• Journal of Innovative Optical Health Sciences
  • Vol. 13, Issue 3, 2030006 (2020)
Wenzhao Yang1 and Sung-Liang Chen1、2、*
Author Affiliations
  • 1University of Michigan-Shanghai, Jiao Tong University Joint Institute, Shanghai Jiao Tong University, Shanghai 200240, P. R. China
  • 2State Key Laboratory of Advanced Optical, Communication Systems and Networks, Shanghai Jiao Tong University, Shanghai 200240, P. R. China
  • show less
    DOI: 10.1142/s1793545820300062 Cite this Article
    Wenzhao Yang, Sung-Liang Chen. Time-gated fluorescence imaging: Advances in technology and biological applications[J]. Journal of Innovative Optical Health Sciences, 2020, 13(3): 2030006 Copy Citation Text show less
    References

    [1] E. J. Soini, L. J. Pelliniemi, I. A. Hemmila, V. M. Mukkala, J. J. Kankare, K. Fr€ojdman, "Lanthanide chelates as new fluorochrome labels for cytochemistry," J. Histochem. Cytochem. 36(11), 1449–1451 (1988).

    [2] S. Andersson-Engels, C. af Klinteberg, K. Svanberg, S. Svanberg, "In vivo fluorescence imaging for tissue diagnostics," Phys. Med. Biol. 42(5), 815 (1997).

    [3] J. V. Frangioni, "In vivo near-infrared fluorescence imaging," Curr. Opin. Chem. Biol. 7(5), 626–634 (2003).

    [4] T. Terai, T. Nagano, "Fluorescent probes for bioimaging applications," Curr. Opin. Chem. Biol. 12(5), 515–521 (2008).

    [5] U. Resch-Genger, M. Grabolle, S. Cavaliere-Jaricot, R. Nitschke, T. Nann, "Quantum dots versus organic dyes as fluorescent labels," Nat. Meth. 5(9), 763 (2008).

    [6] F. Leblond, S. C. Davis, P. A. Valdes, B. W. Pogue, "Pre-clinical whole-body fluorescence imaging: Review of instruments, methods and applications," J. Photochem. Photobiol. B. Biol. 98(1), 77–94 (2010).

    [7] M. V. Marshall, J. C. Rasmussen, I. C. Tan, M. B. Aldrich, K. E. Adams, X. Wang, E. M. Sevick-Muraca, "Near-infrared fluorescence imaging in humans with indocyanine green: A review and update," Open Surg. Oncol. J. (Online), 2(2), 12 (2010).

    [8] S. Bouccara, G. Sitbon, A. Fragola, V. Loriette, N. Lequeux, T. Pons, "Enhancing fluorescence in vivo imaging using inorganic nanoprobes," Curr. Opin. Biotechnol. 34, 65–72 (2015).

    [9] K. Y. Zhang, Q. Yu, H. Wei, S. Liu, Q. Zhao, W. Huang, "Long-lived emissive probes for timeresolved photoluminescence bioimaging and biosensing," Chem. Rev. 118(4), 1770–1839 (2018).

    [10] B. Del Rosal, A. Benayas, "Strategies to overcome autofluorescence in nanoprobe-driven in vivo fluorescence imaging," Small Meth. 2(9), 1800075 (2018).

    [11] G. Marriott, R. M. Clegg, D. J. Arndt-Jovin, T. M. Jovin, "Time resolved imaging microscopy. Phosphorescence and delayed fluorescence imaging," Biophys. J. 60(6), 1374–1387 (1991).

    [12] G. Vereb, E. Jares-Erijman, P. R. Selvin, T. M. Jovin, "Temporally and spectrally resolved imaging microscopy of lanthanide chelates," Biophys. J. 74(5), 2210–2222 (1998).

    [13] R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, G. Valentini, "Time-resolved fluorescence imaging in biology and medicine," J. Phys. D. Appl. Phys. 35(9), R61 (2002).

    [14] R. E. Connally, J. A. Piper, "Time-gated luminescence microscopy," Ann. New York Acad. Sci. 1130(1), 106–116 (2008).

    [15] J. R. Lakowicz, Introduction to fluorescence, Principles of Fluorescence Spectroscopy, Springer, Boston, MA (1999).

    [16] J. R. Lakowicz, Time-domain lifetime measurements, Principles of Fluorescence Spectroscopy, Springer, Boston, MA (1999).

    [17] B. Valeur, "Molecular fluorescence," Digital Encyclopedia Appl. Phys. 477–531 (2003).

    [18] N. Boens, W. Qin, N. Basaric, J. Hofkens, M. Ameloot, J. Pouget, N. D. Silva, "Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy," Anal. Chem. 79(5), 2137–2149 (2007).

    [19] F. Menezes, A. Fedorov, C. Baleizao, B. Valeur, M. N. Berberan-Santos, "Methods for the analysis of complex fluorescence decays: Sum of Becquerel functions versus sum of exponentials," Meth. Appl. Fluores. 1(1), 015002 (2013).

    [20] Y. Lu, M. Abran, G. Cloutier, F. Lesage, Catheterbased time-gated near-infrared fluorescence/OCT imaging system, Diagnostic and Therapeutic Applications of Light in Cardiology, Int. Society for Optics and Photonics, Vol. 10471 (SPIE BiOS, San Francisco, California, United States, 2018) pp. 104710D-1–7.

    [21] S. V. Eliseeva, J. C. G. Bünzli, "Lanthanide luminescence for functional materials and bio-sciences," Chem. Soc. Rev. 39(1), 189–227 (2010).

    [22] P. Hanninen, H. Harma (Eds.)., Lanthanide Luminescence: Photophysical, Analytical and Biological Aspects, Springer Science & Business Media, Vol. 7 (2011).

    [23] G. Marriott, M. Heidecker, E. P. Diamandis, Y. Yan-Marriott, "Time-resolved delayed luminescence image microscopy using an europium ion chelate complex," Biophys. J. 67(3), 957–965 (1994).

    [24] R. E. Connally, J. A. Piper, "Solid-state time-gated luminescence microscope with ultraviolet lightemitting diode excitation and electron-multiplying charge-coupled device detection," J. Biomed. Opt. 13(3), 034022 (2008).

    [25] B. Del Rosal, D. H. Ortgies, N. Fernandez, F. Sanz-Rodriguez, D. Jaque, E. M. Rodriguez, "Overcoming autofluorescence: Long-lifetime infrared nanoparticles for time-gated in vivo imaging," Adv. Mater. 28(46), 10188 (2016).

    [26] X. F. Wang, T. Uchida, D. M. Coleman, S. Minami, "A two-dimensional fluorescence lifetime imaging system using a gated image intensifier," Appl. Spectrosc. 45(3), 360–366 (1991).

    [27] R. Cubeddu, G. Canti, P. Taroni, G. Valentini, "Time-gated fluorescence imaging for the diagnosis of tumors in a murine model," Photochem. Photobiol. 57(3), 480–485 (1993).

    [28] G. Valentini, C. D'Andrea, D. Comelli, A. Pifferi, P. Taroni, A. Torricelli, L. Rossi-Bernardi, "Time-resolved DNA-microarray reading by an intensified CCD for ultimate sensitivity," Opt. Lett. 25(22), 1648–1650 (2000).

    [29] M. Dahan, T. Laurence, F. Pinaud, D. S. Chemla, A. P. Alivisatos, M. Sauer, S. Weiss, "Time-gated biological imaging by use of colloidal quantum dots," Opt. Lett. 26(11), 825–827 (2001).

    [30] R. Connally, D. Jin, J. Piper, "High intensity solidstate UV source for time-gated luminescence microscopy," Cytometr. A. J. Int. Soc. Anal. Cytol. 69(9), 1020–1027 (2006).

    [31] A. May, S. Bhaumik, S. S. Gambhir, C. Zhan, S. Yazdanfar, "Whole-body, real-time preclinical imaging of quantum dot fluorescence with timegated detection," J. Biomed. Opt., 14(6), 060504 (2009).

    [32] D. Jin, J. A. Piper, "Time-gated luminescence microscopy allowing direct visual inspection of lanthanide-stained microorganisms in background-free condition," Anal. Chem. 83(6), 2294–2300 (2011).

    [33] W. Mo, D. J. Rohrbach, U. Sunar, "Imaging a photodynamic therapy photosensitizer in vivo with a time-gated fluorescence tomography system," J. Biomed. Opt. 17(7), 071306 (2012).

    [34] S. Bouccara, A. Fragola, E. Giovanelli, G. Sitbon, N. Lequeux, T. Pons, V. Loriette, "Time-gated cell imaging using long lifetime near-infrared-emitting quantum dots for autofluorescence rejection," J. Biomed. Opt. 19(5), 051208 (2014).

    [35] J. Joo, X. Liu, V. R. Kotamraju, E. Ruoslahti, Y. Nam, M. J. Sailor, "Gated luminescence imaging of silicon nanoparticles," ACS Nano, 9(6), 6233–6241 (2015).

    [36] W. A. Razali, V. K. Sreenivasan, C. Bradac, M. Connor, E.M. Goldys, A. V. Zvyagin, "Wide-field time-gated photoluminescence microscopy for fast ultrahigh-sensitivity imaging of photoluminescent probes," J. Biophoton. 9(8), 848–858 (2016).

    [37] X. Zheng, X. Zhu, Y. Lu, J. Zhao, W. Feng, G. Jia, D. Jin, "High-contrast visualization of upconversion luminescence in mice using time-gating approach," Anal. Chem. 88(7), 3449–3454 (2016).

    [38] X. Liu, G. B. Braun, H. Zhong, D. J. Hall, W. Han, M. Qin, M. J. Sailor, "Tumor-targeted multimodal optical imaging with versatile cadmium-free quantum dots," Adv. Funct. Mater. 26(2), 267–276 (2016).

    [39] C. C. Tu, K. Awasthi, K. P. Chen, C. H. Lin, M. Hamada, N. Ohta, Y. K. Li, "Time-gated imaging on live cancer cells using silicon quantum dot nanoparticles with long-lived fluorescence," ACS Photon. 4(6), 1306–1315 (2017).

    [40] T. Chen, R. Hong, D. Magda, C. Bieniarz, L. Morrison, L. W. Miller, "Time gated luminescence imaging of immunolabeled human tissues," Anal. Chem. 89(23), 12713–12719 (2017).

    [41] T. Li, D. Yang, L. Zhai, S. Wang, B. Zhao, N. Fu, W. Huang, "Thermally activated delayed fluorescence organic dots (TADF Odots) for time-resolved and confocal fluorescence imaging in living cells and in vivo," Adv. Sci. 4(4), 1600166 (2017).

    [42] V. K. Sreenivasan, Wan Razali, W. A., K. Zhang, R. R. Pillai, A. Saini, D. Denkova, E. M. Goldys, "Development of bright and biocompatible nanoruby and its application to background-free timegated imaging of G-protein-coupled receptors," ACS Appl. Mater. Interf. 9(45), 39197–39208 (2017).

    [43] P. Sawosz, S. Wojtkiewicz, M. Kacprzak, E. Zieminska, M. Morawiec, R. Maniewski, A. Liebert, "Towards in-vivo assessment of fluorescence lifetime: imaging using time-gated intensified CCD camera," Biocybernet. Biomed. Eng. 38(4), 966–974 (2018).

    [44] M. Sakiyama, H. Sugimoto, M. Fujii, "Long-lived luminescence of colloidal silicon quantum dots for time-gated fluorescence imaging in the second near infrared window in biological tissue," Nanoscale, 10(29), 13902–13907 (2018).

    [45] Z. Zhu, D. Tian, X. Shu, "Auto-phase-locked timegated luminescence detection for background-free upconversion spectra measurement and true-color biological imaging," Sens. Actuators B. Chem. 260, 289–294 (2018).

    [46] S. Shkolyar, E. J. Eshelman, J. D. Farmer, D. Hamilton, M. G. Daly, C. Youngbull, "Detecting kerogen as a biosignature using colocated UV timegated Raman and fluorescence spectroscopy," Astrobiol., 18(4), 431–453 (2018).

    [47] R. Chib, S. Requena, M. Mummert, Y. M. Strzhemechny, I. Gryczynski, J. Borejdo, R. Fudala, "Fluorescence lifetime imaging with time-gated detection of hyaluronidase using a long lifetime azadioxatriangulenium (ADOTA) fluorophore," Meth. Appl. Fluorescence, 4(4), 047001 (2016).

    [48] S. Cheng, B. Shen, W. Yuan, X. Zhou, Q. Liu, M. Kong, F. Li, "Time-gated ratiometric detection with the same working wavelength to minimize the interferences from photon attenuation for accurate in vivo detection," ACS Central Sci. 5(2), 299–307 (2019).

    [49] T. Pons, S. Bouccara, V. Loriette, N. Lequeux, S. Pezet, A. Fragola, "In vivo imaging of single tumor cells in fast-flowing bloodstream using near-infrared quantum dots and time-gated imaging," ACS Nano, 13(3), 3125–3131 (2019).

    [50] X. D. Chen, Y. Zheng, B. Du, D. F. Li, S. Li, Y. Dong, G.-C. Guo, F. W. Sun, "High-contrast quantum imaging with time-gated fluorescence detection," Phys. Rev. Appl. 11(6), 064024 (2019).

    [51] Y. Gu, Z. Guo, W. Yuan, M. Kong, Y. Liu, Y. Gao, W. Feng, F. Wang, J. Zhou, D. Jin, F. Li, "Highsensitivity imaging of time-domain near-infrared light transducer," Nat. Photon. (2019).

    [52] Z. Zhu, X. Shu, "Global luminescence lifetime imaging of thermally activated delayed fluorescence on an auto-phase-locked time-gated microscope," Sens. Actuators B. Chem. 280, 177–182 (2019).

    [53] H. Kume, S. Suzuki, J. Takeuchi, K. Oba, "Newly developed photomultiplier tubes with position sensitivity capability," IEEE Trans. Nucl. Sci., 32(1), 448–452 (1985).

    [54] K. H. Kim, C. Buehler, K. Bahlmann, T. Ragan, W. C. A. Lee, E. Nedivi, E. L. Heffer, S. Fantini, P. T. C. So, "Multifocal multiphoton microscopy based on multianode photomultiplier tubes," Opt. Exp. 15(18), 11658–11678 (2007).

    [55] M. Caccia, L. Nardo, R. Santoro, D. Schaffhauser, "Silicon photomultipliers and SPAD imagers in biophotonics: advances and perspectives," Nucl. Instrum. Meth. Phys. Res. A. Accel. Spectrom. Detect. Assoc. Equip. 926, 101–117 (2018).

    [56] L. Pancheri, D. Stoppa, "A SPAD-based pixel linear array for high-speed time-gated fluorescence lifetime imaging," 2009 Proc. ESSCIRC (IEEE, Athens, Greece, 2009), pp. 428–431.

    [57] L. Pancheri, N. Massari, D. Stoppa, "SPAD image sensor with analog counting pixel for time-resolved fluorescence detection," IEEE Trans. Electron Dev. 60(10), 3442–3449 (2013).

    [58] A. C. Ulku, C. Bruschini, S. Weiss, X. Michalet, E. Charbon, "A time-gated large-array SPAD camera for picosecond resolution real-time FLIM," Multiphoton Microscopy in the Biomedical Sciences XVIII, Vol. 10498, International Society for Optics and Photonics (SPIE BiOS, San Francisco, California, United States, 2018), p. 104980M.

    [59] I. Gyongy, A. Green, S. W. Hutchings, A. Davies, N. A. Dutton, R. R. Duncan, C. Rickman, R. K. Henderson, P. A. Dalgarno, Fluorescence lifetime imaging of high-speed particles with single-photon image sensors, High-Speed Biomedical Imaging and Spectroscopy IV, Vol. 10889, p. 108890O, International Society for Optics and Photonics (2019).

    [60] M. Perenzoni, N. Massari, D. Perenzoni, L. Gasparini, D. Stoppa, "A 160X120 pixel analogcounting single-photon imager with time-gating and self-referenced column-parallel A/D conversion for fluorescence lifetime imaging," IEEE J. Solid-State Circuit. 51(1), 155–167 (2015).

    [61] W. Becker, B. Su, O. Holub, K. Weisshart, "FLIM and FCS detection in laser-scanning microscopes: Increased e±ciency by GaAsP hybrid detectors," Microscopy Res. Techniq. 74(9), 804–811 (2011).

    [62] D. Kim,W. Hwang, Y. Won, S. Moon, S. Y. Lee, M. Kang, W. S. Han, D. Y. Kim, "Enhancement of performance in time-domain FLIM with GaAsP hybrid detectors," Multiphoton Microscopy in the Biomedical Sciences XIX, International Society for Optics and Photonics, Vol. 10882 (SPIE BiOS, San Francisco, California, United States, 2019), pp. 108821J-1–4.

    [63] T. Lapauw, H. Ingelberts, T. Van den Dries, M. Kuijk, Sub-nanosecond time-gated camera based on a novel current-assisted CMOS image sensor, Photonic Instrumentation Engineering VI, International Society for Optics and Photonics, Vol. 10925 (SPIE OPTO, San Francisco, California, United States, 2019), pp. 1092506-1–9.

    [64] D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S.Webb,A. Sandison, A. Wallace,D. Davis, J. Lever, M. Neil, D. Phillips, G. Stampa, P. Frencha, "Timedomain fluorescence lifetime imaging applied to biological tissue," Photochem. Photobiol. Sci. 3(8), 795–801 (2004).

    [65] K. Suhling, P. M. French, D. Phillips, "Time-resolved fluorescence microscopy," Photochem. Photobiol. Sci. 4(1), 13–22 (2005).

    [66] Y. AndrewaWang, "Cadmium-free quantum dots as time-gated bioimaging probes in highly-auto-fluorescent human breast cancer cells," Chem. Commun. 49(6), 624–626 (2013).

    [67] S. Linden, M. K. Singh, K. D. Wegner, M. Regairaz, F. Dautry, F. Treussart, N. Hildebrandt, "Terbiumbased time-gated F€orster resonance energy transfer imaging for evaluating protein-protein interactions on cell membranes," Dalton Trans. 44(11), 4994–5003 (2015).

    [68] M. C. Dos Santos, N. Hildebrandt, "Recent developments in lanthanide-to-quantum dot FRET using time-gated fluorescence detection and photon upconversion," Trends Anal. Chem. 84, 60–71 (2016).

    [69] C. Chen, L. Ao, Y. T. Wu, V. Cifliku, M. Cardoso Dos Santos, E. Bourrier, M. Delbianco, D. Parker, J. M. Zwier, L. Huang, N. Hildebrandt, "Singlenanoparticle cell barcoding by tunable FRET from lanthanides to quantum dots," Angewandte Chemie Int. Edn. 57(41), 13686–13690 (2018).

    [70] H. B. Beverloo, A. Van Schadewijk, S. van Gelderen- Boele, H. J. Tanke, "Inorganic phosphors as new luminescent labels for immunocytochemistry and time-resolved microscopy," Cytometry. J. Int. Soc. Anal. Cytol. 11(7), 784–792 (1990).

    [71] L. Zhang, X. Zheng, W. Deng, Y. Lu, S. Lechevallier, Z. Ye, E. M. Goldys, J. M. Dawes, J. A. Piper, J. Yuan, M. Verelst, D. Jin, "Practical implementation, characterization and applications of a multicolour time-gated luminescence microscope," Sci. Rep. 4, 6597 (2014).

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

    [73] R. Connally, "A device for gated autosynchronous luminescence detection," Anal. Chem. 83(12), 4782–4787 (2011).

    [74] X. Liu, Z. Tang, B. Song, H. Ma, J. Yuan, "A mitochondria-targeting time-gated luminescence probe for hypochlorous acid based on a europium complex," J. Mater. Chem. B. 5(15), 2849–2855 (2017).

    [75] Z. Dai, L. Tian, B. Song, X. Liu, J. Yuan, "Development of a novel lysosome-targetable timegated luminescence probe for ratiometric and luminescence lifetime detection of nitric oxide in vivo," Chem. Sci. 8(3), 1969–1976 (2017).

    [76] Y. Wang, H. Wang, X. Zhao, Y. Jin, H. Xiong, J. Yuan, J. Wu, "A β-diketonate–europium (III) complex-based fluorescent probe for highly sensitive time-gated luminescence detection of copper and sulfide ions in living cells," New J. Chem. 41(13), 5981–5987 (2017).

    [77] Z. Dai, H. Ma, L. Tian, B. Song, M. Tan, X. Zheng, J. Yuan, "Construction of a multifunctional nanoprobe for tumor-targeted time-gated luminescence and magnetic resonance imaging in vitro and in vivo," Nanoscale 10(24), 11597–11603 (2018).

    [78] N. Sayyadi, I. Justiniano, R. E. Connally, R. Zhang, B. Shi, L. Kautto, A. V. Everest-Dass, J. Yuan, B. J. Walsh, D. Jin, R. D. Willows, J. A. Piper, N. H. Packer, "Sensitive time-gated immunoluminescence detection of prostate cancer cells using a TEGylated europium ligand," Anal. Chem. 88(19), 9564–9571 (2016).

    [79] N. Gahlaut, L. W. Miller, "Time-resolved microscopy for imaging lanthanide luminescence in living cells," Cytometry A 77(12), 1113–1125 (2010).

    [80] M. Rosenberg, K. R. Rostgaard, Z. Liao, A. O. Madsen, K. L. Martinez, T. Vosch, B. W. Laursen, "Design, synthesis, and time-gated cell imaging of carbon-bridged triangulenium dyes with long fluorescence lifetime and red emission," Chem. Sci. 9(12), 3122–3130 (2018).

    [81] B. Song, W. Shi, W. Shi, X. Qin, H. Ma, M. Tan, W. Zhang, L. Guo, J. Yuan, "A dual-modal nanoprobe based on Eu (iii) complex-MnO 2 nanosheet nanocomposites for time-gated luminescence–magnetic resonance imaging of glutathione in vitro and in vivo," Nanoscale 11(14), 6784–6793 (2019).

    [82] H. Ma, B. Song, Y. Wang, D. Cong, Y. Jiang, J. Yuan, "Dual-emissive nanoarchitecture of lanthanide-complex-modified silica particles for in vivo ratiometric time-gated luminescence imaging of hypochlorous acid," Chem. Sci. 8(1), 150–159 (2017).

    [83] H. Ma, B. Song, Y. Wang, C. Liu, X. Wang, J. Yuan, "Development of organelle-targetable europium complex probes for time-gated luminescence imaging of hypochlorous acid in live cells and animals," Dyes Pigments 140, 407–416 (2017).

    [84] Q. Gao, W. Zhang, B. Song, R. Zhang, W. Guo, J. Yuan, "Development of a novel lysosome-targeted ruthenium (II) complex for phosphorescence/timegated luminescence assay of biothiols," Anal. Chem. 89(8), 4517–4524 (2017).

    [85] D. Jin, R. Connally, J. Piper, "Practical time-gated luminescence flow cytometry. II: Experimental evaluation using UV LED excitation," Cytometry A. J. Int. Soc. Anal. Cytol. 71(10), 797–808 (2007).

    [86] L. Gu, D. J. Hall, Z. Qin, E. Anglin, J. Joo, D. J. Mooney, S. B. Howell, M. J. Sailor, "In vivo timegated fluorescence imaging with biodegradable luminescent porous silicon nanoparticles," Nat. Commun. 4, 2326 (2013).

    Wenzhao Yang, Sung-Liang Chen. Time-gated fluorescence imaging: Advances in technology and biological applications[J]. Journal of Innovative Optical Health Sciences, 2020, 13(3): 2030006
    Download Citation