A sensitive and specific genetically-encoded potassium ion biosensor for in vivo applications across the tree of life
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
Grantová podpora
P30 GM138396
NIGMS NIH HHS - United States
R01 GM095903
NIGMS NIH HHS - United States
U24 NS109107
NINDS NIH HHS - United States
FS-154310
CIHR - Canada
Howard Hughes Medical Institute - United States
PubMed
36067248
PubMed Central
PMC9481166
DOI
10.1371/journal.pbio.3001772
PII: PBIOLOGY-D-22-00474
Knihovny.cz E-zdroje
- MeSH
- biosenzitivní techniky * metody MeSH
- draslík MeSH
- ionty MeSH
- myši MeSH
- rezonanční přenos fluorescenční energie * metody MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Názvy látek
- draslík MeSH
- ionty MeSH
Potassium ion (K+) plays a critical role as an essential electrolyte in all biological systems. Genetically-encoded fluorescent K+ biosensors are promising tools to further improve our understanding of K+-dependent processes under normal and pathological conditions. Here, we report the crystal structure of a previously reported genetically-encoded fluorescent K+ biosensor, GINKO1, in the K+-bound state. Using structure-guided optimization and directed evolution, we have engineered an improved K+ biosensor, designated GINKO2, with higher sensitivity and specificity. We have demonstrated the utility of GINKO2 for in vivo detection and imaging of K+ dynamics in multiple model organisms, including bacteria, plants, and mice.
Center for Translational Neuromedicine University of Copenhagen Copenhagen Denmark
Department of Biochemistry University of Alberta Edmonton Alberta Canada
Department of Biology University of Iowa Iowa City Iowa United States of America
Department of Chemistry The University of Tokyo Tokyo Japan
Department of Chemistry University of Alberta Edmonton Alberta Canada
Department of Experimental Plant Biology Charles University Prague Czech Republic
Department of Physiology University of Alberta Edmonton Alberta Canada
Janelia Research Campus Howard Hughes Medical Institute Ashburn Virginia United States of America
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Palmer BF. Regulation of Potassium Homeostasis. Clin J Am Soc Nephrol. 2015;10:1050–1060. doi: 10.2215/CJN.08580813 PubMed DOI PMC
Udensi UK, Tchounwou PB. Potassium Homeostasis, Oxidative Stress, and Human Disease. Int J Clin Exp Physiol. 2017;4:111–122. doi: 10.4103/ijcep.ijcep_43_17 PubMed DOI PMC
Epstein W. The roles and regulation of potassium in bacteria. Prog Nucleic Acid Res Mol Biol. 2003;75:293–320. doi: 10.1016/s0079-6603(03)75008-9 PubMed DOI
Beagle SD, Lockless SW. Unappreciated Roles for K+ Channels in Bacterial Physiology. Trends Microbiol. 2021;29:942–950. doi: 10.1016/j.tim.2020.11.005 PubMed DOI PMC
Zhao Y, Araki S, Wu J, Teramoto T, Chang Y-F, Nakano M, et al.. An expanded palette of genetically encoded Ca2+ indicators. Science. 2011;333:1888–1891. PubMed PMC
Dana H, Sun Y, Mohar B, Hulse BK, Kerlin AM, Hasseman JP, et al.. High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat Methods. 2019;16:649–657. doi: 10.1038/s41592-019-0435-6 PubMed DOI
Frant MS, Ross JW Jr. Potassium ion specific electrode with high selectivity for potassium over sodium. Science. 1970;167:987–988. doi: 10.1126/science.167.3920.987 PubMed DOI
Minta A, Tsien RY. Fluorescent indicators for cytosolic sodium. J Biol Chem. 1989;264:19449–19457. PubMed
Wang Z, Detomasi TC, Chang CJ. A dual-fluorophore sensor approach for ratiometric fluorescence imaging of potassium in living cells. Chem Sci. 2020;12:1720–1729. doi: 10.1039/d0sc03844j PubMed DOI PMC
Liu J, Li F, Wang Y, Pan L, Lin P, Zhang B, et al.. A sensitive and specific nanosensor for monitoring extracellular potassium levels in the brain. Nat Nanotechnol. 2020;1720–1729. PubMed
Liu J, Pan L, Shang C, Lu B, Wu R, Feng Y, et al.. A highly sensitive and selective nanosensor for near-infrared potassium imaging. Sci Adv. 2020;6:eaax9757. doi: 10.1126/sciadv.aax9757 PubMed DOI PMC
Ashraf KU, Josts I, Mosbahi K, Kelly SM, Byron O, Smith BO, et al.. The Potassium Binding Protein Kbp Is a Cytoplasmic Potassium Sensor. Structure. 2016;24:741–749. doi: 10.1016/j.str.2016.03.017 PubMed DOI
Shen Y, Wu S-Y, Rancic V, Aggarwal A, Qian Y, Miyashita S-I, et al.. Genetically encoded fluorescent indicators for imaging intracellular potassium ion concentration. Commun Biol. 2019;2:18. doi: 10.1038/s42003-018-0269-2 PubMed DOI PMC
Bischof H, Rehberg M, Stryeck S, Artinger K, Eroglu E, Waldeck-Weiermair M, et al.. Novel genetically encoded fluorescent probes enable real-time detection of potassium in vitro and in vivo. Nat Commun. 2017;8:1422. doi: 10.1038/s41467-017-01615-z PubMed DOI PMC
Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, et al.. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 1998;280:69–77. doi: 10.1126/science.280.5360.69 PubMed DOI
Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V, et al.. Crystal structure of a potassium ion transporter, TrkH. Nature. 2011;471:336–340. PubMed PMC
Neupert-Laves K, Dobler M. The crystal structure of a K+ complex of valinomycin. Helv Chim Acta. 1975;58:432–442. doi: 10.1002/hlca.19750580212 PubMed DOI
Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature. 2001;414:43–48. doi: 10.1038/35102009 PubMed DOI
Liu S, Li S, Yang Y, Li W. Termini restraining of small membrane proteins enables structure determination at near-atomic resolution. Sci Adv. 2020;6:abe3717. doi: 10.1126/sciadv.abe3717 PubMed DOI PMC
Ding J, Luo AF, Hu L, Wang D, Shao F. Structural basis of the ultrasensitive calcium indicator GCaMP6. Sci China Life Sci. 2014;57:269–274. doi: 10.1007/s11427-013-4599-5 PubMed DOI
Wang Q, Shui B, Kotlikoff MI, Sondermann H. Structural basis for calcium sensing by GCaMP2. Structure. 2008;16:1817–1827. doi: 10.1016/j.str.2008.10.008 PubMed DOI PMC
Nasu Y, Shen Y, Kramer L, Campbell RE. Structure- and mechanism-guided design of single fluorescent protein-based biosensors. Nat Chem Biol. 2021;17:509–518. doi: 10.1038/s41589-020-00718-x PubMed DOI
Yamagata N. The concentration of common cesium and rubidium in human body. J Radiat Res. 1962;3:9–30. doi: 10.1269/jrr.3.9 PubMed DOI
Miesenbock G, De Angelis DA, Rothman JE. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature. 1998;394:192–195. doi: 10.1038/28190 PubMed DOI
Sustr M, Soukup A, Tylova E. Potassium in Root Growth and Development. Plan Theory. 2019;8:435. PubMed PMC
Hasanuzzaman M, Bhuyan MHMB, Nahar K, Hossain MS, Mahmud JA, Hossen MS, et al.. Potassium: A Vital Regulator of Plant Responses and Tolerance to Abiotic Stresses. Agronomy. 2018;8:31.
Walker DJ, Leigh RA, Miller AJ. Potassium homeostasis in vacuolate plant cells. Proc Natl Acad Sci U S A. 1996;93:10510–10514. doi: 10.1073/pnas.93.19.10510 PubMed DOI PMC
Tamura K, Shimada T, Ono E, Tanaka Y, Nagatani A, Higashi S-I, et al.. Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J. 2003;35:545–555. doi: 10.1046/j.1365-313x.2003.01822.x PubMed DOI
Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiol Plant. 2008;133:651–669. doi: 10.1111/j.1399-3054.2007.01008.x PubMed DOI
Felle HH. pH regulation in anoxic plants. Ann Bot. 2005;96:519–532. doi: 10.1093/aob/mci207 PubMed DOI PMC
Halperin SJ, Gilroy S, Lynch JP. Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. J Exp Bot. 2003;54:1269–1280. PubMed
Moseyko N, Feldman LJ. Expression of pH-sensitive green fluorescent protein in Arabidopsis thaliana. Plant Cell Environ. 2001;24:557–563. PubMed
Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M, Karimi M, et al.. Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr Biol. 2014;24:931–940. doi: 10.1016/j.cub.2014.03.025 PubMed DOI
Pietrobon D, Moskowitz MA. Chaos and commotion in the wake of cortical spreading depression and spreading depolarizations. Nat Rev Neurosci. 2014;15:379–393. doi: 10.1038/nrn3770 PubMed DOI
Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev. 2001;81:1065–1096. doi: 10.1152/physrev.2001.81.3.1065 PubMed DOI
Burgstaller S, Bischof H, Rauter T, Schmidt T, Schindl R, Patz S, et al.. Immobilization of Recombinant Fluorescent Biosensors Permits Imaging of Extracellular Ion Signals. ACS Sens. 2021;6:3994–4000. doi: 10.1021/acssensors.1c01369 PubMed DOI PMC
Patterson GH, Knobel SM, Sharif WD, Kain SR, Piston DW. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys J. 1997;73:2782–2790. doi: 10.1016/S0006-3495(97)78307-3 PubMed DOI PMC
Mutch WA, Hansen AJ. Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J Cereb Blood Flow Metab. 1984;4:17–27. doi: 10.1038/jcbfm.1984.3 PubMed DOI
Shen Y, Rosendale M, Campbell RE, Perrais D. pHuji, a pH-sensitive red fluorescent protein for imaging of exo- and endocytosis. J Cell Biol. 2014;207:419–432. doi: 10.1083/jcb.201404107 PubMed DOI PMC
Somjen GG. Ion regulation in the brain: implications for pathophysiology. Neuroscientist. 2002;8:254–267. doi: 10.1177/1073858402008003011 PubMed DOI
Barnett LM, Hughes TE, Drobizhev M. Deciphering the molecular mechanism responsible for GCaMP6m’s Ca2+−dependent change in fluorescence. PLoS ONE. 2017;12:e0170934. doi: 10.1371/journal.pone.0170934 PubMed DOI PMC
Molina RS, Qian Y, Wu J, Shen Y, Campbell RE, Drobizhev M, et al.. Understanding the Fluorescence Change in Red Genetically Encoded Calcium Ion Indicators. Biophys J. 2019;116:1873–1886. doi: 10.1016/j.bpj.2019.04.007 PubMed DOI PMC
Tao R, Zhao Y, Chu H, Wang A, Zhu J, Chen X, et al.. Genetically encoded fluorescent sensors reveal dynamic regulation of NADPH metabolism. Nat Methods. 2017;14:720–728. doi: 10.1038/nmeth.4306 PubMed DOI PMC
Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr. 2010;66:125–132. doi: 10.1107/S0907444909047337 PubMed DOI PMC
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658–674. doi: 10.1107/S0021889807021206 PubMed DOI PMC
Trigo-Mourino P, Thestrup T, Griesbeck O, Griesinger C, Becker S. Dynamic tuning of FRET in a green fluorescent protein biosensor. Sci Adv. 2019;5:eaaw4988. doi: 10.1126/sciadv.aaw4988 PubMed DOI PMC
Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66:486–501. doi: 10.1107/S0907444910007493 PubMed DOI PMC
Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, et al.. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66:213–221. doi: 10.1107/S0907444909052925 PubMed DOI PMC
Cranfill PJ, Sell BR, Baird MA, Allen JR, Lavagnino Z, de Gruiter HM, et al.. Quantitative assessment of fluorescent proteins. Nat Methods. 2016;13:557–562. doi: 10.1038/nmeth.3891 PubMed DOI PMC
Drobizhev M, Molina R, Hughes T. Characterizing the Two-photon Absorption Properties of Fluorescent Molecules in the 680–1300 nm Spectral Range. Bio Protoc. 2020;10:e3498. doi: 10.21769/BioProtoc.3498 PubMed DOI PMC
Brown SD, Jun S. Complete Genome Sequence of Escherichia coli NCM3722. Genome Announc. 2015;3:e00879–e00815. doi: 10.1128/genomeA.00879-15 PubMed DOI PMC
Sarrion-Perdigones A, Vazquez-Vilar M, Palací J, Castelijns B, Forment J, Ziarsolo P, et al.. GoldenBraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiol. 2013;162:1618–1631. doi: 10.1104/pp.113.217661 PubMed DOI PMC
Ishige F, Takaichi M, Foster R, Chua N-H, Oeda K. A G-box motif (GCCACGTGCC) tetramer confers high-level constitutive expression in dicot and monocot plants. Plant J. 1999;18:443–448.
Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. PubMed
Serre NBC, Kralík D, Yun P, Slouka Z, Shabala S, Fendrych M. AFB1 controls rapid auxin signalling through membrane depolarization in Arabidopsis thaliana root. Nat Plants. 2021;7:1229–1238. PubMed PMC
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al.. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019 PubMed DOI PMC
Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118:401–415. doi: 10.1242/dev.118.2.401 PubMed DOI
Kay AR, Raccuglia D, Scholte J, Sivan-Loukianova E, Barwacz CA, Armstrong SR, et al.. Goggatomy: A Method for Opening Small Cuticular Compartments in Arthropods for Physiological Experiments. Front Physiol. 2016;7:398. doi: 10.3389/fphys.2016.00398 PubMed DOI PMC
