Modulation of potassium channels by transmembrane auxiliary subunits via voltage-sensing domains.
KCNQ1
KV
Slo1
auxiliary subunits
cryo-EM
potassium channels
Journal
Physiological reports
ISSN: 2051-817X
Titre abrégé: Physiol Rep
Pays: United States
ID NLM: 101607800
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
revised:
07
03
2024
received:
29
12
2023
accepted:
07
03
2024
medline:
20
3
2024
pubmed:
20
3
2024
entrez:
19
3
2024
Statut:
ppublish
Résumé
Voltage-gated K
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e15980Subventions
Organisme : Japan Society for the Promotion of Science (JSPS)
ID : 21K06786
Informations de copyright
© 2024 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.
Références
Abbott, G. W., Butler, M. H., Bendahhou, S., Dalakas, M. C., Ptacek, L. J., & Goldstein, S. A. (2001). MiRP2 forms potassium channels in skeletal muscle with Kv3.4 and is associated with periodic paralysis. Cell, 104, 217-231.
Abbott, G. W., & Goldstein, S. A. (1998). A superfamily of small potassium channel subunits: Form and function of the MinK-related peptides (MiRPs). Quarterly Reviews of Biophysics, 31, 357-398.
Abbott, G. W., Sesti, F., Splawski, I., Buck, M. E., Lehmann, M. H., Timothy, K. W., Keating, M. T., & Goldstein, S. A. (1999). MiRP1 forms IKr potassium channels with HERG and is associated with cardiac arrhythmia. Cell, 97, 175-187.
Adelman, J. P., Shen, K. Z., Kavanaugh, M. P., Warren, R. A., Wu, Y. N., Lagrutta, A., Bond, C. T., & North, R. A. (1992). Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron, 9, 209-216.
An, W. F., Bowlby, M. R., Betty, M., Cao, J., Ling, H. P., Mendoza, G., Hinson, J. W., Mattsson, K. I., Strassle, B. W., Trimmer, J. S., & Rhodes, K. J. (2000). Modulation of A-type potassium channels by a family of calcium sensors. Nature, 403, 553-556.
Angelo, K., Jespersen, T., Grunnet, M., Nielsen, M. S., Klaerke, D. A., & Olesen, S.-P. (2002). KCNE5 induces time- and voltage-dependent modulation of the KCNQ1 current. Biophysical Journal, 83, 1997-2006.
Barhanin, J., Lesage, F., Guillemare, E., Fink, M., Lazdunski, M., & Romey, G. (1996). K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature, 384, 78-80.
Barro-Soria, R., Rebolledo, S., Liin, S. I., Perez, M. E., Sampson, K. J., Kass, R. S., & Larsson, H. P. (2014). KCNE1 divides the voltage sensor movement in KCNQ1/KCNE1 channels into two steps. Nature Communications, 5, 3750.
Bezerra, G. A., Dobrovetsky, E., Seitova, A., Fedosyuk, S., Dhe-Paganon, S., & Gruber, K. (2015). Structure of human dipeptidyl peptidase 10 (DPPY): A modulator of neuronal Kv4 channels. Scientific Reports, 5, 8769.
Bolton, T. B., & Imaizumi, Y. (1996). Spontaneous transient outward currents in smooth muscle cells. Cell Calcium, 20, 141-152.
Butler, A., Tsunoda, S., McCobb, D. P., Wei, A., & Salkoff, L. (1993). mSlo, a complex mouse gene encoding “maxi” calcium-activated potassium channels. Science, 261, 221-224.
Butler, A., Wei, A. G., Baker, K., & Salkoff, L. (1989). A family of putative potassium channel genes in Drosophila. Science, 243, 943-947.
Chen, G., Li, Q., & Yan, J. (2022). The leucine-rich repeat domains of BK channel auxiliary γ subunits regulate their expression, trafficking, and channel-modulation functions. Journal of Biological Chemistry, 298, 101664.
Connor, J. A., & Stevens, C. F. (1971). Voltage clamp studies of a transient outward membrane current in gastropod neural somata. The Journal of Physiology, 213, 21-30.
Dougherty, K., de Santiago-Castillo, J. A., & Covarrubias, M. (2008). Gating charge immobilization in Kv4.2 channels: The basis of closed-state inactivation. The Journal of General Physiology, 131, 257-273.
Dudem, S., Boon, P. X., Mullins, N., McClafferty, H., Shipston, M. J., Wilkinson, R. D. A., Lobb, I., Sergeant, G. P., Thornbury, K. D., Tikhonova, I. G., & Hollywood, M. A. (2023). Oxidation modulates LINGO2-induced inactivation of large conductance, Ca2+-activated potassium channels. The Journal of Biological Chemistry, 299, 102975.
Dudem, S., Large, R. J., Kulkarni, S., McClafferty, H., Tikhonova, I. G., Sergeant, G. P., Thornbury, K. D., Shipston, M. J., Perrino, B. A., & Hollywood, M. A. (2020). LINGO1 is a regulatory subunit of large conductance, Ca2+-activated potassium channels. Proceedings of the National Academy of Sciences of the United States of America, 117, 2194-2200.
Fedida, D., & Giles, W. R. (1991). Regional variations in action potentials and transient outward current in myocytes isolated from rabbit left ventricle. The Journal of Physiology, 442, 191-209.
Foeger, N. C., Norris, A. J., Wren, L. M., & Nerbonne, J. M. (2012). Augmentation of Kv4.2-encoded currents by accessory dipeptidyl peptidase 6 and 10 subunits reflects selective cell surface Kv4.2 protein stabilization. The Journal of Biological Chemistry, 287, 9640-9650.
Gonzalez-Perez, V., Xia, X.-M., & Lingle, C. J. (2014). Functional regulation of BK potassium channels by γ1 auxiliary subunits. Proceedings of the National Academy of Sciences of the United States of America, 111, 4868-4873.
Grunnet, M., Jespersen, T., Rasmussen, H. B., Ljungstrøm, T., Jorgensen, N. K., Olesen, S.-P., & Klaerke, D. A. (2002). KCNE4 is an inhibitory subunit to the KCNQ1 channel. The Journal of Physiology, 542, 119-130.
Gruslova, A., Semenov, I., & Wang, B. (2012). An extracellular domain of the accessory β1 subunit is required for modulating BK channel voltage sensor and gate. The Journal of General Physiology, 139, 57-67.
Hagiwara, S., Kusano, K., & Saito, N. (1961). Membrane changes of Onchidium nerve cell in potassium-rich media. The Journal of Physiology, 155, 470-489.
Hite, R. K., Tao, X., & MacKinnon, R. (2017). Structural basis for gating the high-conductance Ca2+-activated K+ channel. Nature, 541, 52-57.
Hou, P., Eldstrom, J., Shi, J., Zhong, L., McFarland, K., Gao, Y., Fedida, D., & Cui, J. (2017). Inactivation of KCNQ1 potassium channels reveals dynamic coupling between voltage sensing and pore opening. Nature Communications, 8, 1730.
Jerng, H. H., Qian, Y., & Pfaffinger, P. J. (2004). Modulation of Kv4.2 channel expression and gating by dipeptidyl peptidase 10 (DPP10). Biophysical Journal, 87, 2380-2396.
Jost, N., Papp, J. G., & Varró, A. (2007). Slow delayed rectifier potassium current (IKs) and the repolarization reserve. Annals of Noninvasive Electrocardiology, 12, 64-78.
Kallure, G. S., Pal, K., Zhou, Y., Lingle, C. J., & Chowdhury, S. (2023). High-resolution structures illuminate key principles underlying voltage and LRRC26 regulation of Slo1 channels. bioRxiv. https://doi.org/10.1101/2023.12.20.572542v1
Kang, C., Tian, C., Sönnichsen, F. D., Smith, J. A., Meiler, J., George, A. L., Jr., Vanoye, C. G., Kim, H. J., & Sanders, C. R. (2008). Structure of KCNE1 and implications for how it modulates the KCNQ1 potassium channel. Biochemistry, 47, 7999-8006.
Kasuya, G., & Nakajo, K. (2022). Optimized tight binding between the S1 segment and KCNE3 is required for the constitutively open nature of the KCNQ1-KCNE3 channel complex. eLife, 11, e81683.
Kise, Y., Kasuya, G., Okamoto, H. H., Yamanouchi, D., Kobayashi, K., Kusakizako, T., Nishizawa, T., Nakajo, K., & Nureki, O. (2021). Structural basis of gating modulation of Kv4 channel complexes. Nature, 599, 158-164.
Kitazawa, M., Kubo, Y., & Nakajo, K. (2014). The stoichiometry and biophysical properties of the Kv4 potassium channel complex with K+ channel-interacting protein (KChIP) subunits are variable, depending on the relative expression level. The Journal of Biological Chemistry, 289, 17597-17609.
Kitazawa, M., Kubo, Y., & Nakajo, K. (2015). Kv4.2 and accessory dipeptidyl peptidase-like protein 10 (DPP10) subunit preferentially form a 4:2 (Kv4.2:DPP10) channel complex. The Journal of Biological Chemistry, 290, 22724-22733.
Larsson, H. P., Baker, O. S., Dhillon, D. S., & Isacoff, E. Y. (1996). Transmembrane movement of the shaker K+ channel S4. Neuron, 16, 387-397.
Lin, L., Long, L. K., Hatch, M. M., & Hoffman, D. A. (2014). DPP6 domains responsible for its localization and function. The Journal of Biological Chemistry, 289, 32153-32165.
Lundquist, A. L., Manderfield, L. J., Vanoye, C. G., Rogers, C. S., Donahue, B. S., Chang, P. A., Drinkwater, D. C., Murray, K. T., & George, A. L., Jr. (2005). Expression of multiple KCNE genes in human heart may enable variable modulation of I(Ks). Journal of Molecular and Cellular Cardiology, 38, 277-287.
Ma, D., Zhao, C., Wang, X., Li, X., Zha, Y., Zhang, Y., Fu, G., Liang, P., Guo, J., & Lai, D. (2022). Structural basis for the gating modulation of Kv4.3 by auxiliary subunits. Cell Research, 32, 411-414.
Melman, Y. F., Domènech, A., de la Luna, S., & McDonald, T. V. (2001). Structural determinants of KvLQT1 control by the KCNE family of proteins. The Journal of Biological Chemistry, 276, 6439-6444.
Melman, Y. F., Krumerman, A., & McDonald, T. V. (2002). A single transmembrane site in the KCNE-encoded proteins controls the specificity of KvLQT1 channel gating. The Journal of Biological Chemistry, 277, 25187-25194.
Melman, Y. F., Um, S. Y., Krumerman, A., Kagan, A., & McDonald, T. V. (2004). KCNE1 binds to the KCNQ1 pore to regulate potassium channel activity. Neuron, 42, 927-937.
Murray, C. I., Westhoff, M., Eldstrom, J., Thompson, E., Emes, R., & Fedida, D. (2016). Unnatural amino acid photo-crosslinking of the IKs channel complex demonstrates a KCNE1:KCNQ1 stoichiometry of up to 4:4. eLife, 5, e11815.
Nadal, M. S., Ozaita, A., Amarillo, Y., Vega-Saenz de Miera, E., Ma, Y., Mo, W., Goldberg, E. M., Misumi, Y., Ikehara, Y., Neubert, T. A., & Rudy, B. (2003). The CD26-related dipeptidyl aminopeptidase-like protein DPPX is a critical component of neuronal A-type K+ channels. Neuron, 37, 449-461.
Nakajima, S. (1966). Analysis of K inactivation and TEA action in the supramedullary cells of puffer. The Journal of General Physiology, 49, 629-640.
Nakajo, K., & Kubo, Y. (2007). KCNE1 and KCNE3 stabilize and/or slow voltage sensing S4 segment of KCNQ1 channel. The Journal of General Physiology, 130, 269-281.
Nakajo, K., Nishino, A., Okamura, Y., & Kubo, Y. (2011). KCNQ1 subdomains involved in KCNE modulation revealed by an invertebrate KCNQ1 orthologue. The Journal of General Physiology, 138, 521-535.
Nakajo, K., Ulbrich, M. H., Kubo, Y., & Isacoff, E. Y. (2010). Stoichiometry of the KCNQ1-KCNE1 ion channel complex. Proceedings of the National Academy of Sciences of the United States of America, 107, 18862-18867.
Orio, P., Rojas, P., Ferreira, G., & Latorre, R. (2002). New disguises for an old channel: MaxiK channel β-subunits. Physiology, 17, 156-161.
Osteen, J. D., Gonzalez, C., Sampson, K. J., Iyer, V., Rebolledo, S., Larsson, H. P., & Kass, R. S. (2010). KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proceedings of the National Academy of Sciences of the United States of America, 107, 22710-22715.
Pallotta, B. S., Magleby, K. L., & Barrett, J. N. (1981). Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature, 293, 471-474.
Panaghie, G., Tai, K.-K., & Abbott, G. W. (2006). Interaction of KCNE subunits with the KCNQ1 K+ channel pore. The Journal of Physiology, 570, 455-467.
Pioletti, M., Findeisen, F., Hura, G. L., & Minor, D. L., Jr. (2006). Three-dimensional structure of the KChIP1-Kv4.3 T1 complex reveals a cross-shaped octamer. Nature Structural & Molecular Biology, 13, 987-995.
Redhardt, M., Raunser, S., & Raisch, T. (2023). Cryo-EM structure of Slo1 with the auxiliary γ1 subunit suggests mechanism of depolarization-independent activation. bioRxiv. https://doi.org/10.1101/2023.11.01.565197v1.article-info
Rocheleau, J. M., & Kobertz, W. R. (2008). KCNE peptides differently affect voltage sensor equilibrium and equilibration rates in KCNQ1 K+ channels. The Journal of General Physiology, 131, 59-68.
Sanguinetti, M. C., Curran, M. E., Zou, A., Shen, J., Spector, P. S., Atkinson, D. L., & Keating, M. T. (1996). Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature, 384, 80-83.
Schroeder, B. C., Waldegger, S., Fehr, S., Bleich, M., Warth, R., Greger, R., & Jentsch, T. J. (2000). A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature, 403, 196-199.
Shao, L. R., Halvorsrud, R., Borg-Graham, L., & Storm, J. F. (1999). The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. The Journal of Physiology, 521(Pt 1), 135-146.
Shi, J., & Cui, J. (2001). Intracellular Mg2+ enhances the function of BK-type Ca2+-activated K+ channels. The Journal of General Physiology, 118, 589-606.
Shi, J., Krishnamoorthy, G., Yang, Y., Hu, L., Chaturvedi, N., Harilal, D., Qin, J., & Cui, J. (2002). Mechanism of magnesium activation of calcium-activated potassium channels. Nature, 418, 876-880.
Strop, P., Bankovich, A. J., Hansen, K. C., Garcia, K. C., & Brunger, A. T. (2004). Structure of a human A-type potassium channel interacting protein DPPX, a member of the dipeptidyl aminopeptidase family. Journal of Molecular Biology, 343, 1055-1065.
Sun, J., & MacKinnon, R. (2017). Cryo-EM structure of a KCNQ1/CaM complex reveals insights into congenital long QT syndrome. Cell, 169, 1042-1050.e9.
Sun, J., & MacKinnon, R. (2020). Structural basis of human KCNQ1 modulation and gating. Cell, 180, 340-347.e9.
Takumi, T., Ohkubo, H., & Nakanishi, S. (1988). Cloning of a membrane protein that induces a slow voltage-gated potassium current. Science, 242, 1042-1045.
Tao, X., Hite, R. K., & MacKinnon, R. (2017). Cryo-EM structure of the open high-conductance Ca2+-activated K+ channel. Nature, 541, 46-51.
Tao, X., & MacKinnon, R. (2019). Molecular structures of the human Slo1 K+ channel in complex with β4. eLife, 8, e51409.
Taylor, K. C., Kang, P. W., Hou, P., Yang, N.-D., Kuenze, G., Smith, J. A., Shi, J., Huang, H., White, K. M., Peng, D., George, A. L., Meiler, J., McFeeters, R. L., Cui, J., & Sanders, C. R. (2020). Structure and physiological function of the human KCNQ1 channel voltage sensor intermediate state. eLife, 9, e53901.
Wang, H., Yan, Y., Liu, Q., Huang, Y., Shen, Y., Chen, L., Chen, Y., Yang, Q., Hao, Q., Wang, K., & Chai, J. (2007). Structural basis for modulation of Kv4 K+ channels by auxiliary KChIP subunits. Nature Neuroscience, 10, 32-39.
Wang, N., Dries, E., Fowler, E. D., Harmer, S. C., Hancox, J. C., & Cannell, M. B. (2022). Inducing Ito, f and phase 1 repolarization of the cardiac action potential with a Kv4.3/KChIP2.1 bicistronic transgene. Journal of Molecular and Cellular Cardiology, 164, 29-41.
Wang, Q., Curran, M. E., Splawski, I., Burn, T. C., Millholland, J. M., VanRaay, T. J., Shen, J., Timothy, K. W., Vincent, G. M., de Jager, T., Schwartz, P. J., Toubin, J. A., Moss, A. J., Atkinson, D. L., Landes, G. M., Connors, T. D., & Keating, M. T. (1996). Positional cloning of a novel potassium channel gene: KVLQT1 mutations cause cardiac arrhythmias. Nature Genetics, 12, 17-23.
Wei, A., Covarrubias, M., Butler, A., Baker, K., Pak, M., & Salkoff, L. (1990). K+ current diversity is produced by an extended gene family conserved in Drosophila and mouse. Science, 248, 599-603.
Yamanouchi, D., Kasuya, G., Nakajo, K., Kise, Y., & Nureki, O. (2023). Dual allosteric modulation of voltage and calcium sensitivities of the Slo1-LRRC channel complex. Molecular Cell, 83, 4555-4569.
Yan, J., & Aldrich, R. W. (2010). LRRC26 auxiliary protein allows BK channel activation at resting voltage without calcium. Nature, 466, 513-516.
Yan, J., & Aldrich, R. W. (2012). BK potassium channel modulation by leucine-rich repeat-containing proteins. Proceedings of the National Academy of Sciences of the United States of America, 109, 7917-7922.
Yang, H., Zhang, G., & Cui, J. (2015). BK channels: Multiple sensors, one activation gate. Frontiers in Physiology, 6, 29.
Ye, W., Zhao, H., Dai, Y., Wang, Y., Lo, Y.-H., Jan, L. Y., & Lee, C.-H. (2022). Activation and closed-state inactivation mechanisms of the human voltage-gated KV4 channel complexes. Molecular Cell, 82, 2427-2442.
Zagha, E., Ozaita, A., Chang, S. Y., Nadal, M. S., Lin, U., Saganich, M. J., McCormack, T., Akinsanya, K. O., Qi, S. Y., & Rudy, B. (2005). DPP10 modulates Kv4-mediated A-type potassium channels. The Journal of Biological Chemistry, 280, 18853-18861.
Zaydman, M. A., Kasimova, M. A., McFarland, K., Beller, Z., Hou, P., Kinser, H. E., Liang, H., Zhang, G., Shi, J., Tarek, M., & Cui, J. (2014). Domain-domain interactions determine the gating, permeation, pharmacology, and subunit modulation of the IKs ion channel. eLife, 3, e03606.
Zaydman, M. A., Silva, J. R., Delaloye, K., Li, Y., Liang, H., Larsson, H. P., Shi, J., & Cui, J. (2013). Kv7.1 ion channels require a lipid to couple voltage sensing to pore opening. Proceedings of the National Academy of Sciences of the United States of America, 110, 13180-13185.
Zhang, H., Craciun, L. C., Mirshahi, T., Rohács, T., Lopes, C. M. B., Jin, T., & Logothetis, D. E. (2003). PIP2 activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron, 37, 963-975.
Zicha, S., Xiao, L., Stafford, S., Cha, T. J., Han, W., Varro, A., & Nattel, S. (2004). Transmural expression of transient outward potassium current subunits in normal and failing canine and human hearts. The Journal of Physiology, 561, 735-748.