Rossum‐Fikkert, S. E., van Dijk, W. J., Brejc, K., Smit, A. B., & Sixma, T. K. (2004). Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron, 41(6), 907–914.
Chatterjee, A., Guo, J., Lee, H. S., & Schultz, P. G. (2013). A genetically encoded fluorescent probe in mammalian cells. Journal of the American Chemical Society, 135(34), 12540–12543.
Chen, Y., Ma, J., Lu, W., Tian, M., Thauvin, M., Yuan, C., Volovitch, M., Wang, Q., Holst, J., Liu, M., Vriz, S., Ye, S., Wang, L., & Li, D. (2017). Heritable expansion of the genetic code in mouse and zebrafish. Cell Research, 27(2), 294–297.
Chin, J. W. (2017). Expanding and reprogramming the genetic code. Nature, 550(7674), 53–60.
Coin, I. (2018). Application of non‐canonical crosslinking amino acids to study protein‐protein interactions in live cells. Current Opinion in Chemical Biology, 46, 156–163.
Coin, I., Katritch, V., Sun, T., Xiang, Z., Siu, F. Y., Beyermann, M., Stevens, R. C., & Wang, L. (2013). XGenetically encoded chemical probes in cells reveal the binding path of urocortin‐i to CRF class B GPCR. Cell, 155(6), 1258–1269.
Coin, I., Perrin, M. H., Vale, W. W., & Wang, L. (2011). Photo‐cross‐linkers incorporated into G‐protein‐coupled receptors in mammalian cells: A ligand comparison. Angewandte Chemie International Edition, 50(35), 8077–8081.
Creon, A., Josts, I., Niebling, S., Huse, N., & Tidow, H. (2018). Conformation‐specific detection of calmodulin binding using the unnatural amino acid p‐azido‐phenylalanine (AzF) as an IR‐sensor. Structural Dynamics, 5(6), 064701.
Dabrowski, M., Bukowy‐Bieryllo, Z., & Zietkiewicz, E. (2015). Translational readthrough potential of natural termination codons in eucaryotes – The impact of RNA sequence. Ribonucleic Acid Biology, 12(9), 950–958.
Dai, G., Aman, T. K., DiMaio, F., & Zagotta, W. N. (2019). The HCN channel voltage sensor undergoes a large downward motion during hyperpolarization. Nature Structural & Molecular Biology, 26(8), 686–694.
Deechongkit, S., Nguyen, H., Powers, E. T., Dawson, P. E., Gruebele, M., & Kelly, J. W. (2004). Context‐dependent contributions of backbone hydrogen bonding to β‐sheet folding energetics. Nature, 430(6995), 101–105.
Deisseroth, K. (2015). Optogenetics: 10 years of microbial opsins in neuroscience. Nature Neuroscience, 18(9), 1213–1225.
Dougherty, D. A., & Van Arnam, E. B. (2014). In vivo incorporation of non‐canonical amino acids by using the chemical aminoacylation strategy: A broadly applicable mechanistic tool. Chembiochem, 15(12), 1710–1720.
Elliott, A. C. (2001). Recent developments in non‐excitable cell calcium entry. Cell Calcium, 30(2), 73–93.
Ernst, R. J., Krogager, T. P., Maywood, E. S., Zanchi, R., Beránek, V., Elliott, T. S., Barry, N. P., Hastings, M. H., & Chin, J. W. (2016). Genetic code expansion in the mouse brain. Nature Chemical Biology, 12(10), 776–778.
Feske, S. (2019). CRAC channels and disease‐From human CRAC channelopathies and animal models to novel drugs. Cell Calcium, 80, 112–116.
Gees, M., Colsoul, B., & Nilius, B. (2010). The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harbor Perspectives in Biology, 2(10), a003962.
Greiss, S., & Chin, J. W. (2011). Expanding the genetic code of an animal. Journal of the American Chemical Society, 133(36), 14196–14199.
Han, S., Yang, A., Lee, S., Lee, H. W., Park, C. B., & Park, H. S. (2017). Expanding the genetic code of Mus musculus. Nature Communications, 8, 14568.
He, L., Wang, L., Zeng, H., Tan, P., Ma, G., Zheng, S., Li, Y., Sun, L., Dou, F., Siwko, S., Huang, Y., Wang, Y., & Zhou, Y. (2021). Engineering of a bona fide light‐operated calcium channel. Nature Communications, 12(1), 164.
He, L., Zhang, Q., Zhou, Y., & Huang, Y. (2017). Calcium entry channels in non‐excitable cells. In Taylor & Francis, 2017.| Series: Methods in signal transduction series (pp. 145–160). CRC Press.
Hille, B. (2001). Ion Channels of Excitable Membranes (3rd edn.) Sinauer Associates, Inc.
Hoppmann, C., Lacey, V. K., Louie, G. V., Wei, J., Noel, J. P., & Wang, L. (2014). Genetically encoding photoswitchable click amino acids in Escherichia coli and mammalian cells. Angewandte Chemie International Edition, 53(15), 3932–3936.
Hoppmann, C., Maslennikov, I., Choe, S., & Wang, L. (2015). In situ formation of an azo bridge on proteins controllable by visible light. Journal of the American Chemical Society, 137(35), 11218–11221.
Hoppmann, C., & Wang, L. (2019). Genetically encoding photoswitchable click amino acids for general optical control of conformation and function of proteins. Methods in Enzymology, 624, 249–264.
Horner, K. A., Valette, N. M., & Webb, M. E. (2015). Strain‐promoted reaction of 1,2,4‐triazines with bicyclononynes. Chemistry ‐ A European Journal, 21(41), 14376–14381.
Huang, Y., & Liu, T. (2018). Therapeutic applications of genetic code expansion. Synthetic and Systems Biotechnology, 3(3), 150–158.
Ishii, T., Sato, K., Kakumoto, T., Miura, S., Touhara, K., Takeuchi, S., & Nakata, T. (2015). Light generation of intracellular Ca(2+) signals by a genetically encoded protein BACCS. Nature Communications, 6, 8021.
Ismailov, I. I., & Benos, D. J. (1995). Effects of phosphorylation on ion channel function. Kidney International, 48(4), 1167–1179.
Joshi, J., Rubart, M., & Zhu, W. (2020). Optogenetics: Background, methodological advances and potential applications for cardiovascular research and medicine. Frontiers in Bioengineering and Biotechnology, 7, 466.
Kang, J.‐Y., Kawaguchi, D., Coin, I., Xiang, Z., O'Leary, D. D. M., Slesinger, P. A., & Wang, L. (2013). In vivo expression of a light‐activatable potassium channel using unnatural amino acids. Neuron, 80(2), 358–370.
Klippenstein, V., Ghisi, V., Wietstruk, M., & Plested, A. J. (2014). Photoinactivation of glutamate receptors by genetically encoded unnatural amino acids. Journal of Neuroscience, 34, 980–991.
Klippenstein, V., Hoppmann, C., Ye, S., Wang, L., & Paoletti, P. (2017). Optocontrol of glutamate receptor activity by single side‐chain photoisomerization. Elife, 6, e25808.
Klippenstein, V., Mony, L., & Paoletti, P. (2018). Probing ion channel structure and function using light‐sensitive amino acids. Trends in Biochemical Sciences, 43(6), 436–451.
Kobayashi, T., Hoppmann, C., Yang, B., & Wang, L. (2016). Using protein‐confined proximity to determine chemical reactivity. Journal of the American Chemical Society, 138(45), 14832–14835.
Koh, J. T., Cornish, V. W., & Schultz, P. G. (1997). An experimental approach to evaluating the role of backbone interactions in proteins using unnatural amino acid mutagenesis. Biochemistry, 36(38), 11314–11322.
Kyung, T., Lee, S., Kim, J. E., Cho, T., Park, H., Jeong, Y. M., Kim, D., Shin, A., Kim, S., Baek, J., Kim, J., Kim, N. Y., Woo, D., Chae, S., Kim, C. H., Shin, H. S., Han, Y. M., Kim, D., & Heo, W. D. (2015). Optogenetic control of endogenous Ca(2+) channels in vivo. Nature Biotechnology, 33(10), 1092–1096.
Lammers, M., Neumann, H., Chin, J. W., & James, L. C. (2010). Acetylation regulates Cyclophilin A catalysis, immunosuppression and HIV isomerization. Nature Chemical Biology, 6(5), 331–337.
Lang, K., & Chin, J. W. (2014). Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chemical Reviews, 114(9), 4764–4806.
Lee, H. S., Guo, J., Lemke, E. A., Dimla, R. D., & Schultz, P. G. (2009). Genetic incorporation of a small, environmentally sensitive, fluorescent probe into proteins in Saccharomyces cerevisiae. Journal of the American Chemical Society, 131(36), 12921–12923.
Lee, W. Y., & Sine, S. M. (2004). Invariant aspartic acid in muscle nicotinic receptor contributes selectively to the kinetics of agonist binding. Journal of General Physiology, 124(5), 555–567.
Leisle, L., Valiyaveetil, F., Mehl, R. A., & Ahern, C. A. (2015). Incorporation of non‐canonical amino acids. Advances in Experimental Medicine and Biology, 869, 119–151.
Lemke, E. A., Summerer, D., Geierstanger, B. H., Brittain, S. M., & Schultz, P. G. (2007). Control of protein phosphorylation with a genetically encoded photocaged amino acid. Nature Chemical Biology, 3(12), 769–772.
Levitan, I. B. (1994). Modulation of ION channels by protein phosphorylation and dephosphorylation. Annual Review of Physiology, 56, 193–212.
Liao, Y., Plummer, N. W., George, M. D., Abramowitz, J., Zhu, M. X., & Birnbaumer, L. (2009). A role for Orai in TRPC‐mediated Ca2+ entry suggests that a TRPC: Orai complex may mediate store and receptor operated Ca2+ entry. Proceedings of the National Academy of Sciences, 106(9), 3202–3206.
Luo, J., Torres‐Kolbus, J., Liu, J., & Deiters, A. (2017). Genetic encoding of photocaged tyrosines with improved light‐activation properties for the optical control of protease function. Chembiochem, 18(14), 1442–1447.
Luo, L., Wang, Y., Li, B., Xu, L., Kamau, P. M., Zheng, J., Yang, F., Yang, S., & Lai, R. (2019). Molecular basis for heat desensitization of TRPV1 ion channels. Nature Communications, 10(1), 2134.
Ma, G., He, L., Liu, S., Xie, J., Huang, Z., Jing, J., Lee, Y. T., Wang, R., Luo, H., Han, W., Huang, Y., & Zhou, Y. (2020). Optogenetic engineering to probe the molecular choreography of STIM1‐mediated cell signaling. Nature Communications, 11(1), 1039.
Ma, G., Liu, J., Ke, Y., Liu, X., Li, M., Wang, F., Han, G., Huang, Y., Wang, Y., & Zhou, Y. (2018). Optogenetic control of voltage‐gated calcium channels. Angewandte Chemie (International ed in English), 57(24), 7019–7022.
Ma, G., Wei, M., He, L., Liu, C., Wu, B., Zhang, S. L., Jing, J., Liang, X., Senes, A., Tan, P., Li, S., Sun, A., Bi, Y., Zhong, L., Si, H., Shen, Y., Li, M., Lee, M. S., Zhou, W., … Zhou, Y. (2015). Inside‐out Ca(2+) signalling prompted by STIM1 conformational switch. Nature Communications, 6, 7826.
Maltan, L., Weiß, S., Najjar, H., Leopold, M., Lindinger, S., Höglinger, C., Höbarth, L., Sallinger, M., Grabmayr, H., Berlansky, S., Krivic, D., Hopl, V., Blaimschein, A., Fahrner, M., Frischauf, I., Tiffner, A., & Derler I. (2023). Photocrosslinking‐induced CRAC channel‐like Orai1 activation independent of STIM1. Nature Communications, 14(1), 1286.
Miller, J. C., Silverman, S. K., England, P. M., Dougherty, D. A., & Lester, H. A. (1998). Flash decaging of tyrosine sidechains in an ion channel. Neuron, 20(4), 619–624.
Neumann, H. (2012). Rewiring translation ‐ Genetic code expansion and its applications. Federation of European Biochemical Societies Letters, 586(15), 2057–2064.
Neumann, H., Hancock, S. M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen‐Hughes, T., van Noort, J., Rhodes, D., & Chin, J. W. (2009). A method for genetically installing site‐specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Molecular Cell, 36(1), 153–163.
Neumann, H., Peak‐Chew, S. Y., & Chin, J. W. (2008). Genetically encoding Nε‐acetyllysine in recombinant proteins. Nature Chemical Biology, 4(4), 232–234.
Neumann, H., Wang, K., Davis, L., Garcia‐Alai, M., & Chin, J. W. (2010). Encoding multiple unnatural amino acids via evolution of a quadruplet‐decoding ribosome. Nature, 464(7287), 441–444.
Neumann‐Staubitz, P., & Neumann, H. (2016). The use of unnatural amino acids to study and engineer protein function. Current Opinion in Structural Biology, 38, 119–128.
Nguyen, N. T., He, L., Martinez‐Moczygemba, M., Huang, Y., & Zhou, Y. (2018). Rewiring calcium signaling for precise transcriptional reprogramming. Acute Coronary Syndrome Synthetic Biology, 7(3), 814–821.
Nikić‐Spiegel, I. (2020). Expanding the genetic code for neuronal studies. Chembiochem, 21(22), 3169–3179.
Nilius, B., Owsianik, G., Voets, T., & Peters, J. A. (2007). Transient receptor potential cation channels in disease. Physiological Reviews, 87(1), 165–217.
Nodling, A. R., Spear, L. A., Williams, T. L., Luk, L. Y. P., & Tsai, Y. H. (2019). Using genetically incorporated unnatural amino acids to control protein functions in mammalian cells. Essays in Biochemistry, 63(2), 237–266.
Ong, H. L., de Souza, L. B., & Ambudkar, I. S. (2016). Role of TRPC channels in store‐operated calcium entry. Advances in Experimental Medicine and Biology, 898, 87–109.
Pankratov, Y., & Lalo, U. (2014). Calcium permeability of ligand‐gated Ca2+ channels. European Journal of Pharmacology, 739, 60–73.
Paulsen, C. E., Armache, J.‐P., Gao, Y., Cheng, Y., & Julius, D. (2015). Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature, 520(7548), 511–517.
Philipson, K. D., Gallivan, J. P., Brandt, G. S., Dougherty, D. A., & Lester, H. A. (2001). Incorporation of caged cysteine and caged tyrosine into a transmembrane segment of the nicotinic ACh receptor. American Journal of Physiology‐Cell Physiology, 281(1), C195–C206.
Pinzi, L., & Rastelli, G. (2019). Molecular docking: Shifting paradigms in drug discovery. International Journal of Molecular Sciences, 20(18), 4331.
Plass, T., Milles, S., Koehler, C., Schultz, C., & Lemke, E. A. (2011). Genetically encoded copper‐free click chemistry. Angewandte Chemie‐International Edition, 50(17), 3878–3881.
Pless, S. A., Kim, R. Y., Ahern, C. A., & Kurata, H. T. (2015). Atom‐by‐atom engineering of voltage‐gated ion channels: Magnified insights into function and pharmacology. The Journal of Physiology, 593(12), 2627–2634.
Plested, A. J. R., & Poulsen, M. H. (2021). Crosslinking glutamate receptor ion channels. Methods in Enzymology, 652, 161–192.
Poulsen, M. H., Poshtiban, A., Klippenstein, V., Ghisi, V., & Plested, A. J. R. (2019). Gating modules of the AMPA receptor pore domain revealed by unnatural amino acid mutagenesis. Proceedings of the National Academy of Sciences, 116(27), 13358–13367.
Prakriya, M., & Lewis, R. S. (2015). Store‐operated calcium channels. Physiological Reviews, 95(4), 1383–1436.
Puljung, M. C. (2021). ANAP: A versatile, fluorescent probe of ion channel gating and regulation. Methods in Enzymology, 654, 49–84.
Salido, G. M., Sage, S. O., & Rosado, J. A. (2009). TRPC channels and store‐operated Ca(2+) entry. Biochimica Et Biophysica Acta, 1793(2), 223–230.
Sallinger, M., Grabmayr, H., Humer, C., Bonhenry, D., Romanin, C., Schindl, R., & Derler, I. (2023). Activation mechanisms and structural dynamics of STIM proteins. The Journal of Physiology. 602(8), 1475–1507.
Santarelli, V. P., Eastwood, A. L., Dougherty, D. A., Horn, R., & Ahern, C. A. (2007). A cation‐interaction discriminates among sodium channels that are either sensitive or resistant to tetrodotoxin block *. Journal of Biological Chemistry, 282(11), 8044–8051.
Schmied, W. H., Elsässer, S. J., Uttamapinant, C., & Chin, J. W. (2014). Efficient multisite unnatural amino acid incorporation in mammalian cells via optimized pyrrolysyl tRNA synthetase/tRNA expression and engineered eRF1. Journal of the American Chemical Society, 136(44), 15577–15583.
Schrank, S., Barrington, N., & Stutzmann, G. E. (2020). Calcium‐handling defects and neurodegenerative disease. Cold Spring Harbor perspectives in biology, 12(7), a035212.
Serfling, R., Lorenz, C., Etzel, M., Schicht, G., Böttke, T., Mörl, M., & Coin, I. (2018). Designer tRNAs for efficient incorporation of non‐canonical amino acids by the pyrrolysine system in mammalian cells. Nucleic Acids Research, 46(1), 1–10.
Shen, B., Xiang, Z., Miller, B., Louie, G., Wang, W., Noel, J. P., Gage, F. H., & Wang, L. (2011). Genetically encoding unnatural amino acids in neural stem cells and optically reporting voltage‐sensitive domain changes in differentiated neurons. Stem Cells, 29(8), 1231–1240.
Spagnuolo, G., Genovese, F., Fortunato, L., Simeone, M., Rengo, C., & Tatullo, M. (2019). The impact of optogenetics on regenerative medicine. Applied Sciences, 10(1), 173.
Steinberg, X., Kasimova, M. A., Cabezas‐Bratesco, D., Galpin, J. D., Ladron‐de‐Guevara, E., Villa, F., Carnevale, V., Islas, L., Ahern, C. A., & Brauchi, S. E. (2017). Conformational dynamics in TRPV1 channels reported by an encoded coumarin amino acid. Elife, 6, e28626.
Subramanyam, P., & Colecraft, H. M. (2014). Ion channel engineering: Perspectives and strategies. Journal of Molecular Biology, 427(1), 190–204.
Summerer, D., Chen, S., Wu, N., Deiters, A., Chin, J. W., & Schultz, P. G. (2006). A genetically encoded fluorescent amino acid. Proceedings of the National Academy of Sciences, 103(26), 9785–9789.
Sun, M.‐Y., Zhang, X., Yu, P.‐C., Liu, D., Yang, Y., Cui, W.‐W., Yang, X.‐N., Lei, Y.‐T., Li, X.‐H., Wang, W.‐H., Cao, P., Wang, H.‐S., Zhu, M. X., Li, C.‐Z., Wang, R., Fan, Y.‐Z., & Yu, Y. (2022). Vanilloid agonist‐mediated activation of TRPV1 channels requires coordinated movement of the S1–S4 bundle rather than a quiescent state. Science Bulletin (Beijing), 67(10), 1062–1076.
Tian, M., & Ye, S. (2017). Design of light‐sensitive NMDARs by genetically encoded photo‐cross‐linkers. Methods in Molecular Biology (Clifton, NJ), 1677, 185–197.
Tiffner, A., & Derler, I. (2021). Isoform‐specific properties of orai homologues in activation, downstream signaling, physiology and pathophysiology. International Journal of Molecular Sciences, 22(15), 8020.
Tiffner, A., Maltan, L., Fahrner, M., Sallinger, M., Weiss, S., Grabmayr, H., Hoglinger, C., & Derler, I. (2021). Transmembrane domain 3 (TM3) Governs Orai1 and Orai3 pore opening in an isoform‐specific manner. Frontiers in Cell and Developmental Biology, 9, 635705.
Tiffner, A., Maltan, L., Weiss, S., & Derler, I. (2021). The orai pore opening mechanism. International Journal of Molecular Sciences, 22(2), 533.
Tiffner, A., Schober, R., Höglinger, C., Bonhenry, D., Pandey, S., Lunz, V., Sallinger, M., Frischauf, I., Fahrner, M., Lindinger, S., Maltan, L., Berlansky, S., Stadlbauer, M., Schindl, R., Ettrich, R., Romanin, C., & Derler, I. (2020). A series of Orai1 gating checkpoints in transmembrane and cytosolic regions requires clearance for CRAC channel opening. https://doi.org/10.1101/2020.07.16.207183
Van Arnam, E. B., & Dougherty, D. A. (2014). Functional probes of drug‐receptor interactions implicated by structural studies: Cys‐loop receptors provide a fertile testing ground. Journal of Medicinal Chemistry, 57(15), 6289–6300.
Wagner, B. (2009). The use of coumarins as environmentally‐sensitive fluorescent probes of heterogeneous inclusion systems. Molecules (Basel, Switzerland), 14(1), 210–237.
Walker, O. S., Elsässer, S. J., Mahesh, M., Bachman, M., Balasubramanian, S., & Chin, J. W. (2016). Photoactivation of mutant isocitrate dehydrogenase 2 reveals rapid cancer‐associated metabolic and epigenetic changes. Journal of the American Chemical Society, 138(3), 718–721.
Wang, J., Xie, J., & Schultz, P. G. (2006a). A genetically encoded fluorescent amino acid. Journal of the American Chemical Society, 128(27), 8738–8739.
Wang, L., Xie, J., & Schultz, P. G. (2006b). Expanding the genetic code. Annual Review of Biophysics and Biomolecular Structure, 35, 225–249.
Wang, W., Takimoto, J. K., Louie, G. V., Baiga, T. J., Noel, J. P., Lee, K.‐F., Slesinger, P. A., & Wang, L. (2007). Genetically encoding unnatural amino acids for cellular and neuronal studies. Nature Neuroscience, 10(8), 1063–1072.
Worley, P. F., Zeng, W., Huang, G. N., Yuan, J. P., Kim, J. Y., Lee, M. G., & Muallem, S. (2007). TRPC channels as STIM1‐regulated store‐operated channels. Cell Calcium, 42(2), 205–211.
Xiang, Z., Ren, H., Hu, Y. S., Coin, I., Wei, J., Cang, H., & Wang, L. (2013). Adding an unnatural covalent bond to proteins through proximity‐enhanced bioreactivity. Nature Methods, 10(9), 885–888.
Xiu, X., Puskar, N. L., Shanata, J. A. P., Lester, H. A., & Dougherty, D. A. (2009). Nicotine binding to brain receptors requires a strong cation–π interaction. Nature, 458(7237), 534–537.
Xu, L., Han, Y., Chen, X., Aierken, A., Wen, H., Zheng, W., Wang, H., Lu, X., Zhao, Z., Ma, C., Liang, P., Yang, W., Yang, S., & Yang, F. (2020). Molecular mechanisms underlying menthol binding and activation of TRPM8 ion channel. Nature Communications, 11(1), 3790.
Yang, F., Xiao, X., Lee, B. H., Vu, S., Yang, W., Yarov‐Yarovoy, V., & Zheng, J. (2018). The conformational wave in capsaicin activation of transient receptor potential vanilloid 1 ion channel. Nature Communications, 9(1), 2879.
Yang, S., Lu, X., Wang, Y., Xu, L., Chen, X., Yang, F., & Lai, R. (2020). A paradigm of thermal adaptation in penguins and elephants by tuning cold activation in TRPM8. Proceedings of the National Academy of Sciences, 117(15), 8633–8638.
Ye, S., Huber, T., Vogel, R., & Sakmar, T. P. (2009). FTIR analysis of GPCR activation using azido probes. Nature Chemical Biology, 5(6), 397–399.
Ye, S., Zaitseva, E., Caltabiano, G., Schertler, G. F. X., Sakmar, T. P., Deupi, X., & Vogel, R. (2010). Tracking G‐protein‐coupled receptor activation using genetically encoded infrared probes. Nature, 464(7293), 1386–1389.
Zagotta, W. N., Gordon, M. T., Senning, E. N., Munari, M. A., & Gordon, S. E. (2016). Measuring distances between TRPV1 and the plasma membrane using a noncanonical amino acid and transition metal ion FRET. Journal of General Physiology, 147(2), 201–216.
Zheng, Y., Lewis, T. L., Igo, P., Polleux, F., & Chatterjee, A. (2017). Virus‐enabled optimization and delivery of the genetic machinery for efficient unnatural amino acid mutagenesis in mammalian cells and tissues. Acute Coronary Syndrome Synthetic Biology, 6(1), 13–18.
Zhu, S., Riou, M., Yao, C. A., Carvalho, S., Rodriguez, P. C., Bensaude, O., Paoletti, P., & Ye, S. (2014). Genetically encoding a light switch in an ionotropic glutamate receptor reveals subunit‐specific interfaces. Proceedings of the National Academy of Sciences, 111(16), 6081–6086.