Abstract
Potassium channels play a crucial role in the physiology of all living organisms. They maintain the membrane potential and are involved in electrical signaling, pH homeostasis, cell-cell communication and survival under osmotic stress. Many prokaryotic potassium channels and members of the eukaryotic Slo channels are regulated by tethered cytoplasmic domains or associated soluble proteins, which belong to the family of regulator of potassium conductance (RCK). RCK domains and subunits form octameric rings, which control ion gating. For years, a common regulatory mechanism was suggested: ligand-induced conformational changes in the octameric ring would pull open a gate in the pore via flexible linkers. Consistently, ligand-dependent conformational changes were described for various RCK gating rings. Yet, recent structural and functional data of complete ion channels uncovered that the following signal transduction to the pore domains is divers. The different RCK-regulated ion channels show remarkably heterogeneous mechanisms with neither the connection from the RCK domain to the pore nor the gate being conserved. Some channels even lack the flexible linkers, while in others the gate cannot easily be assigned. In this review we compare available structures of RCK-gated potassium channels, highlight the similarities and differences of channel gating, and delineate existing inconsistencies.
Funding source: Deutsche Forschungsgemeinschaft
Award Identifier / Grant number: HA6322/3-1
Funding statement: I.H. acknowledges funding from the Deutsche Forschungsgemeinschaft (Funder Id: http://dx.doi.org/10.13039/501100001659, HA6322/3-1), and the SFB 807 ‘Transport and Communication across Biological Membranes’. M.S. acknowledges the Integrated Research Training Group – TRAM (SFB 807) for financial support.
References
Albright, R.A., Ibar, J.L., Kim, C.U., Gruner, S.M., and Morais-Cabral, J.H. (2006). The RCK domain of the KtrAB K+ transporter: multiple conformations of an octameric ring. Cell 126, 1147–1159.10.1016/j.cell.2006.08.028Search in Google Scholar PubMed
Bai, Y., Yang, J., Zarrella, T.M., Zhang, Y., Metzger, D.W., and Bai, G. (2014). Cyclic di-AMP impairs potassium uptake mediated by a cyclic di-AMP binding protein in Streptococcus pneumoniae. J. Bacteriol. 196, 614–623.10.1128/JB.01041-13Search in Google Scholar PubMed PubMed Central
Barcia, G., Fleming, M.R., Deligniere, A., Gazula, V.R., Brown, M.R., Langouet, M., Chen, H.J., Kronengold, J., Abhyankar, A., Cilio, R., et al. (2012). De novo gain-of-function KCNT1 channel mutations cause malignant migrating partial seizures of infancy. Nat. Genet. 44, 1255–1259.10.1038/ng.2441Search in Google Scholar PubMed PubMed Central
Barker, J.R., Koestler, B.J., Carpenter, V.K., Burdette, D.L., Waters, C.M., Vance, R.E., and Valdivia, R.H. (2013). STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio 4, 1–11.10.1128/mBio.00018-13Search in Google Scholar PubMed PubMed Central
Barrett, J.N., Magleby, K.L., and Pallotta, B.S. (1982). Properties of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 331, 211–230.10.1113/jphysiol.1982.sp014370Search in Google Scholar PubMed PubMed Central
Becker, D., Fendler, K., Altendorf, K., and Greie, J.C. (2007). The conserved dipole in transmembrane helix 5 of KdpB in the Escherichia coli KdpFABC P-type ATPase is crucial for coupling and the electrogenic K+-translocation step. Biochemistry 46, 13920–13928.10.1021/bi701394hSearch in Google Scholar PubMed
Bellamacina, C.R. (1996). The nicotinamide dinucleotide binding motif: a comparison of nucleotide binding proteins. FASEB J. 10, 1257–1269.10.1096/fasebj.10.11.8836039Search in Google Scholar PubMed
Bhattacharjee, A., Gan, L., and Kaczmarek, L.K. (2002). Localization of the Slack potassium channel in the rat central nervous system. J. Comp. Neurol. 454, 241–254.10.1002/cne.10439Search in Google Scholar PubMed
Brelidze, T.I., Niu, X., and Magleby, K.L. (2003). A ring of eight conserved negatively charged amino acids doubles the conductance of BK channels and prevents inward rectification. Proc. Natl. Acad. Sci. USA 100, 9017–9022.10.1073/pnas.1532257100Search in Google Scholar PubMed PubMed Central
Cao, Y., Jin, X., Huang, H., Derebe, M.G., Levin, E.J., Kabaleeswaran, V., Pan, Y., Punta, M., Love, J., Weng, J., et al. (2011). Crystal structure of a potassium ion transporter, TrkH. Nature 471, 336–340.10.1038/nature09731Search in Google Scholar PubMed PubMed Central
Cao, Y., Pan, Y., Huang, H., Jin, X., Levin, E.J., Kloss, B., and Zhou, M. (2013). Gating of the TrkH ion channel by its associated RCK protein TrkA. Nature 496, 317–322.10.1038/nature12056Search in Google Scholar PubMed PubMed Central
Carvacho, I., Gonzalez, W., Torres, Y.P., Brauchi, S., Alvarez, O., Gonzalez-Nilo, F.D., and Latorre, R. (2008). Intrinsic electrostatic potential in the BK channel pore: role in determining single channel conductance and block. J. Gen. Physiol. 131, 147–161.10.1085/jgp.200709862Search in Google Scholar PubMed PubMed Central
Chakrapani, S. and Perozo, E. (2007). How to gate an ion channel: lessons from MthK. Nat. Struct. Mol. Biol. 14, 180–182.10.1038/nsmb0307-180Search in Google Scholar PubMed
Checchetto, V., Formentin, E., Carraretto, L., Segalla, A., Giacometti, G.M., Szabo, I., and Bergantino, E. (2013). Functional characterization and determination of the physiological role of a calcium-dependent potassium channel from cyanobacteria. Plant. Physiol. 162, 953–964.10.1104/pp.113.215129Search in Google Scholar PubMed PubMed Central
Chin, K.H., Liang, J.M., Yang, J.G., Shih, M.S., Tu, Z.L., Wang, Y.C., Sun, X.H., Hu, N.J., Liang, Z.X., Dow, J.M., et al. (2015). Structural insights into the distinct binding mode of cyclic di-AMP with SaCpaA_RCK. Biochemistry 54, 4936–4951.10.1021/acs.biochem.5b00633Search in Google Scholar PubMed
Contreras, G.F., Castillo, K., Enrique, N., Carrasquel-Ursulaez, W., Castillo, J.P., Milesi, V., Neely, A., Alvarez, O., Ferreira, G., Gonzalez, C., et al. (2013). A BK (Slo1) channel journey from molecule to physiology. Channels 7, 442–458.10.4161/chan.26242Search in Google Scholar PubMed PubMed Central
Corrigan, R.M. and Grundling, A. (2013). Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol. 11, 513–524.10.1038/nrmicro3069Search in Google Scholar PubMed
Corrigan, R.M., Campeotto, I., Jeganathan, T., Roelofs, K.G., Lee, V.T., and Grundling, A. (2013). Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. USA 110, 9084–9089.10.1073/pnas.1300595110Search in Google Scholar PubMed PubMed Central
Diskowski, M., Mikusevic, V., Stock, C., and Hänelt, I. (2015). Functional diversity of the superfamily of K+ transporters to meet various requirements. Biol. Chem. 396, 1003–1014.10.1515/hsz-2015-0123Search in Google Scholar PubMed
Diskowski, M., Mehdipour, A.R., Wunnicke, D., Mills, D.J., Mikusevic, V., Bärland, N., Hoffmann, J., Morgner, N., Steinhoff, H.J., Hummer, G., et al. (2017). Helical jackknives control the gates of the double-pore K+ uptake system KtrAB. eLife 6, 1–21.10.7554/eLife.24303Search in Google Scholar PubMed PubMed Central
Dong, J., Shi, N., Berke, I., Chen, L., and Jiang, Y. (2005). Structures of the MthK RCK domain and the effect of Ca2+ on gating ring stability. J. Biol. Chem. 280, 41716–41724.10.1074/jbc.M508144200Search in Google Scholar
Durell, S.R. and Guy, H.R. (1999). Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K+ channel. Biophys. J. 77, 789–807.10.1016/S0006-3495(99)76932-8Search in Google Scholar
Durell, S.R., Hao, Y., Nakamura, T., Bakker, E.P., and Guy, H.R. (1999). Evolutionary relationship between K+ channels and symporters. Biophys. J. 77, 775–788.10.1016/S0006-3495(99)76931-6Search in Google Scholar
Durell, S.R., Bakker, E.P., and Guy, H.R. (2000). Does the KdpA subunit from the high affinity K+-translocating P-type KDP-ATPase have a structure similar to that of K+ channels? Biophys. J. 78, 188–199.10.1016/S0006-3495(00)76584-2Search in Google Scholar
Elkins, T., Ganetzky, B., and Wu, C.F. (1986). A Drosophila mutation that eliminates a calcium-dependent potassium current. Proc. Natl. Acad. Sci. USA 83, 8415–8419.10.1073/pnas.83.21.8415Search in Google Scholar
Follmann, M., Becker, M., Ochrombel, I., Ott, V., Kramer, R., and Marin, K. (2009). Potassium transport in Corynebacterium glutamicum is facilitated by the putative channel protein CglK, which is essential for pH homeostasis and growth at acidic pH. J. Bacteriol. 191, 2944–2952.10.1128/JB.00074-09Search in Google Scholar
Gangola, P. and Rosen, B.P. (1987). Maintenance of intracellular calcium in Escherichia coli. J. Biol. Chem. 262, 12570–12574.10.1016/S0021-9258(18)45243-XSearch in Google Scholar
Giraldez, T. and Rothberg, B.S. (2017). Understanding the conformational motions of RCK gating rings. J. Gen. Physiol. 149, 431–441.10.1085/jgp.201611726Search in Google Scholar PubMed PubMed Central
Golowasch, J., Kirkwood, A., and Miller, C. (1986). Allosteric effects of Mg2+ on the gating of Ca2+-activated K+ channels from mammalian skeletal muscle. J. Exp. Biol. 124, 5–13.10.1242/jeb.124.1.5Search in Google Scholar PubMed
Gries, C.M., Bose, J.L., Nuxoll, A.S., Fey, P.D., and Bayles, K.W. (2013). The Ktr potassium transport system in Staphylococcus aureus and its role in cell physiology, antimicrobial resistance and pathogenesis. Mol. Microbiol. 89, 760–773.10.1111/mmi.12312Search in Google Scholar PubMed PubMed Central
Gundlach, J., Herzberg, C., Hertel, D., Thurmer, A., Daniel, R., Link, H., and Stülke, J. (2017). Adaptation of Bacillus subtilis to life at extreme potassium limitation. MBio 8, 1–12.10.1128/mBio.00861-17Search in Google Scholar PubMed PubMed Central
Hänelt, I., Löchte, S., Sundermann, L., Elbers, K., Vor der Brüggen, M., and Bakker, E.P. (2010a). Gain of function mutations in membrane region M2C2 of KtrB open a gate controlling K+ transport by the KtrAB system from Vibrio alginolyticus. J. Biol. Chem. 285, 10318–10327.10.1074/jbc.M109.089870Search in Google Scholar PubMed PubMed Central
Hänelt, I., Wunnicke, D., Müller-Trimbusch, M., Vor der Brüggen, M., Kraus, I., Bakker, E.P., and Steinhoff, H.J. (2010b). Membrane region M2C2 in subunit KtrB of the K+ uptake system KtrAB from Vibrio alginolyticus forms a flexible gate controlling K+ flux: An electron paramagnetic resonance study. J. Biol. Chem. 285, 28210–28219.10.1074/jbc.M110.139311Search in Google Scholar PubMed PubMed Central
Hänelt, I., Tholema, N., Kröning, N., Vor der Brüggen, M., Wunnicke, D., and Bakker, E.P. (2011). KtrB, a member of the superfamily of K+ transporters. Eur. J. Cell. Biol. 90, 696–704.10.1016/j.ejcb.2011.04.010Search in Google Scholar PubMed
Harms, C., Domoto, Y., Celik, C., Rahe, E., Stumpe, S., Schmid, R., Nakamura, T., and Bakker, E.P. (2001). Identification of the ABC protein SapD as the subunit that confers ATP dependence to the K+-uptake systems TrkH and TrkG from Escherichia coli K-12. Microbiology 147, 2991–3003.10.1099/00221287-147-11-2991Search in Google Scholar PubMed
Healy, J., Ekkerman, S., Pliotas, C., Richard, M., Bartlett, W., Grayer, S.C., Morris, G.M., Miller, S., Booth, I.R., Conway, S.J., et al. (2014). Understanding the structural requirements for activators of the Kef bacterial potassium efflux system. Biochemistry 53, 1982–1992.10.1021/bi5001118Search in Google Scholar PubMed PubMed Central
Hite, R.K. and MacKinnon, R. (2017). Structural titration of Slo2.2, a Na+-dependent K+ channel. Cell 168, 390–399.10.1016/j.cell.2016.12.030Search in Google Scholar PubMed PubMed Central
Hite, R.K., Yuan, P., Li, Z., Hsuing, Y., Walz, T., and MacKinnon, R. (2015). Cryo-electron microscopy structure of the Slo2.2 Na+-activated K+ channel. Nature 527, 198–203.10.1038/nature14958Search in Google Scholar PubMed PubMed Central
Hite, R.K., Tao, X., and MacKinnon, R. (2017). Structural basis for gating the high-conductance Ca2+-activated K+ channel. Nature 541, 52–57.10.1038/nature20775Search in Google Scholar PubMed PubMed Central
Hou, S., Vigeland, L.E., Zhang, G., Xu, R., Li, M., Heinemann, S.H., and Hoshi, T. (2010). Zn2+ activates large conductance Ca2+-activated K+ channel via an intracellular domain. J. Biol. Chem. 285, 6434–6442.10.1074/jbc.M109.069211Search in Google Scholar PubMed PubMed Central
Humphries, J., Xiong, L., Liu, J., Prindle, A., Yuan, F., Arjes, H.A., Tsimring, L., and Süel, G.M. (2017). Species-independent attraction to biofilms through electrical signaling. Cell 168, 200–209.10.1016/j.cell.2016.12.014Search in Google Scholar
Ishii, A., Shioda, M., Okumura, A., Kidokoro, H., Sakauchi, M., Shimada, S., Shimizu, T., Osawa, M., Hirose, S., and Yamamoto, T. (2013). A recurrent KCNT1 mutation in two sporadic cases with malignant migrating partial seizures in infancy. Gene 531, 467–471.10.1016/j.gene.2013.08.096Search in Google Scholar
Jia, Z., Yazdani, M., Zhang, G., Cui, J., and Chen, J. (2018). Hydrophobic gating in BK channels. Nat. Commun. 9, 1–8.10.1038/s41467-018-05970-3Search in Google Scholar
Jiang, Y., Pico, A., Cadene, M., Chait, B.T., and MacKinnon, R. (2001). Structure of the RCK domain from the E. coli K+ channel and demonstration of its presence in the human BK channel. Neuron 29, 593–601.10.1016/S0896-6273(01)00236-7Search in Google Scholar
Jiang, Y., Lee, A., Chen, J., Cadene, M., Chait, B.T., and MacKinnon, R. (2002a). Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417, 515–522.10.1038/417515aSearch in Google Scholar PubMed
Jiang, Y., Lee, A., Chen, J., Cadene, M., Chait, B.T., and MacKinnon, R. (2002b). The open pore conformation of potassium channels. Nature 417, 523–526.10.1038/417523aSearch in Google Scholar PubMed
Kato, N., Akai, M., Zulkifli, L., Matsuda, N., Kato, Y., Goshima, S., Hazama, A., Yamagami, M., Guy, H.R., and Uozumi, N. (2007). Role of positively charged amino acids in the M2D transmembrane helix of Ktr/Trk/HKT type cation transporters. Channels 1, 161–171.10.4161/chan.4374Search in Google Scholar PubMed
Kim, H., Youn, S.J., Kim, S.O., Ko, J., Lee, J.O., and Choi, B.S. (2015). Structural studies of potassium transport protein KtrA regulator of conductance of K+ (RCK) C domain in complex with cyclic diadenosine monophosphate (c-di-AMP). J. Biol. Chem. 290, 16393–16402.10.1074/jbc.M115.641340Search in Google Scholar PubMed PubMed Central
Kixmüller, D. and Greie, J.C. (2012). An ATP-driven potassium pump promotes long-term survival of Halobacterium salinarum within salt crystals. Environ. Microbiol. Rep. 4, 234–241.10.1111/j.1758-2229.2012.00326.xSearch in Google Scholar PubMed
Kong, C., Zeng, W., Ye, S., Chen, L., Sauer, D.B., Lam, Y., Derebe, M.G., and Jiang, Y. (2012). Distinct gating mechanisms revealed by the structures of a multi-ligand gated K+ channel. eLife 1, 1–20.10.7554/eLife.00184Search in Google Scholar PubMed PubMed Central
Kröning, N., Willenborg, M., Tholema, N., Hänelt, I., Schmid, R., and Bakker, E.P. (2007). ATP binding to the KTN/RCK subunit KtrA from the K+-uptake system KtrAB of Vibrio alginolyticus: its role in the formation of the KtrAB complex and its requirement in vivo. J. Biol. Chem. 282, 14018–14027.10.1074/jbc.M609084200Search in Google Scholar
Kuo, M.M., Haynes, W.J., Loukin, S.H., Kung, C., and Saimi, Y. (2005). Prokaryotic K+ channels: from crystal structures to diversity. FEMS Microbiol. Rev. 29, 961–985.10.1016/j.femsre.2005.03.003Search in Google Scholar
Kuo, M.M., Baker, K.A., Wong, L., and Choe, S. (2007). Dynamic oligomeric conversions of the cytoplasmic RCK domains mediate MthK potassium channel activity. Proc. Natl. Acad. Sci. USA 104, 2151–2156.10.1073/pnas.0609085104Search in Google Scholar
Larkin, J.W., Zhai, X., Kikuchi, K., Redford, S.E., Prindle, A., Liu, J., Greenfield, S., Walczak, A.M., Garcia-Ojalvo, J., Mugler, A., et al. (2018). Signal percolation within a bacterial community. Cell Syst. 7, 137–145.10.1016/j.cels.2018.06.005Search in Google Scholar
Latorre, R., Vergara, C., and Hidalgo, C. (1982). Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc. Natl. Acad. Sci. USA 79, 805–809.10.1073/pnas.79.3.805Search in Google Scholar
Leonetti, M.D., Yuan, P., Hsiung, Y., and MacKinnon, R. (2012). Functional and structural analysis of the human SLO3 pH- and voltage-gated K+ channel. Proc. Natl. Acad. Sci. USA 109, 19274–19279.10.1073/pnas.1215078109Search in Google Scholar
Levin, E.J. and Zhou, M. (2014). Recent progress on the structure and function of the TrkH/KtrB ion channel. Curr. Opin. Struct. Biol. 27, 95–101.10.1016/j.sbi.2014.06.004Search in Google Scholar
Lingle, C.J. (2007). Gating rings formed by RCK domains: keys to gate opening. J. Gen. Physiol. 129, 101–107.10.1085/jgp.200709739Search in Google Scholar
Littleton, J.T. and Ganetzky, B. (2000). Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26, 35–43.10.1016/S0896-6273(00)81135-6Search in Google Scholar
Liu, P., Chen, B., and Wang, Z.W. (2014). SLO-2 potassium channel is an important regulator of neurotransmitter release in Caenorhabditis elegans. Nat. Commun. 5, 1–12.10.1038/ncomms6155Search in Google Scholar PubMed PubMed Central
Loukin, S.H., Kuo, M.M., Zhou, X.L., Haynes, W.J., Kung, C., and Saimi, Y. (2005). Microbial K+ channels. J. Gen. Physiol. 125, 521–527.10.1085/jgp.200509261Search in Google Scholar PubMed PubMed Central
Ma, Z., Lou, X.J., and Horrigan, F.T. (2006). Role of charged residues in the S1–S4 voltage sensor of BK channels. J. Gen. Physiol. 127, 309–328.10.1085/jgp.200509421Search in Google Scholar PubMed PubMed Central
Marty, A. (1981). Ca2+-dependent K+ channels with large unitary conductance in chromaffin cell membranes. Nature 291, 497–500.10.1038/291497a0Search in Google Scholar PubMed
Mäser, P., Hosoo, Y., Goshima, S., Horie, T., Eckelman, B., Yamada, K., Yoshida, K., Bakker, E.P., Shinmyo, A., Oiki, S., et al. (2002). Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc. Natl. Acad. Sci. USA 99, 6428–6433.10.1073/pnas.082123799Search in Google Scholar PubMed PubMed Central
Matsuda, N. and Uozumi, N. (2006). Ktr-mediated potassium transport, a major pathway for potassium uptake, is coupled to a proton gradient across the membrane in Synechocystis sp. PCC 6803. Biosci. Biotechnol. Biochem. 70, 273–275.10.1271/bbb.70.273Search in Google Scholar PubMed
Matsuda, N., Kobayashi, H., Katoh, H., Ogawa, T., Futatsugi, L., Nakamura, T., Bakker, E.P., and Uozumi, N. (2004). Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock. J. Biol. Chem. 279, 54952–54962.10.1074/jbc.M407268200Search in Google Scholar PubMed
Miranda, P., Giraldez, T., and Holmgren, M. (2016). Interactions of divalent cations with calcium binding sites of BK channels reveal independent motions within the gating ring. Proc. Natl. Acad. Sci. USA 113, 14055–14060.10.1073/pnas.1611415113Search in Google Scholar PubMed PubMed Central
Miranda, P., Holmgren, M., and Giraldez, T. (2018). Voltage-dependent dynamics of the BK channel cytosolic gating ring are coupled to the membrane-embedded voltage sensor. eLife 7, 1–18.10.7554/eLife.40664.014Search in Google Scholar
Nakamura, T., Yuda, R., Unemoto, T., and Bakker, E.P. (1998). KtrAB, a new type of bacterial K+-uptake system from Vibrio alginolyticus. J. Bacteriol. 180, 3491–3494.10.1128/JB.180.13.3491-3494.1998Search in Google Scholar PubMed PubMed Central
Nanatani, K., Shijuku, T., Takano, Y., Zulkifli, L., Yamazaki, T., Tominaga, A., Souma, S., Onai, K., Morishita, M., Ishiura, M., et al. (2015). Comparative analysis of kdp and ktr mutants reveals distinct roles of the potassium transporters in the model cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 197, 676–687.10.1128/JB.02276-14Search in Google Scholar PubMed PubMed Central
Nimigean, C.M., Chappie, J.S., and Miller, C. (2003). Electrostatic tuning of ion conductance in potassium channels. Biochemistry 42, 9263–9268.10.1021/bi0348720Search in Google Scholar PubMed
Niu, X., Qian, X., and Magleby, K.L. (2004). Linker-gating ring complex as passive spring and Ca2+-dependent machine for a voltage- and Ca2+-activated potassium channel. Neuron 42, 745–756.10.1016/j.neuron.2004.05.001Search in Google Scholar PubMed
Norris, V., Grant, S., Freestone, P., Canvin, J., Sheikh, F.N., Toth, I., Trinei, M., Modha, K., and Norman, R.I. (1996). Calcium signalling in bacteria. J. Bacteriol. 178, 3677–3682.10.1128/jb.178.13.3677-3682.1996Search in Google Scholar PubMed PubMed Central
Oberhauser, A., Alvarez, O., and Latorre, R. (1988). Activation by divalent cations of a Ca2+-activated K+ channel from skeletal muscle membrane. J. Gen. Physiol. 92, 67–86.10.1085/jgp.92.1.67Search in Google Scholar PubMed PubMed Central
Ochrombel, I., Ott, L., Kramer, R., Burkovski, A., and Marin, K. (2011). Impact of improved potassium accumulation on pH homeostasis, membrane potential adjustment and survival of Corynebacterium glutamicum. Biochim. Biophys. Acta 1807, 444–450.10.1016/j.bbabio.2011.01.008Search in Google Scholar PubMed
Oppenheimer-Shaanan, Y., Wexselblatt, E., Katzhendler, J., Yavin, E., and Ben-Yehuda, S. (2011). C-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep. 12, 594–601.10.1038/embor.2011.77Search in Google Scholar PubMed PubMed Central
Ordal, G.W. (1977). Calcium ion regulates chemotactic behaviour in bacteria. Nature 270, 66–67.10.1038/270066a0Search in Google Scholar PubMed
Pallotta, B.S., Magleby, K.L., and Barrett, J.N. (1981). Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature 293, 471–474.10.1038/293471a0Search in Google Scholar PubMed
Parfenova, L.V., Abarca-Heidemann, K., Crane, B.M., and Rothberg, B.S. (2007). Molecular architecture and divalent cation activation of TvoK, a prokaryotic potassium channel. J. Biol. Chem. 282, 24302–24309.10.1074/jbc.M703650200Search in Google Scholar PubMed PubMed Central
Pau, V.P., Abarca-Heidemann, K., and Rothberg, B.S. (2010). Allosteric mechanism of Ca2+ activation and H+-inhibited gating of the MthK K+ channel. J. Gen. Physiol. 135, 509–526.10.1085/jgp.200910387Search in Google Scholar PubMed PubMed Central
Pau, V.P., Smith, F.J., Taylor, A.B., Parfenova, L.V., Samakai, E., Callaghan, M.M., Abarca-Heidemann, K., Hart, P.J., and Rothberg, B.S. (2011). Structure and function of multiple Ca2+-binding sites in a K+ channel regulator of K+ conductance (RCK) domain. Proc. Natl. Acad. Sci. USA 108, 17684–17689.10.1073/pnas.1107229108Search in Google Scholar PubMed PubMed Central
Pliotas, C., Grayer, S.C., Ekkerman, S., Chan, A.K.N., Healy, J., Marius, P., Bartlett, W., Khan, A., Cortopassi, W.A., Chandler, S.A., et al. (2017). Adenosine monophosphate binding stabilizes the KTN domain of the Shewanella denitrificans Kef potassium efflux system. Biochemistry 56, 4219–4234.10.1021/acs.biochem.7b00300Search in Google Scholar PubMed PubMed Central
Posson, D.J., McCoy, J.G., and Nimigean, C.M. (2013). The voltage-dependent gate in MthK potassium channels is located at the selectivity filter. Nat. Struct. Mol. Biol. 20, 159–166.10.1038/nsmb.2473Search in Google Scholar PubMed PubMed Central
Posson, D.J., Rusinova, R., Andersen, O.S., and Nimigean, C.M. (2015). Calcium ions open a selectivity filter gate during activation of the MthK potassium channel. Nat. Commun. 6, 1–10.10.1038/ncomms9342Search in Google Scholar PubMed PubMed Central
Price-Whelan, A., Poon, C.K., Benson, M.A., Eidem, T.T., Roux, C.M., Boyd, J.M., Dunman, P.M., Torres, V.J., and Krulwich, T.A. (2013). Transcriptional profiling of Staphylococcus aureus during growth in 2 M NaCl leads to clarification of physiological roles for Kdp and Ktr K+ uptake systems. MBio 4, 1–11.10.1128/mBio.00407-13Search in Google Scholar PubMed PubMed Central
Prindle, A., Liu, J., Asally, M., Ly, S., Garcia-Ojalvo, J., and Suel, G.M. (2015). Ion channels enable electrical communication in bacterial communities. Nature 527, 59–63.10.1038/nature15709Search in Google Scholar PubMed PubMed Central
Qian, X., Niu, X., and Magleby, K.L. (2006). Intra- and intersubunit cooperativity in activation of BK channels by Ca2+. J. Gen. Physiol. 128, 389–404.10.1085/jgp.200609486Search in Google Scholar PubMed PubMed Central
Rhoads, D.B., Waters, F.B., and Epstein, W. (1976). Cation transport in Escherichia coli. VIII. Potassium transport mutants. J. Gen. Physiol. 67, 325–341.10.1085/jgp.67.3.325Search in Google Scholar PubMed PubMed Central
Rocha, R., Teixeira-Duarte, C.M., Jorge, J.M.P., and Morais-Cabral, J.H. (2019). Characterization of the molecular properties of KtrC, a second RCK domain that regulates a Ktr channel in Bacillus subtilis. J. Struct. Biol. 205, 34–43.10.1016/j.jsb.2019.02.002Search in Google Scholar PubMed
Römling, U. (2008). Great times for small molecules: C-di-AMP, a second messenger candidate in bacteria and archaea. Sci. Signal. 1, 1–5.10.1126/scisignal.133pe39Search in Google Scholar PubMed
Roosild, T.P., Miller, S., Booth, I.R., and Choe, S. (2002). A mechanism of regulating transmembrane potassium flux through a ligand-mediated conformational switch. Cell 109, 781–791.10.1016/S0092-8674(02)00768-7Search in Google Scholar
Roosild, T.P., Castronovo, S., Miller, S., Li, C., Rasmussen, T., Bartlett, W., Gunasekera, B., Choe, S., and Booth, I.R. (2009). KTN (RCK) domains regulate K+ channels and transporters by controlling the dimer-hinge conformation. Structure 17, 893–903.10.1016/j.str.2009.03.018Search in Google Scholar
Roosild, T.P., Castronovo, S., Healy, J., Miller, S., Pliotas, C., Rasmussen, T., Bartlett, W., Conway, S.J., and Booth, I.R. (2010). Mechanism of ligand-gated potassium efflux in bacterial pathogens. Proc. Natl. Acad. Sci. USA 107, 19784–19789.10.1073/pnas.1012716107Search in Google Scholar
Salkoff, L., Butler, A., Ferreira, G., Santi, C., and Wei, A. (2006). High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7, 921–931.10.1038/nrn1992Search in Google Scholar
Savalli, N., Pantazis, A., Yusifov, T., Sigg, D., and Olcese, R. (2012). The contribution of RCK domains to human BK channel allosteric activation. J. Biol. Chem. 287, 21741–21750.10.1074/jbc.M112.346171Search in Google Scholar
Schlösser, A., Kluttig, S., Hamann, A., and Bakker, E.P. (1991). Subcloning, nucleotide sequence, and expression of trkG, a gene that encodes an integral membrane protein involved in potassium uptake via the Trk system of Escherichia coli. J. Bacteriol. 173, 3170–3176.10.1128/jb.173.10.3170-3176.1991Search in Google Scholar
Schlösser, A., Meldorf, M., Stumpe, S., Bakker, E.P., and Epstein, W. (1995). TrkH and its homolog, TrkG, determine the specificity and kinetics of cation transport by the Trk system of Escherichia coli. J. Bacteriol. 177, 1908–1910.10.1128/jb.177.7.1908-1910.1995Search in Google Scholar
Schreiber, M. and Salkoff, L. (1997). A novel calcium-sensing domain in the BK channel. Biophys. J. 73, 1355–1363.10.1016/S0006-3495(97)78168-2Search in Google Scholar
Shi, J. and Cui, J. (2001). Intracellular Mg2+ enhances the function of BK-type Ca2+-activated K+ channels. J. Gen. Physiol. 118, 589–606.10.1085/jgp.118.5.589Search in Google Scholar
Smith, R.J. (1995). Calcium and bacteria. Adv. Microb. Physiol. 37, 83–133.10.1016/S0065-2911(08)60144-7Search in Google Scholar
Smith, F.J., Pau, V.P., Cingolani, G., and Rothberg, B.S. (2012). Crystal structure of a Ba2+-bound gating ring reveals elementary steps in RCK domain activation. Structure 20, 2038–2047.10.1016/j.str.2012.09.014Search in Google Scholar
Smith, F.J., Pau, V.P., Cingolani, G., and Rothberg, B.S. (2013). Structural basis of allosteric interactions among Ca2+-binding sites in a K+ channel RCK domain. Nat. Commun. 4, 1–10.10.1038/ncomms3621Search in Google Scholar
Stewart, L.M., Bakker, E.P., and Booth, I.R. (1985). Energy coupling to K+ uptake via the Trk system in Escherichia coli: the role of ATP. J. Gen. Microbiol. 131, 77–85.10.1099/00221287-131-1-77Search in Google Scholar
Strahl, H. and Greie, J.C. (2008). The extremely halophilic archaeon Halobacterium salinarum R1 responds to potassium limitation by expression of the K+-transporting KdpFABC P-type ATPase and by a decrease in intracellular K+. Extremophiles 12, 741–752.10.1007/s00792-008-0177-3Search in Google Scholar
Stumpe, A., Schlösser, A., Schleyer, M., and Bakker, E.P. (1996). K+ circulation across the prokaryotic cell membrane: K+-uptake systems. In: Handbook of Biological Physics, Vol. 2 (Amsterdam: Elsevier), pp. 473–499.10.1016/S1383-8121(96)80062-5Search in Google Scholar
Sweet, T.B. and Cox, D.H. (2008). Measurements of the BKCa channel’s high-affinity Ca2+ binding constants: effects of membrane voltage. J. Gen. Physiol. 132, 491–505.10.1085/jgp.200810094Search in Google Scholar
Szollosi, A., Vieira-Pires, R.S., Teixeira-Duarte, C.M., Rocha, R., and Morais-Cabral, J.H. (2016). Dissecting the molecular mechanism of nucleotide-dependent activation of the KtrAB K+ transporter. PLoS Biol. 14, 1–21.10.1371/journal.pbio.1002356Search in Google Scholar
Tao, X., Hite, R.K., and MacKinnon, R. (2017). Cryo-EM structure of the open high-conductance Ca2+-activated K+ channel. Nature 541, 46–51.10.1038/nature20608Search in Google Scholar
Tholema, N., Bakker, E.P., Suzuki, A., and Nakamura, T. (1999). Change to alanine of one out of four selectivity filter glycines in KtrB causes a two orders of magnitude decrease in the affinities for both K+ and Na+ of the Na+ dependent K+ uptake system KtrAB from Vibrio alginolyticus. FEBS Lett. 450, 217–220.10.1016/S0014-5793(99)00504-9Search in Google Scholar
Tholema, N., Vor der Bruggen, M., Maser, P., Nakamura, T., Schroeder, J.I., Kobayashi, H., Uozumi, N., and Bakker, E.P. (2005). All four putative selectivity filter glycine residues in KtrB are essential for high affinity and selective K+ uptake by the KtrAB system from Vibrio alginolyticus. J. Biol. Chem. 280, 41146–41154.10.1074/jbc.M507647200Search in Google Scholar PubMed
Thompson, J. and Begenisich, T. (2012). Selectivity filter gating in large-conductance Ca2+-activated K+ channels. J. Gen. Physiol. 139, 235–244.10.1085/jgp.201110748Search in Google Scholar
Thomson, A.S. and Rothberg, B.S. (2010). Voltage-dependent inactivation gating at the selectivity filter of the MthK K+ channel. J. Gen. Physiol. 136, 569–579.10.1085/jgp.201010507Search in Google Scholar
Thomson, S.J., Hansen, A., and Sanguinetti, M.C. (2015). Identification of the intracellular Na+ sensor in Slo2.1 potassium channels. J. Biol. Chem. 290, 14528–14535.10.1074/jbc.M115.653089Search in Google Scholar
Tisa, L.S., Olivera, B.M., and Adler, J. (1993). Inhibition of Escherichia coli chemotaxis by omega-conotoxin, a calcium ion channel blocker. J. Bacteriol. 175, 1235–1238.10.1128/jb.175.5.1235-1238.1993Search in Google Scholar
Trautmann, A. and Marty, A. (1984). Activation of Ca2+-dependent K+ channels by carbamoylcholine in rat lacrimal glands. Proc. Natl. Acad. Sci. USA 81, 611–615.10.1073/pnas.81.2.611Search in Google Scholar
Vanderver, A., Simons, C., Schmidt, J.L., Pearl, P.L., Bloom, M., Lavenstein, B., Miller, D., Grimmond, S.M., and Taft, R.J. (2014). Identification of a novel de novo p.Phe932Ile KCNT1 mutation in a patient with leukoencephalopathy and severe epilepsy. Pediatr. Neurol. 50, 112–214.10.1016/j.pediatrneurol.2013.06.024Search in Google Scholar
Vieira-Pires, R.S., Szollosi, A., and Morais-Cabral, J.H. (2013). The structure of the KtrAB potassium transporter. Nature 496, 323–328.10.1038/nature12055Search in Google Scholar
Wallén, P., Robertson, B., Cangiano, L., Low, P., Bhattacharjee, A., Kaczmarek, L.K., and Grillner, S. (2007). Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow after hyperpolarization in lamprey spinal neurons. J. Physiol. 585, 75–90.10.1113/jphysiol.2007.138156Search in Google Scholar
Wang, Z.W., Saifee, O., Nonet, M.L., and Salkoff, L. (2001). SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32, 867–881.10.1016/S0896-6273(01)00522-0Search in Google Scholar
Wei, A., Solaro, C., Lingle, C., and Salkoff, L. (1994). Calcium sensitivity of BK-type KCa channels determined by a separable domain. Neuron 13, 671–681.10.1016/0896-6273(94)90034-5Search in Google Scholar
Wu, Y., Yang, Y., Ye, S., and Jiang, Y. (2010). Structure of the gating ring from the human large-conductance Ca2+-gated K+ channel. Nature 466, 393–397.10.1038/nature09252Search in Google Scholar
Yan, Y., Yang, Y., Bian, S., and Sigworth, F.J. (2012). Expression, purification and functional reconstitution of slack sodium-activated potassium channels. J. Membr. Biol. 245, 667–674.10.1007/s00232-012-9425-7Search in Google Scholar
Yang, H., Hu, L., Shi, J., Delaloye, K., Horrigan, F.T., and Cui, J. (2007). Mg2+ mediates interaction between the voltage sensor and cytosolic domain to activate BK channels. Proc. Natl. Acad. Sci. USA 104, 18270–18275.10.1073/pnas.0705873104Search in Google Scholar
Yang, H., Zhang, G., and Cui, J. (2015). BK channels: multiple sensors, one activation gate. Front. Physiol. 6, 1–16.10.3389/fphys.2015.00029Search in Google Scholar
Ye, S., Li, Y., Chen, L., and Jiang, Y. (2006). Crystal structures of a ligand-free MthK gating ring: Insights into the ligand gating mechanism of K+ channels. Cell 126, 1161–1173.10.1016/j.cell.2006.08.029Search in Google Scholar
Yuan, A., Santi, C.M., Wei, A., Wang, Z.W., Pollak, K., Nonet, M., Kaczmarek, L., Crowder, C.M., and Salkoff, L. (2003). The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37, 765–773.10.1016/S0896-6273(03)00096-5Search in Google Scholar
Yuan, P., Leonetti, M.D., Hsiung, Y., and MacKinnon, R. (2011). Open structure of the Ca2+ gating ring in the high-conductance Ca2+-activated K+ channel. Nature 481, 94–97.10.1038/nature10670Search in Google Scholar PubMed PubMed Central
Zhang, X., Solaro, C.R., and Lingle, C.J. (2001). Allosteric regulation of BK channel gating by Ca2+ and Mg2+ through a nonselective, low affinity divalent cation site. J. Gen. Physiol. 118, 607–636.10.1085/jgp.118.5.607Search in Google Scholar PubMed PubMed Central
Zhang, Z., Rosenhouse-Dantsker, A., Tang, Q.Y., Noskov, S., and Logothetis, D.E. (2010). The RCK2 domain uses a coordination site present in Kir channels to confer sodium sensitivity to Slo2.2 channels. J. Neurosci. 30, 7554–7562.10.1523/JNEUROSCI.0525-10.2010Search in Google Scholar PubMed PubMed Central
Zhou, Y., Yang, H., Cui, J., and Lingle, C.J. (2017). Threading the biophysics of mammalian Slo1 channels onto structures of an invertebrate Slo1 channel. J. Gen. Physiol. 149, 985–1007.10.1085/jgp.201711845Search in Google Scholar PubMed PubMed Central
Zulkifli, L., Akai, M., Yoshikawa, A., Shimojima, M., Ohta, H., Guy, H.R., and Uozumi, N. (2010). The KtrA and KtrE subunits are required for Na+-dependent K+ uptake by KtrB across the plasma membrane in Synechocystis sp. strain PCC 6803. J. Bacteriol. 192, 5063–5070.10.1128/JB.00569-10Search in Google Scholar PubMed PubMed Central
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Articles in the same Issue
- Frontmatter
- Spotlight on biomembranes – the 11th Transport Colloquium
- ABCB4/MDR3 in health and disease – at the crossroads of biochemistry and medicine
- Staphylococcus aureus α-toxin: small pore, large consequences
- 19F NMR as a versatile tool to study membrane protein structure and dynamics
- Mg2+ homeostasis and transport in cyanobacteria – at the crossroads of bacterial and chloroplast Mg2+ import
- How RCK domains regulate gating of K+ channels
- Exofacial phospholipids at the plasma membrane: ill-defined targets for early infection processes
- Aryl hydrocarbon receptor ligands increase ABC transporter activity and protein expression in killifish (Fundulus heteroclitus) renal proximal tubules
- Organic anion transporters 1 and 3 influence cellular energy metabolism in renal proximal tubule cells
- CFTR structure, stability, function and regulation
- Homo- and heterodimerization is a common feature of the solute carrier family SLC10 members
- Research Articles/Short Communications
- Cell Biology and Signaling
- Identification of the molecular determinants for nuclear import of PRV EP0
Articles in the same Issue
- Frontmatter
- Spotlight on biomembranes – the 11th Transport Colloquium
- ABCB4/MDR3 in health and disease – at the crossroads of biochemistry and medicine
- Staphylococcus aureus α-toxin: small pore, large consequences
- 19F NMR as a versatile tool to study membrane protein structure and dynamics
- Mg2+ homeostasis and transport in cyanobacteria – at the crossroads of bacterial and chloroplast Mg2+ import
- How RCK domains regulate gating of K+ channels
- Exofacial phospholipids at the plasma membrane: ill-defined targets for early infection processes
- Aryl hydrocarbon receptor ligands increase ABC transporter activity and protein expression in killifish (Fundulus heteroclitus) renal proximal tubules
- Organic anion transporters 1 and 3 influence cellular energy metabolism in renal proximal tubule cells
- CFTR structure, stability, function and regulation
- Homo- and heterodimerization is a common feature of the solute carrier family SLC10 members
- Research Articles/Short Communications
- Cell Biology and Signaling
- Identification of the molecular determinants for nuclear import of PRV EP0