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Time-Gated FRET Detection for Multiplexed Biosensing

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Reviews in Fluorescence 2016

Part of the book series: Reviews in Fluorescence ((RFLU))

Abstract

Förster resonance energy transfer (FRET) has become an indispensable technique for biosensing in both microscopy and spectroscopy. FRET based on photoluminescence intensity and lifetime is both well known. However, their combination into time-gated (TG) intensity detection has been much less exploited, although many commercial diagnostic/screening assays and academic studies concerning TG FRET have demonstrated the successful application since more than two decades. In this chapter we explain the theoretical and practical background of TG FRET and discuss various applications. In particular, multiplexed detection of biomolecules and/or biomolecular interactions using photoluminescence spectroscopy and microscopy and the advantages and limitations of TG FRET compared to other technologies will be discussed.

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References

  1. Haugland RP (2005) The handbook. a guide to fluorescent probes and labeling technologies, 10 edn. Invitrogen, San Diego

    Google Scholar 

  2. Hötzer B, Medintz IL, Hildebrandt N (2012) Fluorescence in nanobiotechnology: sophisticated fluorophores for novel applications. Small 8(15):2297–2326

    Article  PubMed  CAS  Google Scholar 

  3. Sapsford KE, Berti L, Medintz IL (2006) Materials for fluorescence resonance energy tansfer analysis: beyond traditional donor-acceptor combinations. Angew Chem Int Ed 45(28):4562–4589

    Article  CAS  Google Scholar 

  4. Sapsford KE, Wildt B, Mariani A, Yeatts AB, Medintz IL (2014) Materials for FRET analysis: beyond traditonal dye-dye combinations. In: Medintz IL, Hildebrandt N (eds) FRET – Förster Resonance Energy Transfer. From theory to applications. Wiley-VCH, Singapore

    Google Scholar 

  5. Andrews DL, Demidov AA (1999) Resonance energy transfer. Wiley, Chichester

    Google Scholar 

  6. Clegg RM (1996) Fluorescence resonance energy transfer. In: Wang XF, Herman B (eds) Fluorescence imaging spectroscopy and microscopy. Wiley, New York, pp 179–251

    Google Scholar 

  7. Clegg RM (2009) Förster resonance energy transfer - FRET what is it, why do it, and how it’s done. In: Gadella TWJ (ed) Laboratory techniques in biochemistry and molecular biology. Academic, Burlington, pp 1–57

    Google Scholar 

  8. Gadella TWJ. (2009); FRET and FLIM techniques. Elsevier, Amsterdam/London p xxiii, 534 p

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Medintz IL, Hildebrandt N (2014) FRET - Förster Resonance Energy Transfer. From theory to applications. Wiley-VCH, Weinheim, p. 105

    Google Scholar 

  11. Periasamy A, Day RN (2005) Molecular imaging : FRET microscopy and spectroscopy. Oxford University Press, New York; Oxford. p xv, 312 p

    Google Scholar 

  12. Selvin PR (1996) Lanthanide-based resonance energy transfer. IEEE J Sel Top Quant Electron 2(4):1077–1087

    Article  CAS  Google Scholar 

  13. Vogel, S. S.; Thaler, C.; Koushik, S. V. (2006) Fanciful FRET.. Sci. STKE 2006 (331), re2

    Google Scholar 

  14. Lakowicz J R (2006) Principles of fluorescence spectroscopy, 3rd ed. Springer, New York. p xxvi, 954 p

    Google Scholar 

  15. Turro NJ, Ramamurthy V, Scaiano JC (2009) Principles of molecular photochemistry: an introduction. University Science Books, Sausalito

    Google Scholar 

  16. Turro N J, Ramamurthy V, Scaiano J C (2010) Modern molecular photochemistry of organic molecules. University Science Books, Sausalito, Calif. p xxxiii, 1084 p

    Google Scholar 

  17. Valeur B, Berberan-Santos MN (2013) Molecular fluorescence: principles and applications, 2nd edn. WIley-VCH Verlag & Co. KGaA, Weinheim

    Google Scholar 

  18. Algar WR, Kim H, Medintz IL, Hildebrandt N (2014) Emerging non-traditional Förster resonance energy transfer configurations with semiconductor quantum dots: Investigations and applications. Coord Chem Rev 263:65–85

    Article  CAS  Google Scholar 

  19. Hildebrandt N, Wegner KD, Algar WR (2014) Luminescent terbium complexes: superior Förster resonance energy transfer donors for flexible and sensitive multiplexed biosensing. Coord Chem Rev 273:125–138

    Article  CAS  Google Scholar 

  20. Cardoso Dos Santos M, Hildebrandt N (2016) Recent developments in lanthanide-to-quantum dot FRET using time-gated fluorescence detection and photon upconversion. TrAC Trends Anal Chem 84:60–71

    Article  CAS  Google Scholar 

  21. Sy M, Nonat A, Hildebrandt N, Charbonniere LJ (2016) Lanthanide-based luminescence biolabelling. Chem Commun 52(29):5080–5095

    Article  CAS  Google Scholar 

  22. Bünzli JCG (2010) Lanthanide luminescence for biomedical analyses and imaging. Chem Rev 110(5):2729–2755

    Article  PubMed  CAS  Google Scholar 

  23. Eliseeva SV, Bünzli JCG (2010) Lanthanide luminescence for functional materials and bio-sciences. Chem Soc Rev 39(1):189–227

    Article  CAS  PubMed  Google Scholar 

  24. Zwier JM, Bazin H, Lamarque L, Mathis G (2014) Luminescent lanthanide cryptates: from the bench to the bedside. Inorg Chem 53(4):1854–1866

    Article  CAS  PubMed  Google Scholar 

  25. Montgomery CP, Murray BS, New EJ, Pal R, Parker D (2009) Cell-penetrating metal complex optical probes: targeted and responsive systems based on lanthanide luminescence. Acc Chem Res 42(7):925–937

    Article  CAS  PubMed  Google Scholar 

  26. New EJ, Parker D, Smith DG, Walton JW (2010) Development of responsive lanthanide probes for cellular applications. Curr Opin Chem Biol 14:238–246

    Article  CAS  PubMed  Google Scholar 

  27. Scholler P, Zwier JM, Trinquet E, Rondard P, Pin J-P, Prézeau L, Kniazeff J (2013) Time-resolved Förster resonance energy transfer-based technologies to investigate G protein-coupled receptor machinery: high-throughput screening and future development. Prog Mol Biol Transl Sci 113:275–312

    Article  CAS  PubMed  Google Scholar 

  28. Charbonnière LJ, Hildebrandt N (2008) Lanthanide complexes and quantum dots: a bright wedding for resonance energy transfer. Eur J Inorg Chem 21:3241–3251

    Article  CAS  Google Scholar 

  29. Geißler D, Linden S, Liermann K, Wegner KD, Charbonnière LJ, Hildebrandt N (2014) Lanthanides and quantum dots as Förster resonance energy transfer agents for diagnostics and cellular imaging. Inorg Chem 53(4):1824–1838

    Article  PubMed  CAS  Google Scholar 

  30. Geißler D, Hildebrandt N (2011) Lanthanide complexes in FRET applications. Curr Inorg Chem 1(1):17–35

    Article  Google Scholar 

  31. Selvin PR (2002) Principles and biophysical applications of lanthanide-based probes. Annu Rev Biophys Biomol Struct 31:275–302

    Article  CAS  PubMed  Google Scholar 

  32. Trinquet E, Mathis G (2006) Fluorescence technologies for the investigation of chemical libraries. Mol BioSyst 2(8):380–387

    Article  CAS  PubMed  Google Scholar 

  33. Mathis G (1995) Probing molecular interactions with homogeneous techniques based on rare earth cryptates and fluorescence energy transfer. Clin Chem 41:1391–1397

    CAS  PubMed  Google Scholar 

  34. Jin ZW, Geißler D, Qiu X, Wegner KD, Hildebrandt N (2015) A rapid, amplification-free, and sensitive diagnostic assay for single-step multiplexed fluorescence detection of microRNA. Angewandte Chemie-International Edition 54(34):10024–10029

    Article  CAS  PubMed  Google Scholar 

  35. Alpha B, Lehn JM, Mathis G (1987) Energy-transfer luminescence of europium(III) and terbium(III) cryptates of macrobicyclic polypyridine ligands. Angewandte Chemie-International Edition 26(3):266–267

    Article  Google Scholar 

  36. Degorce F, Card A, Soh S, Trinquet E, Knapik GP, Xie B (2009) HTRF: a technology tailored for drug discovery – a review of theoretical aspects and recent applications. Curr Inorg Chem 3:22–32

    CAS  Google Scholar 

  37. Cisbio Bioassays HTRF® Technology (2016) http://www.cisbio.com/drug-discovery/htrf-technology

  38. Cezanne/BRAHMS/ThermoFisher Scientific: TRACE-Technology (2016) http://www.brahms-instruments.com/

  39. Xu J, Corneillie TM, Moore EG, Law G-L, Butlin NG, Raymond KN (2011) Octadentate cages of Tb(III) 2-hydroxyisophthalamides: a new standard for luminescent lanthanide labels. J Am Chem Soc 133(49):19900–19910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lumiphore (2016) http://www.lumiphore.com

  41. Trinquet E, Maurin F, Preaudat M, Mathis G (2001) Allophycocyanin 1 as a near infrared fluorescent tracer: isolation, characterization, chemical modification and use in a homogeneous fluorescence energy transfer system. Anal Biochem 296:126–135

    Article  CAS  Google Scholar 

  42. Zwier JM, Roux T, Cottet M, Durroux T, Douzon S, Bdioui S, Gregor N, Bourrier E, Oueslati N, Nicolas L, Tinel N, Boisseau C, Yverneau P, Charrier-Savournin F, Fink M, Trinquet E (2010) A fluorescent ligand-binding alternative using Tag-lite® technology. J Biomol Screen 15(10):1248–1259

    Article  CAS  PubMed  Google Scholar 

  43. Doumazane E, Scholler P, Fabre L, Zwier JM, Trinquet E, Pin J-P, Rondard P (2013) Illuminating the activation mechanisms and allosteric properties of metabotropic glutamate receptors. Proc Natl Acad Sci 110(15):E1416–E1425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Trinquet E, Fink M, Bazin H, Grillet F, Maurin F, Bourrier E, Ansanay H, Leroy C, Michaud A, Durroux T, Maurel D, Malhaire F, Goudet C, Pin J-P, Naval M, Hernout O, Chrétien F, Chapleur Y, Mathis G (2006) d-myo-Inositol 1-phosphate as a surrogate of d-myo-inositol 1,4,5-tris phosphate to monitor G protein-coupled receptor activation. Anal Biochem 358(1):126–135

    Article  CAS  PubMed  Google Scholar 

  45. Perkin Elmer LANCE Technology (2016) http://www.perkinelmer.com/category/lance-tr-fret

  46. Hemmilä I, Webb S (1997) Time-resolved fluorometry: an overview of the labels and core technologies for drug screening applications. Drug Discov Today 2(9):373–381

    Article  Google Scholar 

  47. ThermoFisher Scientific LanthaScreen Technology (2016) http://www.thermofisher.com/us/en/home/industrial/pharma-biopharma/drug-discovery-development/target-and-lead-identification-and-validation/kinasebiology/kinase-activity-assays/lanthascreen-tr-fret-toolbox.html

  48. Ge P, Selvin PR (2008) New 9-or 10-dentate luminescent lanthanide chelates. Bioconjug Chem 19(5):1105–1111

    Article  CAS  PubMed  Google Scholar 

  49. Geißler D, Stufler S, Löhmannsröben H-G, Hildebrandt N (2013) Six-color time-resolved förster resonance energy transfer for ultrasensitive multiplexed biosensing. J Am Chem Soc 135(3):1102–1109

    Article  PubMed  CAS  Google Scholar 

  50. Hilal T, Puetter V, Otto C, Parczyk K, Bader B (2010) A dual estrogen receptor TR-FRET assay for simultaneous measurement of steroid site binding and coactivator recruitment. J Biomol Screen 15(3):268–278

    Article  CAS  PubMed  Google Scholar 

  51. Jeyakumar M, Katzenellenbogen JA (2009) A dual-acceptor time-resolved Förster resonance energy transfer assay for simultaneous determination of thyroid hormone regulation of corepressor and coactivator binding to the thyroid hormone receptor: mimicking the cellular context of thyroid hormone action. Anal Biochem 386(1):73–78

    Article  CAS  PubMed  Google Scholar 

  52. Kim SH, Gunther JR, Katzenellenbogen JA (2010) Monitoring a coordinated exchange process in a four-component biological interaction system: development of a time-resolved terbium-based one-donor/three-acceptor multicolor FRET system. J Am Chem Soc 132(13):4685–4692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kokko T, Kokko L, Soukka T (2009) Terbium(III) chelate as an efficient donor for multiple-wavelength fluorescent acceptors. J Fluoresc 19(1):159–164

    Article  CAS  PubMed  Google Scholar 

  54. Kokko T, Liljenback T, Peltola MT, Kokko L, Soukka T (2008) Homogeneous dual-parameter assay for prostate-specific antigen based on fluorescence resonance energy transfer. Anal Chem 80(24):9763–9768

    Article  CAS  PubMed  Google Scholar 

  55. Kupcho KR, Stafslien DK, DeRosier T, Hallis TM, Ozers MS, Vogel KW (2007) Simultaneous monitoring of discrete binding events using dual-acceptor terbium-based LRET. J Am Chem Soc 129(44):13372

    Article  CAS  PubMed  Google Scholar 

  56. Baldo B, Paganetti P, Grueninger S, Marcellin D, Kaltenbach LS, Lo DC, Semmelroth M, Zivanovic A, Abramowski D, Smith D, Lotz GP, Bates GP, Weiss A (2012) TR-FRET-based duplex immunoassay reveals an inverse correlation of soluble and aggregated mutant huntingtin in Huntington’s Disease. Chem Biol 19(2):264–275

    Article  CAS  PubMed  Google Scholar 

  57. Comps-Agrar L, Kniazeff J, Brock C, Trinquet E, Pin J-P (2012) Stability of GABAB receptor oligomers revealed by dual TR-FRET and drug-induced cell surface targeting. FASEB J 26(8):3430–3439

    Article  CAS  PubMed  Google Scholar 

  58. Bhuckory S, Lefebvre O, Qiu X, Wegner KD, Hildebrandt N (2016) Evaluating quantum dot performance in homogeneous FRET immunoassays for prostate specific antigen. Sensors 16(2):197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Geißler D, Charbonniere LJ, Ziessel RF, Butlin NG, Löhmannsröben H-G, Hildebrandt N (2010) Quantum dot biosensors for ultrasensitive multiplexed diagnostics. Angew Chem Int Edn 49(8):1396–1401

    Article  CAS  Google Scholar 

  60. Geißler D, Hildebrandt N (2016) Recent developments in Förster resonance energy transfer (FRET) diagnostics using quantum dots. Anal Bioanal Chem 408(17):4475–4483

    Article  PubMed  CAS  Google Scholar 

  61. Morgner F, Stufler S, Geißler D, Medintz IL, Algar WR, Susumu K, Stewart MH, Blanco-Canosa JB, Dawson PE, Hildebrandt N (2011) Terbium to quantum dot FRET bioconjugates for clinical diagnostics: influence of human plasma on optical and assembly properties. Sensors 11(10):9667–9684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Qiu X, Hildebrandt N (2015) Rapid and multiplexed microRNA diagnostic assay using quantum dot-based forster resonance energy transfer. ACS Nano 9(8):8449–8457

    Article  CAS  PubMed  Google Scholar 

  63. Wegner KD, Jin ZW, Linden S, Jennings TL, Hildebrandt N (2013) Quantum-dot-based förster resonance energy transfer immunoassay for sensitive clinical diagnostics of low-volume serum samples. ACS Nano 7(8):7411–7419

    Article  CAS  PubMed  Google Scholar 

  64. Wegner KD, Lanh PT, Jennings T, Oh E, Jain V, Fairclough SM, Smith JM, Giovanelli E, Lequeux N, Pons T, Hildebrandt N (2013) Influence of luminescence quantum yield, surface coating, and functionalization of quantum dots on the sensitivity of time-resolved FRET bioassays. ACS Appl Mater Interfaces 5:2881–2892

    Article  CAS  PubMed  Google Scholar 

  65. Wegner KD, Linden S, Jin ZW, Jennings TL, el Khoulati R, van Bergen en Henegouwen PMP, Hildebrandt N (2014) Nanobodies and nanocrystals: highly sensitive quantum dot-based homogeneous FRET immunoassay for serum-Based EGFR Detection. Small 10(4):734–740

    Article  CAS  PubMed  Google Scholar 

  66. Connally R, Jin D, Piper J (2006) High intensity solid-state UV source for time-gated luminescence microscopy. Cytometry Part A 69A(9):1020–1027

    Article  Google Scholar 

  67. Gahlaut N, Miller LW (2010) Time-resolved microscopy for imaging lanthanide luminescence in living cells. Cytometry Part A 77A(12):1113–1125

    Article  CAS  Google Scholar 

  68. Grichine A, Haefele A, Pascal S, Duperray A, Michel R, Andraud C, Maury O (2014) Millisecond lifetime imaging with a europium complex using a commercial confocal microscope under one or two-photon excitation. Chem Sci 5(9):3475–3485

    Article  CAS  Google Scholar 

  69. Ramshesh VK, Lemasters JJ (2008) Pinhole shifting lifetime imaging microscopy. J Biomed Opt 13(6):064001–064010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Butler SJ, Delbianco M, Lamarque L, McMahon BK, Neil ER, Pal R, Parker D, Walton JW, Zwier JM (2015) EuroTracker® dyes: design, synthesis, structure and photophysical properties of very bright europium complexes and their use in bioassays and cellular optical imaging. Dalton Trans 44(11):4791–4803

    Article  CAS  PubMed  Google Scholar 

  71. Pal R (2015) Phase modulation nanoscopy: a simple approach to enhanced optical resolution. Faraday Discuss 177:507–515

    Article  CAS  PubMed  Google Scholar 

  72. Liao Z, Tropiano M, Faulkner S, Vosch T, Sorensen TJ (2015) Time-resolved confocal microscopy using lanthanide centred near-IR emission. RSC Adv 5(86):70282–70286

    Article  CAS  Google Scholar 

  73. Rajendran M, Miller LW (2015) Evaluating the performance of time-gated live-cell microscopy with lanthanide Probes. Biophys J 109(2):240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rajendran M, Yapici E, Miller LW (2014) Lanthanide-based imaging of protein–protein interactions in live cells. Inorg Chem 53(4):1839–1853

    Article  CAS  PubMed  Google Scholar 

  75. Vicidomini G, Moneron G, Han KY, Westphal V, Ta H, Reuss M, Engelhardt J, Eggeling C, Hell SW (2011) Sharper low-power STED nanoscopy by time gating. Nat Methods 8(7):571–573

    Article  CAS  PubMed  Google Scholar 

  76. Vaasa A, Ligi K, Mohandessi S, Enkvist E, Uri A, Miller LW (2012) Time-gated luminescence microscopy with responsive nonmetal probes for mapping activity of protein kinases in living cells. Chem Commun 48(68):8595–8597

    Article  CAS  Google Scholar 

  77. Soini E, Lövgren T, Reimer CB (1987) Time-resolved fluorescence of lanthanide probes and applications in biotechnology. CRC Crit Rev Anal Chem 18(2):105–154

    Article  CAS  Google Scholar 

  78. Beverloo HB, van Schadewijk A, Bonnet J, van der Geest R, Runia R, Verwoerd NP, Vrolijk J, Ploem JS, Tanke HJ (1992) Preparation and microscopic visualization of multicolor luminescent immunophosphors. Cytometry 13(6):561–570

    Article  CAS  PubMed  Google Scholar 

  79. Seveus LVM, Syrjänen S, Sandberg M, Kuusisto A, Harju R, Salo J, Hemmilä I, Kojola H, E. S (1992) Time-resolved fluorescence imaging of europium chelate label in immunohistochemistry and in situ hybridization. Cytometry 13(4):329–338

    Article  CAS  PubMed  Google Scholar 

  80. Marriott G, Heidecker M, Diamandis EP, Yan-Marriott Y (1994) Time-resolved delayed luminescence image microscopy using an europium ion chelate complex. Biophys J 67(3):957–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Vereb G, Jares-Erijman E, Selvin PR, Jovin TM (1998) Temporally and spectrally resolved imaging microscopy of lanthanide chelates. Biophys J 74(5):2210–2222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Moore EG, Samuel APS, Raymond KN (2009) From antenna to assay: lessons learned in lanthanide luminescence. Acc Chem Res 42(4):542–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Härmä H, Soukka T, Lövgren T (2001) Europium nanoparticles and time resolved fluorescence for ultrasensitive detection of prostate specific antigen. Clin Chem 47:561–568

    PubMed  Google Scholar 

  84. Lu Y, Zhao J, Zhang R, Liu Y, Liu D, Goldys EM, Yang X, Xi P, Sunna A, Lu J, Shi Y, Leif RC, Huo Y, Shen J, Piper JA, Robinson JP, Jin D (2014) Tunable lifetime multiplexing using luminescent nanocrystals. Nat Photonics 8(1):32–36

    Article  CAS  Google Scholar 

  85. Wang F, Deng R, Wang J, Wang Q, Han Y, Zhu H, Chen X, Liu X (2011) Tuning upconversion through energy migration in core–shell nanoparticles. Nat Mater 10(12):968–973

    Article  CAS  PubMed  Google Scholar 

  86. Beeby A, Botchway SW, Clarkson IM, Faulkner S, Parker AW, Parker D, Williams JAG (2000) Luminescence imaging microscopy and lifetime mapping using kinetically stable lanthanide(III) complexes. Journal of Photochemistry and Photobiology B: Biology 57:83–89

    Google Scholar 

  87. Charbonnière L, Ziessel R, Guardigli M, Roda A, Sabbatini N, Cesario M (2001) Lanthanide tags for time-resolved luminescence microscopy displaying improved stability and optical properties. J Am Chem Soc 123(10):2436–2437

    Article  PubMed  CAS  Google Scholar 

  88. Hanaoka K, Kikuchi K, Kobayashi S, Nagano T (2007) Time-resolved long-lived luminescence imaging method employing luminescent lanthanide probes with a new microscopy system. J Am Chem Soc 129(44):13502–13509

    Article  CAS  PubMed  Google Scholar 

  89. Liu M, Ye Z, Wang G, Yuan J (2012) Development of a novel europium(III) complex-based luminescence probe for time-resolved luminescence imaging of the nitric oxide production in neuron cells. Talanta 99:951–958

    Article  CAS  PubMed  Google Scholar 

  90. Liu M, Ye Z, Xin C, Yuan J (2013) Development of a ratiometric time-resolved luminescence sensor for pH based on lanthanide complexes. Anal Chim Acta 761:149–156

    Article  CAS  PubMed  Google Scholar 

  91. Montgomery CP, New EJ, Palsson LO, Parker D, Batsanov AS, Lamarque L (2009) Emissive and Cell-Permeable 3-Pyridyl- and 3-Pyrazolyl-4-azaxanthone lanthanide complexes and their behaviour in cellulo. Helvetica Chimica Acta 92(11):2186–2213

    Article  CAS  Google Scholar 

  92. Pandya S, Yu J, Parker D (2006) Engineering emissive europium and terbium complexes for molecular imaging and sensing. Dalton Trans 23:2757–2766

    Article  CAS  Google Scholar 

  93. Poole RA, C. M, EJ N, Congreve A, Parker D, Botta M (2007) Identification of emissive lanthanide complexes suitable for cellular imaging that resist quenching by endogenous anti-oxidants. Org Biomol Chem 5(13):2055–2062

    Article  CAS  PubMed  Google Scholar 

  94. Smith DG, McMahon BK, Pal R, Parker D (2012) Live cell imaging of lysosomal pH changes with pH responsive ratiometric lanthanide probes. Chem Commun 48(68):8520–8522

    Article  CAS  Google Scholar 

  95. Song B, Ye Z, Yang Y, Ma H, Zheng X, Jin D, Yuan J (2015) Background-free in-vivo imaging of Vitamin C using time-gateable responsive probe. Sci Rep 5:14194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Song B, Wang G, Tan M, Yuan J (2006) A europium(III) complex as an efficient singlet oxygen luminescence probe. J Am Chem Soc 128(41):13442–13450

    Article  CAS  PubMed  Google Scholar 

  97. Sun J, Song B, Ye Z, Yuan J (2015) Mitochondria targetable time-gated luminescence probe for singlet oxygen based on a β-Diketonate–Europium complex. Inorg Chem 54(24):11660–11668

    Article  CAS  PubMed  Google Scholar 

  98. Walton JW, Bourdolle A, Butler SJ, Soulie M, Delbianco M, McMahon BK, Pal R, Puschmann H, Zwier JM, Lamarque L, Maury O, Andraud C, Parker D (2013) Very bright europium complexes that stain cellular mitochondria. Chem Commun 49(16):1600–1602

    Article  CAS  Google Scholar 

  99. D’Aléo A, Pompidor G, Elena B, Vicat J, Baldeck PL, Toupet L, Kahn R, Andraud C, Maury O (2007) Two-photon microscopy and spectroscopy of lanthanide bioprobes. ChemPhysChem 8(14):2125–2132

    Article  PubMed  CAS  Google Scholar 

  100. Piszczek G, Maliwall BP, Gryczynskil I, Dattelbaum J, Lakowicz JR (2001) Multiphoton Ligand-Enhanced Excitation of Lanthanides. J Fluoresc 11(2):101–107

    Article  CAS  Google Scholar 

  101. Werts MHV, Nerambourg N, Pelegry D, Le Grand Y, Blanchard-Desce M (2005) Action cross sections of two-photon excited luminescence of some Eu(III) and Tb(III) complexes. Photochem Photobiol Sci 4(7):531–538

    Article  CAS  PubMed  Google Scholar 

  102. Bourdolle A, D’Aléo A, Philippot C, Baldeck PL, Guyot Y, Dubois F, Ibanez A, Andraud C, Brasselet S, Maury O (2016) NIR-to-NIR two-photon scanning laser microscopy imaging of single nanoparticles doped by YbIII complexes. ChemPhysChem 17(1):128–135

    Article  CAS  PubMed  Google Scholar 

  103. D’Aléo A, Bourdolle A, Brustlein S, Fauquier T, Grichine A, Duperray A, Baldeck PL, Andraud C, Brasselet S, Maury O (2012) Ytterbium-based bioprobes for near-infrared two-photon scanning laser microscopy imaging. Angew Chem 124(27):6726–6729

    Article  Google Scholar 

  104. Picot A, D’Aléo A, Baldeck PL, Grichine A, Duperray A, Andraud C, Maury O (2008) Long-lived two-photon excited luminescence of water-soluble europium complex: applications in biological imaging using two-photon scanning microscopy. J Am Chem Soc 130(5):1532–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ghose S, Trinquet E, Laget M, Bazin H, Mathis G (2008) Rare earth cryptates for the investigation of molecular interactions in vitro and in living cells. J Alloys Compd 451(1–2):35–37

    Article  CAS  Google Scholar 

  106. Fernandez-Moreira V, Song B, Sivagnanam V, Chauvin AS, Vandevyver CDB, Gijs M, Hemmilä I, Lehr HA, Bünzli JCG (2010) Bioconjugated lanthanide luminescent helicates as multilabels for lab-on-a-chip detection of cancer biomarkers. Analyst 135:42–52

    Article  CAS  PubMed  Google Scholar 

  107. Albizu L, Cottet M, Kralikova M, Stoev S, Seyer R, Brabet I, Roux T, Bazin H, Bourrier E, Lamarque L, Breton C, Rives M-L, Newman A, Javitch J, Trinquet E, Manning M, Pin J-P, Mouillac B, Durroux T (2010) Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat Chem Biol 6(8):587–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Doumazane E, Scholler P, Zwier JM, Trinquet E, Rondard P, Pin J-P (2011) A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J 25(1):66–77

    Article  CAS  PubMed  Google Scholar 

  109. Bourdolle A, Allali M, Mulatier J-C, Le Guennic B, Zwier JM, Baldeck PL, Bünzli J-CG, Andraud C, Lamarque L, Maury O (2011) Modulating the photophysical properties of azamacrocyclic europium complexes with charge-transfer antenna chromophores. Inorg Chem:4987–4999

    Google Scholar 

  110. Takalo H, Hemmilä I, Sutela T, Latva M (1996) Synthesis and luminescence of novel EuIII complexing agents and labels with 4-(Phenylethynyl)pyridine subunits. Helv Chim Acta 79(3):789–802

    Article  CAS  Google Scholar 

  111. Butler SJ, Lamarque L, Pal R, Parker D (2014) EuroTracker dyes: highly emissive europium complexes as alternative organelle stains for live cell imaging. Chem Sci:1750–1756

    Google Scholar 

  112. Soulié M, Latzko F, Bourrier E, Placide V, Butler SJ, Pal R, Walton JW, Baldeck PL, Le Guennic B, Andraud C, Zwier JM, Lamarque L, Parker D, Maury O (2014) Comparative analysis of conjugated alkynyl chromophore-triazacyclononane ligands for sensitized emission of europium and terbium. Chem Eur J 20:8636–8646

    Article  PubMed  CAS  Google Scholar 

  113. Delbianco M, Sadovnikova V, Bourrier E, Mathis G, Lamarque L, Zwier JM, Parker D (2014) Bright, highly water-Soluble Triazacyclononane europium complexes to detect ligand binding with time-resolved FRET microscopy. Angew Chem Int Ed 53:10718–10722

    Article  CAS  Google Scholar 

  114. Starck M, Pal R, Parker D (2016) Structural control of cell permeability with highly emissive europium(III) complexes permits different microscopy applications. Chem Eur J 22(2):570–580

    Article  CAS  PubMed  Google Scholar 

  115. Placide V, Pitrat D, Grichine A, Duperray A, Andraud C, Maury O (2014) Design and synthesis of europium luminescent bio-probes featuring sulfobetaine moieties. Tetrahedron Lett 55(7):1357–1361

    Article  CAS  Google Scholar 

  116. Keppler A, Gendreizig S, Gronemeyer T, Pick H, H V, Johnsson K (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 21:86–89

    Article  CAS  PubMed  Google Scholar 

  117. Placide V, Bui AT, Grichine A, Duperray A, Pitrat D, Andraud C, Maury O (2015) Two-photon multiplexing bio-imaging using a combination of Eu- and Tb-bioprobes. Dalton Trans 44(11):4918–4924

    Article  CAS  PubMed  Google Scholar 

  118. Bui AT, Grichine A, Brasselet S, Duperray A, Andraud C, Maury O (2015) Unexpected efficiency of a luminescent samarium(iii) complex for combined visible and near-infrared biphotonic microscopy. Chem Eur J 21(49):17757–17761

    Article  CAS  PubMed  Google Scholar 

  119. Perfetto SP, Chattopadhyay PK, Roederer M (2004) Seventeen-colour flow cytometry: unravelling the immune system. Nat Rev Immunol 4(8):648–655

    Article  CAS  PubMed  Google Scholar 

  120. Lu J, Martin J, Lu Y, Zhao J, Yuan J, Ostrowski M, Paulsen I, Piper JA, Jin D (2012) Resolving low-expression cell surface antigens by time-gated orthogonal scanning automated microscopy. Anal Chem 84(22):9674–9678

    Article  CAS  PubMed  Google Scholar 

  121. Lu Y, Jin D, Leif RC, Deng W, Piper JA, Yuan J, Duan Y, Huo Y (2011) Automated detection of rare-event pathogens through time-gated luminescence scanning microscopy. Cytometry 79A(5):349–355

    Article  Google Scholar 

  122. Lu Y, Lu J, Zhao J, Cusido J, Raymo FM, Yuan J, Yang S, Leif RC, Huo Y, Piper JA, Paul Robinson J, Goldys EM, Jin D (2014) On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays. Nat Commun 5:3741

    Google Scholar 

  123. Lu Y, Xi P, Piper JA, Huo Y, Jin D (2012) Time-gated orthogonal scanning automated microscopy (osam) for high-speed cell detection and analysis. Sci Rep 2:837

    PubMed  PubMed Central  Google Scholar 

  124. Wu J, Ye Z, Wang G, Jin D, Yuan J, Guan Y, Piper J (2009) Visible-light-sensitized highly luminescent europium nanoparticles: preparation and application for time-gated luminescence bioimaging. J Mater Chem 19(9):1258–1264

    Article  CAS  Google Scholar 

  125. Jin D, Piper JA (2011) Time-gated luminescence microscopy allowing direct visual inspection of lanthanide-stained microorganisms in background-free condition. Anal Chem 83(6):2294–2300

    Article  CAS  PubMed  Google Scholar 

  126. Zhang L, Zheng X, Deng W, Lu Y, Lechevallier S, Ye Z, Goldys EM, Dawes JM, Piper JA, Yuan J, Verelst M, Jin D (2014) Practical implementation characterization and applications of a multi-colour time-gated luminescence microscope. Sci Rep 4:6597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Charbonnière LJ, Hildebrandt N, Ziessel RF, Löhmannsröben H-G (2006) Lanthanides to quantum dots resonance energy transfer in time-resolved fluoro-immunoassays and luminescence microscopy. J Am Chem Soc 128(39):12800–12809

    Article  PubMed  CAS  Google Scholar 

  128. Rajapakse HE, Gahlaut N, Mohandessi S, Yu D, Turner JR, Miller LW (2010) Time-resolved luminescence resonance energy transfer imaging of protein-protein interactions in living cells. Proc Natl Acad Sci 107:13582–13587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Mohandessi S, Rajendran M, Magda D, Miller LW (2012) Cell-penetrating peptides as delivery vehicles for a protein-targeted terbium complex. Chem Eur J 18(35):10825–10829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Maurel D, Comps-Agrar L, Brock C, Rives M-L, Bourrier E, Ayoub MA, Bazin H, Tinel N, Durroux T, Prézeau L, Trinquet E, Pin J-P (2008) Cell-surface protein-protein interaction analyses with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat Methods 5:561–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Faklaris O, Cottet M, Falco A, Villier B, Laget M, Zwier JM, Trinquet E, Mouillac B, Pin J-P, Durroux T (2015) Multicolor time-resolved Förster resonance energy transfer microscopy reveals the impact of GPCR oligomerization on internalization processes. FASEB J 29(6):2235–2246

    Article  CAS  PubMed  Google Scholar 

  132. Levoye A, Zwier JM, Jaracz-Ros A, Klipfel L, Cottet M, Maurel D, Bdioui S, Balabanian K, Prézeau L, Trinquet E, Durroux T, Bachelerie F (2015) A broad g protein-coupled receptor internalization assay that combines snap-tag labeling, diffusion-enhanced resonance energy transfer, and a highly emissive terbium cryptate. Front Endocrinol 6:167

    Article  Google Scholar 

  133. Zou X, Rajendran M, Magda D, Miller LW (2015) Cytoplasmic delivery and selective, Multicomponent labeling with oligoarginine-linked protein tags. Bioconjug Chem 26(3):460–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Gaborit N, Larbouret C, Vallaghe J, Peyrusson F, Bascoul-Mollevi C, Crapez E, Azria D, Chardes T, Poul M-A, Mathis G, Bazin H, Pélegrin A (2011) Time resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies. J Biol Chem 286:11337–11345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Ho-Pun-Cheung A, Bazin H, Gaborit N, Larbouret C, Garnero P, Assenat E, Castan F, Bascoul-Mollevi C, Ramos J, Ychou M, Pélegrin A, Mathis G, Lopez-Crapez E (2012) Quantification of HER expression and dimerization in patients tumor samples using time-resolved Förster resonance energy transfer. PLoS ONE 7(7):e37065 EP

    Article  CAS  Google Scholar 

  136. Maurel D, Kniazeff J, Mathis G, Trinquet E, Pin J-P, Ansanay H (2004) Cell surface detection of membrane protein interaction with homogeneous time-resolved fluorescence resonance energy transfer technology. Anal Biochem 329(2):253–262

    Article  CAS  PubMed  Google Scholar 

  137. Rondard P, Huang S, Monnier C, Tu H, Blanchard B, Oueslati N, Malhaire F, Li Y, Trinquet E, Labesse G, Pin J-P, Liu J (2008) Functioning of the dimeric GABAB receptor extracellular domain revealed by glycan wedge scanning. EMBO J 27:131–144

    Article  CAS  Google Scholar 

  138. Linden S, Singh MK, Wegner KD, Regairaz M, Dautry F, Treussart F, Hildebrandt N (2015) Terbium-based time-gated Forster resonance energy transfer imaging for evaluating protein-protein interactions on cell membranes. Dalton Trans 44(11):4994–5003

    Article  CAS  PubMed  Google Scholar 

  139. Afsari HS, Cardoso Dos Santos M, Lindén S, Chen T, Qiu X, van Bergen en Henegouwen PMP, Jennings TL, Susumu K, Medintz IL, Hildebrandt N, Miller LW (2016) Time-gated FRET nanoassemblies for rapid and sensitive intra- and extracellular fluorescence imaging. Sci Adv 2(6):e1600265

    Article  PubMed  PubMed Central  Google Scholar 

  140. Hildebrandt, N.; Spillmann, C. M.; Algar, W. R.; Pons, T.; Stewart, M. H.; Oh, E.; Susumu, K.; Díaz, S. A.; Delehanty, J. B.; Medintz, I. L.,2016 Energy Transfer with Semiconductor Quantum Dot Bioconjugates: A Versatile Platform for Biosensing, Energy Harvesting, and Other Developing Applications. Chem Rev. doi:10.1021/acs.chemrev.6b00030

  141. Cheng L, Yang K, Shao M, Lee S-T, Liu Z (2011) Multicolor in vivo imaging of upconversion nanoparticles with emissions tuned by luminescence resonance energy transfer. J Phys Chem C 115(6):2686–2692

    Article  CAS  Google Scholar 

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Acknowledgements

NH thanks the Institut Universitaire de France.

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Authors and Affiliations

  1. R&D, Cisbio Bioassays, Parc Marcel Boiteux, BP 84175, 30200, Codolet, France

    Jurriaan M. Zwier

  2. NanoBioPhotonics, Institute for Integrative Biology of the Cell, Université Paris-Sud, Université Paris-Saclay, CNRS, CEA, 91405, Orsay Cedex, France

    Niko Hildebrandt

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  1. Jurriaan M. Zwier
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  2. Niko Hildebrandt
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Correspondence to Jurriaan M. Zwier or Niko Hildebrandt .

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  1. Institute of Fluorescence, University of Maryland Baltimore County, Baltimore, Maryland, USA

    Chris D. Geddes

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Zwier, J.M., Hildebrandt, N. (2017). Time-Gated FRET Detection for Multiplexed Biosensing. In: Geddes, C. (eds) Reviews in Fluorescence 2016. Reviews in Fluorescence. Springer, Cham. https://doi.org/10.1007/978-3-319-48260-6_3

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