Dimerisation of the Yeast K+ Translocation Protein Trk1 Depends on the K+ Concentration
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
16-19221S
Czech Science Foundation
LM2015055
Ministry of Education Youth and Sports
8J22AT012
Ministry of Education Youth and Sports
149/2016/P
Grantová agentura Jihočeské univerzity v Českých Budějovicích
e-INFRA CZ LM2018140
Ministry of Education Youth and Sports
PubMed
36613841
PubMed Central
PMC9820094
DOI
10.3390/ijms24010398
PII: ijms24010398
Knihovny.cz E-zdroje
- Klíčová slova
- K+ translocation, MD simulation, Saccharomyces cerevisiae, bimolecular fluorescence complementation, dimerisation, molecular modelling,
- MeSH
- biologický transport MeSH
- buněčná membrána metabolismus MeSH
- draslík metabolismus MeSH
- fungální proteiny metabolismus MeSH
- proteiny přenášející kationty * genetika metabolismus MeSH
- Saccharomyces cerevisiae - proteiny * genetika metabolismus MeSH
- Saccharomyces cerevisiae metabolismus MeSH
- translokace genetická MeSH
- transportní proteiny metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- draslík MeSH
- fungální proteiny MeSH
- proteiny přenášející kationty * MeSH
- Saccharomyces cerevisiae - proteiny * MeSH
- transportní proteiny MeSH
- TRK1 protein, S cerevisiae MeSH Prohlížeč
In baker's yeast (Saccharomyces cerevisiae), Trk1, a member of the superfamily of K-transporters (SKT), is the main K+ uptake system under conditions when its concentration in the environment is low. Structurally, Trk1 is made up of four domains, each similar and homologous to a K-channel α subunit. Because most K-channels are proteins containing four channel-building α subunits, Trk1 could be functional as a monomer. However, related SKT proteins TrkH and KtrB were crystallised as dimers, and for Trk1, a tetrameric arrangement has been proposed based on molecular modelling. Here, based on Bimolecular Fluorescence Complementation experiments and single-molecule fluorescence microscopy combined with molecular modelling; we provide evidence that Trk1 can exist in the yeast plasma membrane as a monomer as well as a dimer. The association of monomers to dimers is regulated by the K+ concentration.
Bioinformatics University of Applied Sciences Upper Austria 4232 Hagenberg Austria
Institute of Microbiology of the Czech Academy of Sciences Zamek 136 3733 Nove Hrady Czech Republic
Institute of Symbolic AI Johannes Kepler University 4040 Linz Austria
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Bertl A., Ramos J., Ludwig J., Lichtenberg-Fraté H., Reid J., Bihler H., Calero F., Martinez P., Ljungdahl P.O. Characterization of potassium transport in wild-type and isogenic yeast strains carrying all combinations of trk1, trk2 and tok1 null mutations. Mol. Microbiol. 2003;47:767–780. doi: 10.1046/j.1365-2958.2003.03335.x. PubMed DOI
Gaber R.F., Styles C.A., Fink G.R. TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 1988;8:2848–2859. doi: 10.1128/mcb.8.7.2848. PubMed DOI PMC
Ramos J., Alijo R., Haro R., Rodriguez-Navarro A. TRK2 is not a low-affinity potassium transporter in Saccharomyces cerevisiae. J. Bacteriol. 1994;176:249–252. doi: 10.1128/jb.176.1.249-252.1994. PubMed DOI PMC
Petrezsélyová S., Ramos J., Sychrová H. Trk2 transporter is a relevant player in K+ supply and plasma-membrane potential control in Saccharomyces cerevisiae. Folia Microbiol. 2011;56:23–28. doi: 10.1007/s12223-011-0009-1. PubMed DOI
Zimmermannová O., Felcmanová K., Rosas-Santiago P., Papoušková K., Pantoja O., Sychrová H. Erv14 cargo receptor participates in regulation of plasma-membrane potential, intracellular pH and potassium homeostasis via its interaction with K+-specific transporters Trk1 and Tok1. Biochim. Et Biophys. Acta Mol. Cell Res. 2019;1866:1376–1388. doi: 10.1016/j.bbamcr.2019.05.005. PubMed DOI
Zimmermannova O., Felcmanova K., Sacka L., Colinet A.-S., Morsomme P., Sychrova H. K+-specific importers Trk1 and Trk2 play different roles in Ca2+ homeostasis and signalling in Saccharomyces cerevisiae cells. FEMS Yeast Res. 2021;21:1–12. doi: 10.1093/femsyr/foab015. PubMed DOI
Diskowski M., Mikusevic V., Stock C., Hänelt I. Functional diversity of the superfamily of K+ transporters to meet various requirements. Biol. Chem. 2015;396:1003–1014. doi: 10.1515/hsz-2015-0123. PubMed DOI
Huang C., Pedersen B.P., Stokes D.L. Crystal Structure of the Potassium Importing KdpFABC Membrane Complex. Nature. 2017;546:681–685. doi: 10.1038/nature22970. PubMed DOI PMC
Stock C., Hielkema L., Tascón I., Wunnicke D., Oostergetel G.T., Azkargorta M., Paulino C., Hänelt I. Cryo-EM structures of KdpFABC suggest a K+ transport mechanism via two inter-subunit half-channels. Nat. Commun. 2018;9:1–10. doi: 10.1038/s41467-018-07319-2. PubMed DOI PMC
Durell S.R., Guy H.R. Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K+ channel. Biophys. J. 1999;77:789–807. doi: 10.1016/S0006-3495(99)76932-8. PubMed DOI PMC
Durell S.R., Hao Y., Nakamura T., Bakker E.P., Guy H.R. Evolutionary relationship between K+ channels and symporters. Biophys. J. 1999;77:775–788. doi: 10.1016/S0006-3495(99)76931-6. PubMed DOI PMC
Doyle D.A., Cabral J.M., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The Structure of the PotassiumChannel: Molecular Basis of K+ Conduction and Selectivity. Science. 1998;280:1–9. doi: 10.1126/science.280.5360.69. PubMed DOI
Kale D., Spurny P., Shamayeva K., Spurna K., Kahoun D., Ganser D., Zayats V., Ludwig J. The S. cerevisiae cation translocation protein Trk1 is functional without its “long hydrophilic loop” but LHL regulates cation translocation activity and selectivity. Biochim. Et Biophys. Acta Biomembr. 2019;1861:1476–1488. doi: 10.1016/j.bbamem.2019.06.010. PubMed DOI
Zayats V., Stockner T., Pandey S.K., Wörz K., Ettrich R., Ludwig J. A refined atomic scale model of the Saccharomyces cerevisiae K+-translocation protein Trk1p combined with experimental evidence confirms the role of selectivity filter glycines and other key residues. Biochim. Et Biophys. Acta Biomembr. 2015;1848:1183–1195. doi: 10.1016/j.bbamem.2015.02.007. PubMed DOI
Cao Y., Jin X., Huang H., Derebe M.G., Levin E.J., Kabaleeswaran V., Pan Y., Punta M., Love J., Weng J., et al. Crystal structure of a potassium ion transporter, TrkH. Nature. 2011;471:336–341. doi: 10.1038/nature09731. PubMed DOI PMC
Vieira-Pires R.S., Szollosi A., Morais-Cabral J.H. The structure of the KtrAB potassium transporter. Nature. 2013;496:323–328. doi: 10.1038/nature12055. PubMed DOI
Kuroda T., Bihler H., Bashi E., Slayman C.L., Rivetta A. Chloride channel function in the yeast TRK-potassium transporters. J. Membr. Biol. 2004;198:177–192. doi: 10.1007/s00232-004-0671-1. PubMed DOI
Pardo J.P., González-Andrade M., Allen K., Kuroda T., Slayman C.L., Rivetta A. A structural model for facultative anion channels in an oligomeric membrane protein: The yeast TRK (K+) system. Pflug. Arch. Eur. J. Physiol. 2015;467:2447–2460. doi: 10.1007/s00424-015-1712-6. PubMed DOI
Ariño J., Aydar E., Drulhe S., Ganser D., Jorrín J., Kahm M., Krause F., Petrezsélyová S., Yenush L., Zimmermannová O. Systems Biology of Monovalent Cation Homeostasis in Yeast. The Translucent Contribution. Adv. Microb. Physiol. 2014;64:1–63. doi: 10.1016/b978-0-12-800143-1.00001-4. PubMed DOI
Ramos J., Haro R., Rodriguez-Navarro A. Regulation of potassium fluxes in Saccharomyces cerevisiae. BBA Biomembr. 1990;1029:211–217. doi: 10.1016/0005-2736(90)90156-I. PubMed DOI
Ramos J., Rodriguez-Navarro A. Regulation and interconversion of the potassium transport systems of Saccharomyces cerevisiae as revealed by rubidium transport. Eur. J. Biochem. 1986;154:307–311. doi: 10.1111/j.1432-1033.1986.tb09398.x. PubMed DOI
Rodriguez-Navarro A., Ramos J. Dual System for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 1984;159:940–945. doi: 10.1128/jb.159.3.940-945.1984. PubMed DOI PMC
Masaryk J., Sychrová H. Yeast Trk1 Potassium Transporter Gradually Changes Its Affinity in Response to Both External and Internal Signals. J. Fungi. 2022;8:432. doi: 10.3390/jof8050432. PubMed DOI PMC
Boles E., Hollenberg C.P. The molecular genetics of hexose transport in yeasts. FEMS Microbiol. Rev. 1997;21:85–111. doi: 10.1111/j.1574-6976.1997.tb00346.x. PubMed DOI
Kim J.-H., Roy A., Jouandot D., Cho K.H. The glucose signaling network in yeast. Biochim. Et Biophys. Acta Gen. Subj. 2013;1830:5204–5210. doi: 10.1016/j.bbagen.2013.07.025. PubMed DOI PMC
Pacheco A., Donzella L., Hernandez-Lopez M.J., Almeida M.J., Prieto J.A., Randez-Gil F., Morrissey J.P., Sousa M.J. Hexose transport in Torulaspora delbrueckii: Identification of Igt1, a new dual-affinity transporter. FEMS Yeast Res. 2020;20:1–10. doi: 10.1093/femsyr/foaa004. PubMed DOI
Fu H.H., Luan S. AtKUP1: A dual-affinity K+ transporter from Arabidopsis. Plant Cell. 1998;10:63–73. doi: 10.1105/tpc.10.1.63. PubMed DOI PMC
Kim E.J., Kwak J.M., Uozumi N., Schroeder J.I. AtKUP1: An arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell. 1998;10:51–62. doi: 10.1105/tpc.10.1.51. PubMed DOI PMC
Tsay Y.F., Schroeder J.I., Feldmann K.A., Crawford N.M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell. 1993;72:705–713. doi: 10.1016/0092-8674(93)90399-B. PubMed DOI
Sun J., Bankston J.R., Payandeh J., Hinds T.R., Zagotta W.N., Zheng N. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature. 2014;507:73–77. doi: 10.1038/nature13074. PubMed DOI PMC
Brachmann C., Davies A., Cost G.J., Caputo E., Li J., Hieter P., Boeke J.D. Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 1998;14:115–132. doi: 10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2. PubMed DOI
Zahrádka J., Sychrová H. Plasma-membrane hyperpolarization diminishes the cation efflux via Nha1 antiporter and Ena ATPase under potassium-limiting conditions. FEMS Yeast Res. 2012;12:439–446. doi: 10.1111/j.1567-1364.2012.00793.x. PubMed DOI
Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 2002;20:87–90. doi: 10.1038/nbt0102-87. PubMed DOI
Güldener U., Heck S., Fiedler T., Beinhauer J., Hegemann J.H. A New Efficient Gene Disruption Cassette for Repeated Use in Budding Yeast. Nucleic Acids Res. 1996;24:2519–2524. doi: 10.1093/nar/24.13.2519. PubMed DOI PMC
Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989;77:51–59. doi: 10.1016/0378-1119(89)90358-2. PubMed DOI
Gietz R.D., Schiestl R.H. Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2007;2:1–4. doi: 10.1038/nprot.2007.17. PubMed DOI
Shamayeva K., Spurna K., Kulik N., Kale D., Munko O., Spurny P., Zayats V., Ludwig J. MPM motifs of the yeast SKT protein Trk1 can assemble to form a functional K+-translocation system. Biochim. Et Biophys. Acta Biomembr. 2021;1863:183513. doi: 10.1016/j.bbamem.2020.183513. PubMed DOI
Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC
Buchroithner B., Mayr S., Hauser F., Priglinger E., Stangl H., Santa-Maria A.R., Deli M.A., Der A., Klar T.A., Axmann M., et al. Dual channel microfluidics for mimicking the blood-brain barrier. ACS Nano. 2021;15:2984–2993. doi: 10.1021/acsnano.0c09263. PubMed DOI PMC
Hauser F., Jacak J. Real-time 3D single-molecule localization microscopy analysis using lookup tables. Biomed. Opt. Express. 2021;12:4955. doi: 10.1364/BOE.424016. PubMed DOI PMC
Falk T., Mai D., Bensch R., Çiçek Ö., Abdulkadir A., Marrakchi Y., Böhm A., Deubner J., Jäckel Z., Seiwald K., et al. U-Net: Deep learning for cell counting, detection, and morphometry. Nat. Methods. 2019;16:67–70. doi: 10.1038/s41592-018-0261-2. PubMed DOI
Krieger E., Koraimann G., Vriend G. Increasing the Precision of Comparative Models with YASARA NOVA—A Self-Parameterizing Force Field. PROTEINS: Struct. Funct. Genet. 2002;47:393–402. doi: 10.1002/prot.10104. PubMed DOI
Huang J., Rauscher S., Nawrocki G., Ran T., Feig M., de Groot B.L., Grubmüller H., MacKerell A.D., Jr. CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nat. Methods. 2016;14:71–73. doi: 10.1038/nmeth.4067. PubMed DOI PMC
Krieger E., Nielsen J.E., Spronk C.A., Vriend G. Fast empirical pKa prediction by Ewald summation. J. Mol. Graph. Model. 2006;25:481–486. doi: 10.1016/j.jmgm.2006.02.009. PubMed DOI
Schneidman-Duhovny D., Inbar Y., Nussinov R., Wolfson H.J. PatchDock and SymmDock: Servers for rigid and symmetric docking. Nucleic Acids Research. 2005;33((Suppl. 2)):363–367. doi: 10.1093/nar/gki481. PubMed DOI PMC
Madden T.L., Tatusov R.L., Zhang J. Applications of network BLAST server. Computer methods for macromolecular sequence analysis. Methods Enzymol. 1996;266:131–141. PubMed
Cuff J.A., Clamp M.E., Siddiqui A.S., Finlay M., Barton G. JPred: A consensus secondary structure prediction server. Bioinformatics. 1998;14:892–893. doi: 10.1093/bioinformatics/14.10.892. PubMed DOI
Yang J., Yan R., Roy A., Xu D., Poisson J., Zhang Y. The I-TASSER suite: Protein structure and function prediction. Nat. Methods. 2014;12:7–8. doi: 10.1038/nmeth.3213. PubMed DOI PMC
Canutescu A.A., Dunbrack R.L. Cyclic coordinate descent: A robotics algorithm for protein loop closure. Protein Sci. 2003;12:963–972. doi: 10.1110/ps.0242703. PubMed DOI PMC
Konagurthu A., Whisstock J., Stuckey P., Lesk A. MUSTANG: A Multiple Structural Alignment Algorithm. Proteins Struct. Funct. Bioinform. 2006;14:659–664. doi: 10.1002/prot.20921. PubMed DOI