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Development of FRET biosensors for mammalian and plant systems

  • Special Issue: New/Emerging Techniques in Biological Microscopy
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Abstract

Genetically encoded biosensors are increasingly used in visualising signalling processes in different organisms. Sensors based on green fluorescent protein technology are providing a great opportunity for using Förster resonance energy transfer (FRET) as a tool that allows for monitoring dynamic processes in living cells. The development of these FRET biosensors requires careful selection of fluorophores, substrates and recognition domains. In this review, we will discuss recent developments, strategies to create and optimise FRET biosensors and applications of FRET-based biosensors for use in the two major eukaryotic kingdoms and elaborate on different methods for FRET detection.

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Abbreviations

FRET:

Förster resonance energy transfer

DNA:

Deoxyribonucleic acid

FP:

Fluorescent protein

FLIM:

Fluorescence lifetime imaging

cAMP:

Cyclic adenosine monophosphate

AvGFP:

Aequorea victoria GFP

GFP:

Green fluorescent protein

cpGFP:

Circular permuted green fluorescent protein

BFP:

Blue fluorescent protein

ECFP:

Enhanced cyan fluorescent protein

EPAC:

Exchange protein activated by cAMP

EYFP:

Enhanced yellow fluorescent protein

mRFP:

Monomeric red fluorescent protein

YC3.60:

Yellow cameleon version 3.60

cp:

Circular permutation

ER:

Endoplasmic reticulum

GTP:

Guanosine-5′-triphosphate

References

  • Adams JP, Adeli A, Hsu CY, Harkess RL, Page GP, Depamphilis CW, Schultz EB, Yuceer C (2012) Plant-based FRET biosensor discriminates environmental zinc levels. Plant biotechnology journal 10(2):207–216

    Article  CAS  PubMed  Google Scholar 

  • Adjobo-Hermans MJ, Goedhart J, van Weeren L, Nijmeijer S, Manders EM, Offermanns S, Gadella TW (2011) Real-time visualization of heterotrimeric G protein Gq activation in living cells. BMC biology 9(1):32

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ai HW, Hazelwood KL, Davidson MW, Campbell RE (2008) Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat Methods 5(5):401–403

    Article  CAS  PubMed  Google Scholar 

  • Allen MD, Zhang J (2006) Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem Biophys Res Commun 348(2):716–721

    Article  CAS  PubMed  Google Scholar 

  • Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289(5488):2338–2342

    Article  CAS  PubMed  Google Scholar 

  • Aoki K, Komatsu N, Hirata E, Kamioka Y, Matsuda M (2012) Stable expression of FRET biosensors: a new light in cancer research. Cancer Sci 103(4):614–619

    Article  CAS  PubMed  Google Scholar 

  • Aucher W, Becker E, Ma E, Miron S, Martel A, Ochsenbein F, Marsolier-Kergoat MC, Guerois R (2010) A strategy for interaction site prediction between phospho-binding modules and their partners identified from proteomic data. Mol Cell Proteomics 9(12):2745–2759

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baird GS, Zacharias DA, Tsien RY (2000) Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97(22):11984–11989

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Betzig E (2005a) Excitation strategies for optical lattice microscopy. Opt Express 13(8):3021–3036

    Article  PubMed  Google Scholar 

  • Betzig E (2005b) Multifocal three-dimensional imaging with optical lattice excitation. Microsc Microanal 11(S02):80–81

    Article  Google Scholar 

  • Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642–1645

    Article  CAS  PubMed  Google Scholar 

  • Bogner M, Ludewig U (2007) Visualization of arginine influx into plant cells using a specific FRET-sensor. J Fluoresc 17(4):350–360

    Article  CAS  PubMed  Google Scholar 

  • Bollmann JH, Helmchen F, Borst JG, Sakmann B (1998) Postsynaptic Ca2+ influx mediated by three different pathways during synaptic transmission at a calyx-type synapse. J Neurosci 18(24):10409–10419

    CAS  PubMed  Google Scholar 

  • Borst JW, Hink MA, van Hoek A, Visser AJ (2005) Effects of refractive index and viscosity on fluorescence and anisotropy decays of enhanced cyan and yellow fluorescent proteins. J Fluoresc 15(2):153–160

    Article  CAS  PubMed  Google Scholar 

  • Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482(7383):103–106

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri B, Hormann F, Lalonde S, Brady SM, Orlando DA, Benfey P, Frommer WB (2008) Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J 56(6):948–962

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chaudhuri B, Hormann F, Frommer WB (2011) Dynamic imaging of glucose flux impedance using FRET sensors in wild-type Arabidopsis plants. J Exp Bot 62(7):2411–2417

    Article  CAS  PubMed  Google Scholar 

  • Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90(3):1103–1163

    Article  CAS  PubMed  Google Scholar 

  • Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125(1):61–64

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deuschle K, Chaudhuri B, Okumoto S, Lager I, Lalonde S, Frommer WB (2006) Rapid metabolism of glucose detected with FRET glucose nanosensors in epidermal cells and intact roots of Arabidopsis RNA-silencing mutants. Plant Cell 18(9):2314–2325

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fields S, Song O (1989) A novel genetic system to detect protein–protein interactions. Nature 340(6230):245–246

    Article  CAS  PubMed  Google Scholar 

  • Fiil BK, Qiu JL, Petersen K, Petersen M, Mundy J (2008) Coimmunoprecipitation (co-IP) of nuclear proteins and chromatin immunoprecipitation (ChIP) from Arabidopsis. CSH protocols 2008:pdb prot5049

  • Förster T (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys 437(1–2):55–75

    Article  Google Scholar 

  • Fritz RD, Letzelter M, Reimann A, Martin K, Fusco L, Ritsma L, Ponsioen B, Fluri E, Schulte-Merker S, van Rheenen J, Pertz O (2013) A versatile toolkit to produce sensitive FRET biosensors to visualize signaling in time and space. Sci Signal 6(285):rs12

    Article  PubMed  Google Scholar 

  • Gao L, Shao L, Higgins CD, Poulton JS, Peifer M, Davidson MW, Wu X, Goldstein B, Betzig E (2012) Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens. Cell 151(6):1370–1385

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21(13):1598–1602

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Giavalisco P, Hummel J, Lisec J, Inostroza AC, Catchpole G, Willmitzer L (2008) High-resolution direct infusion-based mass spectrometry in combination with whole 13C metabolome isotope labeling allows unambiguous assignment of chemical sum formulas. Anal Chem 80(24):9417–9425

    Article  CAS  PubMed  Google Scholar 

  • Giavalisco P, Kohl K, Hummel J, Seiwert B, Willmitzer L (2009) 13C isotope-labeled metabolomes allowing for improved compound annotation and relative quantification in liquid chromatography-mass spectrometry-based metabolomic research. Anal Chem 81(15):6546–6551

    Article  CAS  PubMed  Google Scholar 

  • Giurumescu CA, Kang S, Planchon TA, Betzig E, Bloomekatz J, Yelon D, Cosman P, Chisholm AD (2012) Quantitative semi-automated analysis of morphogenesis with single-cell resolution in complex embryos. Development 139(22):4271–4279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goedhart J, Vermeer JE, Adjobo-Hermans MJ, van Weeren L, Gadella TW Jr (2007) Sensitive detection of p65 homodimers using red-shifted and fluorescent protein-based FRET couples. PLoS One 2(10):e1011

    Article  PubMed Central  PubMed  Google Scholar 

  • Goedhart J, van Weeren L, Hink MA, Vischer NO, Jalink K, Gadella TW Jr (2010) Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat Methods 7(2):137–139

    Article  CAS  PubMed  Google Scholar 

  • Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, van Weeren L, Gadella TW Jr, Royant A (2012) Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93 %. Nat Commun 3:751

    Article  PubMed Central  PubMed  Google Scholar 

  • Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein mechanism and applications. Journal of Biological Chemistry 276(31):29188–29194

    Article  CAS  PubMed  Google Scholar 

  • Grunberg R, Burnier JV, Ferrar T, Beltran-Sastre V, Stricher F, van der Sloot AM, Garcia-Olivas R, Mallabiabarrena A, Sanjuan X, Zimmermann T, Serrano L (2013) Engineering of weak helper interactions for high-efficiency FRET probes. Nat Methods 10:1021–1027

    Article  PubMed  Google Scholar 

  • Haccoun J, Piro B, Tran LD, Dang LA, Pham MC (2004) Reagentless amperometric detection of l-lactate on an enzyme-modified conducting copolymer poly (5-hydroxy-1,4-naphthoquinone-co-5-hydroxy-3-thioacetic acid-1,4-naphthoquinone). Biosens Bioelectron 19(10):1325–1329

    Article  CAS  PubMed  Google Scholar 

  • Haugh JM (2012) Live-cell fluorescence microscopy with molecular biosensors: what are we really measuring? Biophys J 102(9):2003–2011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heim R, Tsien RY (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6(2):178–182

    Article  CAS  PubMed  Google Scholar 

  • Hess A, Sergejeva M, Budinsky L, Zeilhofer HU, Brune K (2007) Imaging of hyperalgesia in rats by functional MRI. Eur J Pain 11(1):109–119

    Article  PubMed  Google Scholar 

  • Hires SA, Zhu Y, Tsien RY (2008) Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc Natl Acad Sci 105(11):4411–4416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J, Rasmussen SG, Sunahara RK, El-Samad H, Huang B, von Zastrow M (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495(7442):534–538

    Article  CAS  PubMed  Google Scholar 

  • Jares-Erijman EA, Jovin TM (2003) FRET imaging. Nat Biotechnol 21(11):1387–1395

    Article  CAS  PubMed  Google Scholar 

  • Ji N, Magee JC, Betzig E (2008a) High-speed, low-photodamage nonlinear imaging using passive pulse splitters. Nat Methods 5(2):197–202

    Article  CAS  PubMed  Google Scholar 

  • Ji N, Shroff H, Zhong H, Betzig E (2008b) Advances in the speed and resolution of light microscopy. Curr Opin Neurobiol 18(6):605–616

    Article  CAS  PubMed  Google Scholar 

  • Ji N, Sato TR, Betzig E (2012) Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex. Proc Natl Acad Sci U S A 109(1):22–27

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones AM, Grossmann G, Danielson JA, Sosso D, Chen LQ, Ho CH, Frommer WB (2013a) In vivo biochemistry: applications for small molecule biosensors in plant biology. Curr Opin Plant Biol 16(3):389–395

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones AM, Grossmann G, Danielson JA, Sosso D, Chen LQ, Ho CH, Frommer WB (2013b) In vivo biochemistry: applications for small molecule biosensors in plant biology. Curr Opin Plant Biol 16:389–395

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klarenbeek JB, Goedhart J, Hink MA, Gadella TW, Jalink K (2011) A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS One 6(4):e19170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Komatsu N, Aoki K, Yamada M, Yukinaga H, Fujita Y, Kamioka Y, Matsuda M (2011) Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol Biol Cell 22(23):4647–4656

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci U S A 105(28):9823–9828

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kotera I, Iwasaki T, Imamura H, Noji H, Nagai T (2010) Reversible dimerization of Aequorea victoria fluorescent proteins increases the dynamic range of FRET-based indicators. ACS Chem Biol 5(2):215–222

    Article  CAS  PubMed  Google Scholar 

  • Kramer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Current opinion in biotechnology 16(2):133–141

    Article  PubMed  Google Scholar 

  • Krebs M, Held K, Binder A, Hashimoto K, Den Herder G, Parniske M, Kudla J, Schumacher K (2012) FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca(2)(+) dynamics. Plant J 69(1):181–192

    Article  CAS  PubMed  Google Scholar 

  • Lakowicz JR, Gryczynski I, Gryczynski Z, Dattelbaum JD (1999) Anisotropy-based sensing with reference fluorophores. Anal Biochem 267(2):397–405

    Article  CAS  PubMed  Google Scholar 

  • Lam AJ, St-Pierre F, Gong Y, Marshall JD, Cranfill PJ, Baird MA, McKeown MR, Wiedenmann J, Davidson MW, Schnitzer MJ (2012) Improving FRET dynamic range with bright green and red fluorescent proteins. Nat Methods

  • Lin W, Lu D, Gao X, Jiang S, Ma X, Wang Z, Mengiste T, He P, Shan L (2013) Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc Natl Acad Sci U S A 110(29):12114–12119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mancuso S, Marras AM, Magnus V, Baluska F (2005) Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Anal Biochem 341(2):344–351

    Article  CAS  PubMed  Google Scholar 

  • Mang A, Pill J, Gretz N, Kranzlin B, Buck H, Schoemaker M, Petrich W (2005) Biocompatibility of an electrochemical sensor for continuous glucose monitoring in subcutaneous tissue. Diabetes Technol Ther 7(1):163–173

    Article  CAS  PubMed  Google Scholar 

  • Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, Betzig E, Lippincott-Schwartz J (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5(2):155–157

    Article  CAS  PubMed  Google Scholar 

  • Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52(5):973–986

    Article  CAS  PubMed  Google Scholar 

  • Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48(6):883–894

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388(6645):882–887

    Article  CAS  PubMed  Google Scholar 

  • Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21(8):2341–2356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mues M, Bartholomaus I, Thestrup T, Griesbeck O, Wekerle H, Kawakami N, Krishnamoorthy G (2013) Real-time in vivo analysis of T cell activation in the central nervous system using a genetically encoded calcium indicator. Nat Med 19(6):778–783

    Article  CAS  PubMed  Google Scholar 

  • Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20(1):87–90

    Article  CAS  PubMed  Google Scholar 

  • Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101(29):10554–10559

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nguyen AW, Daugherty PS (2005) Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat Biotechnol 23(3):355–360

    Article  CAS  PubMed  Google Scholar 

  • Ni Q, Titov DV, Zhang J (2006) Analyzing protein kinase dynamics in living cells with FRET reporters. Methods 40(3):279–286

    Article  CAS  PubMed  Google Scholar 

  • Nienhaus GU (2008) The green fluorescent protein: a key tool to study chemical processes in living cells. Angewandte Chemie 47(47):8992–8994

    Article  CAS  PubMed  Google Scholar 

  • Okumoto S, Jones A, Frommer WB (2012) Quantitative imaging with fluorescent biosensors. Annu Rev Plant Biol 63:663–706

    Article  CAS  PubMed  Google Scholar 

  • Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, Baker D, Tsien RY (2006) Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13(5):521–530

    Article  CAS  PubMed  Google Scholar 

  • Piljic A, Schultz C (2008) Simultaneous recording of multiple cellular events by FRET. ACS Chem Biol 3(3):156–160

    Article  CAS  PubMed  Google Scholar 

  • Piljic A, de Diego I, Wilmanns M, Schultz C (2011) Rapid development of genetically encoded FRET reporters. ACS Chem Biol 6(7):685–691

    Article  CAS  PubMed  Google Scholar 

  • Roderick HL, Bootman MD (2006) New Ca2+ indicator has freedom to express. Chem Biol 13(5):463–464

    Article  CAS  PubMed  Google Scholar 

  • Roh-Johnson M, Shemer G, Higgins CD, McClellan JH, Werts AD, Tulu US, Gao L, Betzig E, Kiehart DP, Goldstein B (2012) Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 335(6073):1232–1235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sadanandom A, Napier RM (2010) Biosensors in plants. Curr Opin Plant Biol 13(6):736–743

    Article  CAS  PubMed  Google Scholar 

  • Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341(6148):889–892

    Article  CAS  PubMed  Google Scholar 

  • Shaner NC, Lambert GG, Chammas A, Ni Y, Cranfill PJ, Baird MA, Sell BR, Allen JR, Day RN, Israelsson M, Davidson MW, Wang J (2013) A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat Methods 10(5):407–409

    Article  CAS  PubMed  Google Scholar 

  • Shcherbakova DM, Hink MA, Joosen L, Gadella TW, Verkhusha VV (2012) An orange fluorescent protein with a large Stokes shift for single-excitation multicolor FCCS and FRET imaging. J Am Chem Soc 134(18):7913–7923

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shcherbo D, Murphy CS, Ermakova GV, Solovieva EA, Chepurnykh TV, Shcheglov AS, Verkhusha VV, Pletnev VZ, Hazelwood KL, Roche PM, Lukyanov S, Zaraisky AG, Davidson MW, Chudakov DM (2009a) Far-red fluorescent tags for protein imaging in living tissues. Biochem J 418(3):567–574

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shcherbo D, Souslova EA, Goedhart J, Chepurnykh TV, Gaintzeva A, Shemiakina II, Gadella TW, Lukyanov S, Chudakov DM (2009b) Practical and reliable FRET/FLIM pair of fluorescent proteins. BMC Biotechnol 9:24

    Article  PubMed Central  PubMed  Google Scholar 

  • Shimozono S, Hosoi H, Mizuno H, Fukano T, Tahara T, Miyawaki A (2006) Concatenation of cyan and yellow fluorescent proteins for efficient resonance energy transfer. Biochemistry 45(20):6267–6271

    Article  CAS  PubMed  Google Scholar 

  • Shroff H, Galbraith CG, Galbraith JA, White H, Gillette J, Olenych S, Davidson MW, Betzig E (2007) Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc Natl Acad Sci U S A 104(51):20308–20313

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shroff H, Galbraith CG, Galbraith JA, Betzig E (2008a) Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 5(5):417–423

    Article  CAS  PubMed  Google Scholar 

  • Shroff H, White H, Betzig E (2008b) Photoactivated localization microscopy (PALM) of adhesion complexes. Curr Protoc Cell Biol Chapter 4:Unit 4 21

    Google Scholar 

  • Spiering JJB-C, Yasmin Moshfegh, Veronika Miskolci, Louis Hodgson (2013) Quantitative Ratiometric imaging of FRET-biosensors in living cells. Methods Cell Biol 114:593–609, Digital Microscopy

    Article  PubMed Central  PubMed  Google Scholar 

  • Stein F, Kress M, Reither S, Piljic A, Schultz C (2013) FluoQ: a tool for rapid analysis of multiparameter fluorescence imaging data applied to oscillatory events. ACS Chem Biol 8:1862–1868

    Google Scholar 

  • Subach FV, Subach OM, Gundorov IS, Morozova KS, Piatkevich KD, Cuervo AM, Verkhusha VV (2009) Monomeric fluorescent timers that change color from blue to red report on cellular trafficking. Nature chemical biology 5(2):118–126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suhling K, French PM, Phillips D (2005) Time-resolved fluorescence microscopy. Photochemical & photobiological sciences. Official journal of the European Photochemistry Association and the European Society for Photobiology 4(1):13–22

    Article  CAS  Google Scholar 

  • Tembe S, Inamdar S, Haram S, Karve M, D’Souza SF (2007) Electrochemical biosensor for catechol using agarose-guar gum entrapped tyrosinase. J Biotechnol 128(1):80–85

    Article  CAS  PubMed  Google Scholar 

  • Terskikh A, Fradkov A, Ermakova G, Zaraisky A, Tan P, Kajava AV, Zhao X, Lukyanov S, Matz M, Kim S, Weissman I, Siebert P (2000) “Fluorescent timer”: protein that changes color with time. Science 290(5496):1585–1588

    Article  CAS  PubMed  Google Scholar 

  • Tsien RY (1998) The green fluorescent protein. Annual review of biochemistry 67:509–544

    Article  CAS  PubMed  Google Scholar 

  • Valeur KR, Degli Agosti R (2002) Simulations of temperature sensitivity of the peroxidase-oxidase oscillator. Biophys Chem 99(3):259–270

    Article  CAS  PubMed  Google Scholar 

  • van der Krogt GN, Ogink J, Ponsioen B, Jalink K (2008) A comparison of donor-acceptor pairs for genetically encoded FRET sensors: application to the Epac cAMP sensor as an example. PLoS One 3(4):e1916

    Article  PubMed Central  PubMed  Google Scholar 

  • van Rheenen J, Langeslag M, Jalink K (2004) Correcting confocal acquisition to optimize imaging of fluorescence resonance energy transfer by sensitized emission. Biophys J 86(4):2517–2529

    Article  PubMed Central  PubMed  Google Scholar 

  • VanEngelenburg SB, Palmer AE (2008) Fluorescent biosensors of protein function. Curr Opin Chem Biol 12(1):60–65

    Article  CAS  PubMed  Google Scholar 

  • Vinkenborg JL, Evers TH, Reulen SW, Meijer E, Merkx M (2007) Enhanced sensitivity of FRET-based protease sensors by redesign of the GFP Dimerization interface. ChemBioChem 8(10):1119–1121

    Article  CAS  PubMed  Google Scholar 

  • Violin JD, Zhang J, Tsien RY, Newton AC (2003) A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J Cell Biol 161(5):899–909

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Werthmann RC, Von Hayn K, Nikolaev VO, Lohse MJ, Bünemann M (2009) Real-time monitoring of cAMP levels in living endothelial cells: thrombin transiently inhibits adenylyl cyclase 6. J Physiol 587(16):4091–4104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilmes S, Staufenbiel M, Lisse D, Richter CP, Beutel O, Busch KB, Hess ST, Piehler J (2012) Triple-color super-resolution imaging of live cells: resolving submicroscopic receptor organization in the plasma membrane. Angew Chem Int Ed Engl 51(20):4868–4871

    Article  CAS  PubMed  Google Scholar 

  • Wysocki LM, Grimm JB, Tkachuk AN, Brown TA, Betzig E, Lavis LD (2011) Facile and general synthesis of photoactivatable xanthene dyes. Angew Chem Int Ed Engl 50(47):11206–11209

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou X, Herbst-Robinson KJ, Zhang J (2012) Visualizing dynamic activities of signaling enzymes using genetically encodable FRET-based biosensors from designs to applications. Methods Enzymol 504:317–340

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are very grateful to Prof. Dr. A.J.W.G. Visser and A.H. Westphal for critical reading of this manuscript. J.G and L.v.V.V are supported by NanoNextNL, a micro- and nanotechnology consortium of the Government of The Netherlands and 130 partners. DH is funded by The Netherlands Organisation for Scientific Research (NWO) in the framework of Earth and Life Sciences open program.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratory of Biochemistry and Microspectroscopy Centre, Wageningen University, Wageningen, The Netherlands

    Danny Hamers & Jan Willem Borst

  2. Molecular Cytology, Swammerdam Institute for Life Sciences, van Leeuwenhoek Centre for Advanced Microscopy, University of Amsterdam, Amsterdam, The Netherlands

    Laura van Voorst Vader & Joachim Goedhart

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  1. Danny Hamers
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  2. Laura van Voorst Vader
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  4. Joachim Goedhart
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Hamers, D., van Voorst Vader, L., Borst, J.W. et al. Development of FRET biosensors for mammalian and plant systems. Protoplasma 251, 333–347 (2014). https://doi.org/10.1007/s00709-013-0590-z

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  • DOI: https://doi.org/10.1007/s00709-013-0590-z

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