Out-of-Phase Imaging after Optical Modulation (OPIOM) for Multiplexed Fluorescence Imaging Under Adverse Optical Conditions.

Raja Chouket, Ruikang Zhang, Agnès Pellissier-Tanon, Annie Lemarchand, Agathe Espagne, Thomas Le Saux, Ludovic Jullien
Author Information
  1. Raja Chouket: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France.
  2. Ruikang Zhang: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France.
  3. Agnès Pellissier-Tanon: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France.
  4. Annie Lemarchand: Laboratoire de Physique Théorique de la Matière Condensée (LPTMC), Sorbonne Université, Centre National de la Recherche Scientifique (CNRS), Paris, Cedex 05, France.
  5. Agathe Espagne: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France.
  6. Thomas Le Saux: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France. Thomas.Lesaux@ens.fr.
  7. Ludovic Jullien: PASTEUR, Département de Chimie, École normale supérieure, PSL University, Sorbonne Université, CNRS, Paris, France. Ludovic.Jullien@ens.fr.

Abstract

Fluorescence imaging has become a powerful tool for observations in biology. Yet it has also encountered limitations to overcome optical interferences of ambient light, autofluorescence, and spectrally interfering fluorophores. In this account, we first examine the current approaches which address these limitations. Then we more specifically report on Out-of-Phase Imaging after Optical Modulation (OPIOM), which has proved attractive for highly selective multiplexed fluorescence imaging even under adverse optical conditions. After exposing the OPIOM principle, we detail the protocols for successful OPIOM implementation.

Keywords

References

Giepmans BNG, Adams SR, Ellisman MH, Tsien RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312:217–224 [PMID: 16614209]
Waters JC (2009) Accuracy and precision in quantitative fluorescence microscopy. J Cell Biol 185:1135–48 [PMID: 19564400]
Swedlow JR, Hu K, Andrews PD, Roos DS, Murray JM (2002) Measuring tubulin content in toxoplasma gondii: a comparison of laser-scanning confocal and wide-field fluorescence microscopy. Proc Nat Acad Sci 99:2014–2019 [PMID: 11830634]
Murray JM, Appleton PL, Swedlow JR, Waters JC (2007) Evaluating performance in three-dimensional fluorescence microscopy. J Microsc 228:390–405 [PMID: 18045334]
Manley S, Gillette J, H Patterson G, Shroff H, F Hess H, Betzig E, Lippincott-Schwartz J (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5:155–157
George T, Jung Sun Y, Kwang-Sup S, Ralf S, Vasilis N (2009) Real-time intraoperative fluorescence imaging system using light-absorption correction. J Biomed Opt 14 6:064012
Troyan S, Kianzad V, L Gibbs-Strauss S, Gioux S, Matsui A, Oketokoun R, Ngo L, Kamen A, Azar F, V Frangioni J (2009) The flare intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann Surg Oncol 16:2943–2952
Chaerle L, Hagenbeek D, Bruyne ED, Valcke R, Straeten DVD (2004) Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage. Plant Cell Physiol 45 7:887–896 [PMID: 15295072]
Chaerle L, Leinonen I, Jones HG, Van Der Straeten D (2007) Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. J Exp Bot 58:773–784 [PMID: 17189594]
Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132 2:485–493 [PMID: 12805581]
Flexas J, Briantais JM, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sens Environ 73:283–297 [DOI: 10.1016/S0034-4257(00)00104-8]
Plascyk JA (1975) The mk ii fraunhofer line discriminator (fld-ii) for airborne and orbital remote sensing of solar-stimulated luminescence. Optical Eng 14:339–346 [DOI: 10.1117/12.7971842]
GomezChova L, AlonsoChorda L, Amoros Lopez J, Vila Frances J, del ValleTascon S, Calpe J, Moreno J (2006) Solar induced fluorescence measurements using a field spectroradiometer. AIP Conf Proc 852:274–281 [DOI: 10.1063/1.2349354]
Moya I, Ounis A, Moise N, Goulas Y (2006) First airborne multiwavelength passive chlorophyll fluorescence measurements over la Mancha (Spain) fields. In: Second recent advances in quantitative remote sensing pp 820–825
Alonso L, Gomez-Chova L, Vila-Frances J, Amoros-Lopez J, Guanter L, Calpe J, Moreno J (2007) Sensitivity analysis of the Fraunhofer line discrimination method for the measurement of chlorophyll fluorescence using a field spectroradiometer. In: 2007 ieee international geoscience and remote sensing symposium, pp 3756–3759
Mazzoni M, Agati G, Cecchi G, Toci G, Mazzinghi P (2017) High resolution measurements of solar induced chlorophyll fluorescence in the Fraunhofer oxygen bands. ProcSPIE 10567:10567
Yamaguchi T, Sunaga Y, Haruta M, Motoyama M, Ohta Y, Takehara H, Noda T, Sasagawa K, Tokuda T, Ohta J (2015) Fluorescence imaging under background light with a self-reset complementary metal-oxide semiconductor image sensor. J Eng 2015:328–330 [DOI: 10.1049/joe.2015.0046]
H Norikane J, Kurata K (2001) Water stress detection by monitoring fluorescence of plants under ambient light. Transactions of the ASAE 44:1915–1922
Mazel CH (2005) Underwater fluorescence photography in the presence of ambient light. Limnol Oceanogr Methods 3:499–510 [DOI: 10.4319/lom.2005.3.499]
Dominik E, Daniel G, Matthias R, Thomas B (2012) A compact multi-channel fluorescence sensor with ambient light suppression. Meas Sci Technol 23:035702 [DOI: 10.1088/0957-0233/23/3/035702]
Sexton K, Davis SC, McClatchy D, Valdes PA, Kanick SC, Paulsen KD, Roberts DW, Pogue BW (2013) Pulsed-light imaging for fluorescence guided surgery under normal room lighting. Opt Lett 38:3249–3252 [PMID: 23988926]
Nedbal L, Soukupová J, Kaftan D, Whitmarsh J, Trtílek M (2000) Kinetic imaging of chlorophyll fluorescence using modulated light. Photosynth Res 66:3–12 [PMID: 16228406]
J Sexton K, Zhao Y, C Davis S, Jiang S, W Pogue B (2017) Optimization of fluorescent imaging in the operating room through pulsed acquisition and gating to ambient background cycling. Biomed Opt Express 8:2635
Weinstein S, Pane D, Ernst LA, Warren-Rhodes K, Dohm JM, Hock AN, Piatek JL, Emani S, Lanni F, Wagner M, Fisher GW, Minkley E, Dansey LE, Smith T, Grin EA, Stubbs K, Thomas G, Cockell CS, Marinangeli L, Ori GG, Heys S, Teza JP, Moersch JE, Coppin P, Diaz GC, Wettergreen DS, Cabrol NA, Waggoner AS (2008) Application of pulsed-excitation fluorescence imager for daylight detection of sparse life in tests in the atacama desert. J Geophys Res Biogeosciences 113:G1 [DOI: 10.1029/2006JG000319]
Lanni F, Pane D, J Weinstein S, Waggoner A (2007) Compact flashlamp-based fluorescence imager for use under ambient-light conditions. Rev Sci Instrum 78:033702
Banghe Z, John CR, Eva MSM (2014) Non-invasive fluorescence imaging under ambient light conditions using a modulated ICCD and laser diode. Biomed Opt Express 5:562–572 [DOI: 10.1364/BOE.5.000562]
Shimshon B, Sharon Yk, Yossef K, Victor K, Tali S, Yonatan A, Cheinat ZP, Zahi R, Amos N, Aharon JA (2017) Remote detection of buried landmines using a bacterial sensor. Nat Biotechnol 35:308–310 [DOI: 10.1038/nbt.3791]
Policard A (1924) Etude sur les aspects offerts par des tumeurs expérimentales examinées à la lumière de Wood. Comptes Rendus Hebdomadaires des Séances Mémories la Société Biol Filiales 91:1423
Aubin JE (1979) Autofluorescence of viable cultured mammalian cells. J Histochem Cytochem 27:36–43 [PMID: 220325]
Richards-Kortum RR, Sevick-Muraca EM (1996) Quantitative optical spectroscopy for tissue diagnosis. Ann Rev Phys Chem 47:555–606 [DOI: 10.1146/annurev.physchem.47.1.555]
Koenig K, Schneckenburger H (1994) Laser-induced autofluorescence for medical diagnosis. J Fluoresc 4:17–40 [PMID: 24233290]
Zipfel WR, Williams RM, Christie R, Nikitin AY, Hyman BT, Webb WW (2003) Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Nat Acad Sci 100:7075–7080 [PMID: 12756303]
Monici M (2005) Cell and tissue autofluorescence research and diagnostic applications. Biotechnol Ann Rev 11:227–256 [DOI: 10.1016/S1387-2656(05)11007-2]
Inaguma M, Hashimoto K (2000) Porphyrin-like fluorescence in oral cancer. Cancer 86:2201–2211 [DOI: 10.1002/(SICI)1097-0142(19991201)86]
Talamond P, Verdeil JL, Conéjéro G (2015) Secondary metabolite localization by autofluorescence in living plant cells. Molecules 20(3):5024–5037 [PMID: 25808147]
Cerovic ZG, Samson G, Morales F, Tremblay N, Moya I (1999) Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomie 19:543–578 [DOI: 10.1051/agro]
Berg RH (2004) Evaluation of spectral imaging for plant cell analysis. J Microsc 214:174–181 [PMID: 15102064]
Willemse MTM (1989) Physico-Chemical Characterisation of Plant Residues for Industrial and Feed Use. Springer, Dordrecht
Goodwin RH (1953) Fluorescent substances in plants. Ann Rev Plant Physiol 4:283–304 [DOI: 10.1146/annurev.pp.04.060153.001435]
Harris P, Hartley R (1976) Detection of bound ferulic acid in cell walls of the gramineae by ultraviolet fluorescence microscopy. Nature 259:508–510 [DOI: 10.1038/259508a0]
Lichtenthaler HK, Schweiger J (1998) Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of plants. J Plant Physiol 152:272–282 [DOI: 10.1016/S0176-1617(98)80142-9]
Shimasaki H, Ueta N, Privett OS (1980) Isolation and analysis of age-related fluorescent substances in rat testes. Lipids 15:236–241 [PMID: 7374376]
Tsuchida M, Miura T, Aibara K (1987) Lipofuscin and lipofuscin-like substances. Chem Phys Lipids 44:297–325 [PMID: 3311421]
Matsumoto Y (2001) Lipofuscin pigmentation in pleomorphic adenoma of the palate. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92:299–302 [PMID: 11552147]
Buschmann C, Langsdorf G, Lichtenthaler H (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38:483–491 [DOI: 10.1023/A]
Blomfield J, Farrar JF (1969) The fluorescent properties of maturing arterial elastin. Cardiovasc Res 3:161–170 [PMID: 5346452]
Croce AC, Bottiroli G (2014) Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis. Eur J Histochem
Duysens L, Amesz J (1957) Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region. Biochim Biophys Acta 24:19–26 [PMID: 13426197]
Duysens L, Kronenberg G (1957) The fluorescence spectrum of the complex of reduced phosphopyridine nucleotide and alcohol dehydrogenase from yeast. Biochim Biophys Acta 26:437–438 [PMID: 13499390]
Wolfbeis O (1985) The fluorescence of organic natural products. In: Molecular luminescence spectroscopy part I: methods and applications, pp 167–370
Del Rosal B, Villa I, Jaque D, Sanz-Rodriguez F (2015) In vivo autofluorescence in the biological windows: the role of pigmentation. J Biophoton 9:1059–1067 [DOI: 10.1002/jbio.201500271]
Mihalcescu I, Gateau MVM, Chelli B, Pinel C, Ravanat JL (2015) Green autofluorescence, a double edged monitoring tool for bacterial growth and activity in micro-plates. Phys Biol 12:066016 [PMID: 26656747]
Walmsley R, Billinton N, Heyer WD (1997) Green fluorescent protein as a reporter for the DNA damage-induced gene RAD54 in Saccharomyces cerevisiae. Yeast 13:1535–1545 [PMID: 9509573]
Billinton N, Knight AW (2001) Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence. Anal Biochem 291:175–197 [PMID: 11401292]
Jaeger PA, McElfresh C, Wong LR, Ideker T (2015) Beyond agar: gel substrates with improved optical clarity and drug efficiency and reduced autofluorescence for microbial growth experiments. Appl Environ Microbiol 81(16):5639–5649 [PMID: 26070672]
Spencer VA, Kumar S, Paszkiet B, Fein J, Zmuda JF (2014) Cell culture media for fluorescence imaging. Genet Eng Biotechnol News 34:16–18 [DOI: 10.1089/gen.34.10.09]
Randers-Eichhorn L, Albano CR, Sipior J, Bentley WE, Rao G (1997) On-line green fluorescent protein sensor with LED excitation. Biotechnol Bioeng 55:921–926 [PMID: 18636601]
An JH, Blackwell TK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17 15:1882–1893
Staughton TJ, McGillicuddy CJ, Weinberg PD (2001) Techniques for reducing the interfering effects of autofluorescence in fluorescence microscopy: improved detection of sulphorhodamine b-labelled albumin in arterial tissue. J Microsc 201(Pt 1):70–76 [PMID: 11136441]
Teuscher AC, Ewald CY (2018) Overcoming autofluorescence to assess GFP expression during normal physiology and aging in Caenorhabditis elegans. Bio Protocol 8:e2940 [PMID: 30073182]
Patonay G, Antoine MD (1991) Near-infrared fluorogenic labels: new approach to an old problem. Anal Chem 63:321A–327A [DOI: 10.1021/ac00006a716]
Troy T, Jekic-McMullen D, Sambucetti LC, Rice B (2004) Quantitative comparison of the sensitivity of detection of fluorescent and bioluminescent reporters in animal models. Molecular imaging 3(1):9–23 [PMID: 15142408]
Müller MG, Georgakoudi I, Zhang Q, Wu J, Feld MS (2001) Intrinsic fluorescence spectroscopy in turbid media: disentangling effects of scattering and absorption. Appl Opt 40:4633–4646 [PMID: 18360504]
Diao S, Hong G, Antaris AL, Blackburn JL, Cheng K, Cheng Z, Dai H (2015) Biological imaging without autofluorescence in the second near-infrared region. Nano Res 8:3027–3034 [DOI: 10.1007/s12274-015-0808-9]
Weissleder R, Ntziachristos V (2002) Shedding light onto live molecular targets. Nat Med 6:79–93
John S, Lucjan S, Gabor P (2002) DNA and protein applications of near-infrared dyes. J Biomed Opt 7(4):571–575 [DOI: 10.1117/1.1502262]
Cordina NM, Sayyadi N, Parker LM, Everest-Dass A, Brown LJ, Packer NH (2018) Reduced background autofluorescence for cell imaging using nanodiamonds and lanthanide chelates. Sci Rep 8:4521 [PMID: 29540838]
Amy SG, Yonghong Z, Todd H, Dayle M, D Michael O (2004) Quantitative, two-color western blot detection with infrared fluorescence. LI-COR Biosciences
Deng G, Li S, Sun Z, Li W, Zhou L, Zhang J, Gong P, Cai L (2018) Near-infrared fluorescence imaging in the largely unexplored window of 900–1,000 nm. Theranostics 8:4116–4128 [PMID: 30128040]
Clancy B, Cauller L (1998) Reduction of background autofluorescence in brain sections following immersion in sodium borohydride. J Neurosci Methods 83:97–102 [PMID: 9765122]
Baschong W, Suetterlin R, Laeng RH (2001) Control of autofluorescence of archival formaldehyde-fixed, paraffin-embedded tissue in confocal laser scanning microscopy (CLSM). J Histochem Cytochem 49 12:1565–1572 [PMID: 11724904]
Davis AS, Richter A, Becker S, Moyer JE, Sandouk A, Skinner J, Taubenberger JK (2014) Characterizing and diminishing autofluorescence in formalin-fixed paraffin-embedded human respiratory tissue. J Histochem Cytochem 62(6):405–423 [PMID: 24722432]
Metcalf RL (1943) The storage and interaction of water soluble vitamins in the malpighian system of Periplaneta americana (L.). Arch Biochem 2:55–62
Schnell S, Staines W, Wessendorf M (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47:719–730 [PMID: 10330448]
Potter KA, Simon JS, Velagapudi B, Capadona JR (2012) Reduction of autofluorescence at the microelectrode-cortical tissue interface improves antibody detection. J Neurosci Methods 203(1):96–105 [PMID: 21978484]
Mosiman VL, Patterson BK, Canterero L, Goolsby CL (2002) Reducing cellular autofluorescence in flow cytometry: an in situ method. Cytometry 30:151–156 [DOI: 10.1002/(SICI)1097-0320(19970615)30]
Srivastava GK, Reinoso R, Singh AK, Fernandez-Bueno I, Hileeto D, Martino MD, García-Gutiérrez MT, Merino JMP, Alonso NF, Corell A, Pastor JC (2011) Trypan Blue staining method for quenching the autofluorescence of RPE cells for improving protein expression analysis. Exp Eye Res 93(6):956–962 [PMID: 21777584]
Pfüller U, Franz H, Preiß A (1977) Sudan black B: chemical structure and histochemistry of the blue main components. Histochemistry 54:237–250 [PMID: 75201]
Oliveira VC, Carrara RCV, Simoes DLC, Saggioro FP, Carlotti Jr CG, Covas DT, Neder L (2010) Sudan black b treatment reduces autofluorescence and improves resolution of in situ hybridization specific fluorescent signals of brain sections. Histol Histopathol 25:1017–1024 [PMID: 20552552]
Sun Y, Yu HJ, Zheng DX, Cao Q, Wang Y, Harris D, Wang Y (2011) Sudan black b reduces autofluorescence in murine renal tissue. Arch Pathol Lab Med 135(10):1335–1342 [PMID: 21970489]
Qi L, Knapton EK, Zhang X, Zhang T, Gu C, Zhao Y (2017) Pre-culture sudan black B treatment suppresses autofluorescence signals emitted from polymer tissue scaffolds. Sci Rep 7:8361 [PMID: 28827657]
Viegas MS, Martins TCM, Seco F, carmo AD (2007) An improved and cost-effective methodology for the reduction of autofluorescence in direct immunofluorescence studies on formalin-fixed paraffin-embedded tissues. Eur J Histochem 51(1):59–66
Yang X, Vidunas AJ, Beniash E (2017) Optimizing immunostaining of enamel matrix: application of Sudan Black B and minimization of false positives from normal sera and IgGs. Front Physiol 8:239 [PMID: 28487659]
Puneet G, Richa K (2017) A unique immunofluorescence protocol to detect protein expression in vascular tissues: tacking a long standing pathological hitch. Turk Patoloji Derg 34:57–65
Erben T, Ossig R, Naim HY, Schnekenburger J (2016) What to do with high autofluorescence background in pancreatic tissues—an efficient Sudan Black B quenching method for specific immunofluorescence labelling. Histopathology 69:406–422 [PMID: 26802460]
Zhang Y, Wang Y, Cao W, Ma K, Ji W, Han Z, Si J, Li L (2018) Spectral characteristics of autofluorescence in renal tissue and methods for reducing fluorescence background in confocal laser scanning microscopy. J Fluoresc 28:561–572 [PMID: 29560601]
Widengren J, Rigler R (1996) Mechanisms of photobleaching investigated by fluorescence correlation spectroscopy. Bioimaging 4:149–157 [DOI: 10.1002/1361-6374(199609)4]
Neumann MF, Gabel D (2002) Simple method for reduction of autofluorescence in fluorescence microscopy. J. Histochem. Cytochem. 50(3):437–439 [PMID: 11850446]
Duong H, Han M (2013) A multispectral LED array for the reduction of background autofluorescence in brain tissue. J Neurosci Methods 220:46–54 [PMID: 23994358]
Kumar BS, Sandhyamani S, Nazeer sS, Jayasree R (2015) Rapid and simple method of photobleaching to reduce background autofluorescence in lung tissue sections. Indian J Biochem Biophys 52:107–110
Sun Y, Ip P, Chakrabartty A (2017) Simple elimination of background fluorescence in formalin-fixed human brain tissue for immunofluorescence microscopy. J Vis Exp Jove 2017:e56188
Zhe L, Luke DL, Eric B (2015) Imaging live-cell dynamics and structure at the single-molecule level. Mol Cell 58(4):644–659 [DOI: 10.1016/j.molcel.2015.02.033]
Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T (2008) Quantum dots versus organic dyes as fluorescent labels. Nat Methods 5:763–776 [PMID: 18756197]
Lavis LD, Raines RT (2014) Bright building blocks for chemical biology. ACS Chem Biol 9(4):855–866 [PMID: 24579725]
Schnell U, Dijk F, Sjollema KA, Giepmans BNG (2012) Immunolabeling artifacts and the need for live-cell imaging. Nat Methods 9:152–158 [PMID: 22290187]
Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K (2002) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 21:86–89 [PMID: 12469133]
Gautier A, Juillerat A, Heinis C, Corrêa IR, Kindermann M, Beaufils F, Johnsson K (2008) An engineered protein tag for multiprotein labeling in living cells. Chem Biol 15:128–136 [PMID: 18291317]
Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N, Zimprich C, Wood MG, Learish R, Ohana RF, Urh M, Simpson D, Mendez J, Zimmerman K, Otto P, Vidugiris G, Zhu J, Darzins A, Klaubert DH, Bulleit RF, Wood KV (2008) Halotag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem Biol 3(6):373–382 [PMID: 18533659]
Gao X, Yang L, Petros JA, Marshall FF, Simons JW, Nie S (2005) In vivo molecular and cellular imaging with quantum dots. Curr Opin Biotechnol 16(1):63–72 [PMID: 15722017]
Chan WC, Maxwell DJ, Gao X, Bailey RE, Han M, Nie S (2002) Luminescent quantum dots for multiplexed biological detection and imaging. Curr Opin Biotechnol 13:40–46 [PMID: 11849956]
Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T (2008) Quantum dots versus organic dyes as fluorescent labels. Nat Methods 5:763–772 [PMID: 18756197]
Zhang Y, He J, Wang PN, Chen JY, Lu ZJ, Lu DR, Guo J, Wang CC, Yang WL (2006) Time-dependent photoluminescence blue shift of the quantum dots in living cells: effect of oxidation by singlet oxygen. J Am Chem Soc 128(41):13396–13401 [PMID: 17031951]
Ma J, Chen JY, Guo J, Wang C, Yang W, Xu L, N Wang P (2006) Photostability of thiol-capped CdTe quantum dots in living cells: the effect of photo-oxidation. Nanotechnology 17:2083–2089
Zuo P, Lu X, Sun ZG, Guo Y, He H (2015) A review on syntheses, properties, characterization and bioanalytical applications of fluorescent carbon dots. Microchim Acta 183:519–542 [DOI: 10.1007/s00604-015-1705-3]
Medintz IL, Uyeda HT, Goldman ER, Mattoussi H (2005) Quantum dot bioconjugates for imaging, labelling and sensing. Nat Materials 4:435–446 [PMID: 15928695]
Xing Y, Chaudry Q, Shen C, Kong KY, Zhau HE, Chung LW, Petros JA, O’Regan RM, Yezhelyev MV, Simons JW, Wang MD, Nie S (2007) Bioconjugated quantum dots for multiplexed and quantitative immunohistochemistry. Nat Protocols 2:1152–1166 [PMID: 17546006]
Howarth M, Takao K, Hayashi Y, Ting AY (2005) Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc Nat Acad Sci 102(21):7583–7588. https://doi.org/10.1073/pnas.0503125102 [PMID: 15897449]
Chen I, Howarth M, Lin W, Ting AY (2005) Site-specific labeling of cell surface proteins with biophysical probes using biotin ligase. Nat Methods 2:99– 104 [PMID: 15782206]
Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of Aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59(3):223–239 [PMID: 13911999]
Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ (1992) Primary structure of the aequorea victoria green-fluorescent protein. Gene 111(2):229–233 [PMID: 1347277]
Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805. https://doi.org/10.1126/science.8303295 [PMID: 8303295]
Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90:1103–1163 [PMID: 20664080]
Rodriguez EA, Campbell RE, Lin JY, Lin MZ, Miyawaki A, Palmer AE, Shu X, Zhang J, Tsien RY (2017) The growing and glowing toolbox of fluorescent and photoactive proteins. Trends Biochem Sci 42(2):111–129 [PMID: 27814948]
Tomosugi W, Matsuda T, Tani T, Nemoto T, Kotera I, Saito K, Horikawa K, Nagai T (2009) An ultramarine fluorescent protein with increased photostability and ph insensitivity. Nat Methods 6(2):351–354 [PMID: 19349978]
Subach OM, Gundorov IS, Yoshimura M, Subach FV, Zhang J, Gruenwald D, Souslova EA, Chudakov DM, Verkhusha VV (2008) Conversion of red fluorescent protein into a bright blue probe. Chem Biol 15:1116–1124 [PMID: 18940671]
Ai Hw, Henderson JN, Remington S, Campbell RE (2006) Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem J 400(3):531–540 [DOI: 10.1042/BJ20060874]
Sarkisyan KS, Goryashchenko AS, Lidsky PV, Gorbachev DA, Bozhanova NG, Gorokhovatsky AY, Pereverzeva AR, Ryumina AP, Zherdeva VV, Savitsky AP, Solntsev KM, Bommarius AS, Sharonov GV, Lindquist JR, Drobizhev M, Hughes TE, Rebane A, Lukyanov KA, Mishin AS (2015) Green fluorescent protein with anionic tryptophan-based chromophore and long fluorescence lifetime. Biophys J 109:380–389 [PMID: 26200874]
Hoi H, Howe ES, Ding Y, Zhang W, Baird MA, Sell BR, Allen JR, Davidson MW, Campbell RE (2013) An engineered monomeric Zoanthus sp. yellow fluorescent protein. Chem Biol 20:1296–1304 [PMID: 24094838]
Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567–1572 [PMID: 15558047]
Bindels DS, Haarbosch L, van Weeren L, Postma M, Wiese KE, Mastop M, Aumonier S, Gotthard G, Royant A, Hink MA, Gadella Jr TWJ (2016) mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat Methods 14:53–56 [PMID: 27869816]
Matela G, Gao P, Guigas G, Eckert AF, Nienhaus K, Ulrich Nienhaus G (2017) A far-red emitting fluorescent marker protein mGarnet2 for microscopy and STED nanoscopy. Chem Commun 53:979–982 [DOI: 10.1039/C6CC09081H]
Shcherbakova DM, Baloban M, Emelyanov AV, Brenowitz M, Guo P, Verkhusha VV (2016) Bright monomeric near-infrared fluorescent proteins as tags and biosensors for multiscale imaging. Nat Commun 7:12405 [PMID: 27539380]
Zimmermann T (2005) Spectral Imaging and Linear Unmixing in Light Microscopy. Springer, Berlin [DOI: 10.1007/b102216]
Zimmermann T, Rietdorf J, Pepperkok R (2003) Spectral imaging and its applications in live cell microscopy. FEBS Lett 546(1):87–92 [PMID: 12829241]
Clayton AHA, Hanley QS, Verveer PJ (2004) Graphical representation and multicomponent analysis of single-frequency fluorescence lifetime imaging microscopy data. J Microsc 213(1):1–5 [PMID: 14678506]
Redford G, Clegg R (2005) Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J Fluoresc 15:805–815 [PMID: 16341800]
Digman MA, Caiolfa VR, Zamai M, Gratton E (2008) The phasor approach to fluorescence lifetime imaging analysis. Biophys J 94:L14–L16 [PMID: 17981902]
Fereidouni F, Bader AN, Gerritsen HC (2012) Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images. Opt Express 20(12):12729–12741 [PMID: 22714302]
Malacrida L, Astrada S, Briva A, Bollati-Fogollin M, Gratton E, Bagatolli L (2016) Spectral phasor analysis of LAURDAN fluorescence in live A549 lung cells to study the hydration and time evolution of intracellular lamellar body-like structures:. Biochim Biophys Acta 1858:2625–2635. https://doi.org/10.1016/j.bbamem.2016.07.017
Valm A, Cohen S, Legant W, Melunis J, Hershberg U, Wait E, Cohen A, Davidson M, Betzig E, Lippincott-Schwartz J (2017) Applying systems-level spectral imaging and analysis to reveal the organelle interactome. Nature 546:162–167 [PMID: 28538724]
Neher R, Neher E (2004) Optimizing imaging parameters for the separation of multiple labels in a fluorescence image. J Microsc 213:46–62 [PMID: 14678512]
Mansfield JR, Gossage KW, Hoyt CC, Levenson RM (2005) Autofluorescence removal, multiplexing, and automated analysis methods for in-vivo fluorescence imaging. J Biomed Opt 104:041207 [DOI: 10.1117/1.2032458]
Gao L, Smith RT (2015) Optical hyperspectral imaging in microscopy and spectroscopy—a review of data acquisition. J Biophoton 8(6):441–456 [DOI: 10.1002/jbio.201400051]
Jahr W, Schmid B, Schmied C, Fahrbach FO, Huisken J (2015) Hyperspectral light sheet microscopy. Nat Commun 6:7990 [PMID: 26329685]
Valm AM, Welch JLM, Rieken CW, Hasegawa Y, Sogin ML, Oldenbourg R, Dewhirst FE, Borisy GG (2011) Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc Natl Acad Sci USA 108:4153–4157 [DOI: 10.1073/pnas.1101134108]
Cutrale F, Trivedi V, Trinh LA, Chiu CL, Choi JM, Artiga MS, Fraser SE (2017) Hyperspectral phasor analysis enables multiplexed 5d in vivo imaging. Nat Meth 14:149–152 [DOI: 10.1038/nmeth.4134]
Wagnieres GA, Star WM, Wilson BC (1998) In vivo fluorescence spectroscopy and imaging for oncological applications. Photochem Photobiol 68:603–632 [PMID: 9825692]
Quérard J, Saux TL, Gautier A, Alcor D, Croquette V, Lemarchand A, Gosse C, Jullien L (2016) Kinetics of reactive modules adds discriminative dimensions for selective cell imaging. ChemPhysChem 17:1396–1413 [PMID: 26833808]
Lakowicz JR, Szmacinski H, Nowaczyk K, Berndt KW, Jonson M (1992) Fluorescence lifetime imaging. Anal Biochem 202:316–330 [PMID: 1519759]
Bastiaens PI, Squire A (1999) Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol 9:48–52 [PMID: 10087617]
Berezin MY, Achilefu S (2010) Fluorescence lifetime measurements and biological imaging. Chem Rev 110(5):2641–2684 [PMID: 2924670]
Seefeldt B, Kasper R, Seidel T, Tinnefeld P, Dietz KJ, Heilemann M, Sauer M (2008) Fluorescent proteins for single-molecule fluorescence applications. J Biophoton 1(1):74–82 [DOI: 10.1002/jbio.200710024]
Jin D, Piper JA (2011) Time-gated luminescence microscopy allowing direct visual inspection of lanthanide-stained microorganisms in background-free condition. Anal Chem 83:2294–2300 [PMID: 21344865]
Rich RM, Stankowska DL, Maliwal BP, Sørensen TJ, Laursen BW, Krishnamoorthy RR, Gryczynski Z, Borejdo J, Gryczynski I, Fudala R (2013) Elimination of autofluorescence background from fluorescence tissue images by use of time-gated detection and the AzaDiOxaTriAngulenium (ADOTA) fluorophore. Anal Bioanal Chem 405:2065–2075 [PMID: 23254457]
Rich RM, Mummert M, Gryczynski Z, Borejdo J, Sørensen TJ, Laursen BW, Foldes-Papp Z, Gryczynski I, Fudala R (2013) Elimination of autofluorescence in fluorescence correlation spectroscopy using the AzaDiOxaTriAngulenium (ADOTA) fluorophore in combination with time-correlated single-photon counting (TCSPC). Anal Bioanal Chem 405:4887–4894 [PMID: 23564284]
Fleischer BC, Petty JT, Hsiang JC, Dickson RM (2017) Optically activated delayed fluorescence. J Phys Chem Lett 8(15):3536–3543 [PMID: 28696723]
Hofmann M, Eggeling C, Jakobs S, Hell SW (2005) Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci USA 102:17565–17569 [PMID: 16314572]
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 313:1642–1645 [PMID: 16902090]
Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793–796 [PMID: 16896339]
Dertinger T, Colyer R, Iyer G, Weiss S, Enderlein J (2009) Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI). Proc Natl Acad Sci USA 106:22287–22292 [PMID: 20018714]
Dempsey GT, Bates M, Kowtoniuk WE, Liu DR, Tsien RY, Zhuang X (2009) Photoswitching mechanism of cyanine dyes. J Am Chem Soc 131:18192–18193 [PMID: 19961226]
Fukaminato T (2011) Single-molecule fluorescence photoswitching: design and synthesis of photoswitchable fluorescent molecules. J Photochem Photobiol C Photochem Rev 12:177–208 [DOI: 10.1016/j.jphotochemrev.2011.08.006]
Bourgeois D, Adam V (2012) Reversible photoswitching in fluorescent proteins: a mechanistic view. IUBMB Life 64:482–491 [PMID: 22535712]
Zhou XX, Lin MZ (2013) Photoswitchable fluorescent proteins: ten years of colorful chemistry and exciting applications. Curr Opin Chem Biol 17:682–690 [PMID: 23876529]
Ando R, Mizuno H, Miyawaki A (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306:1370–1373 [PMID: 15550670]
Andresen M, Stiel AC, Trowitzsch S, Weber G, Eggeling C, Wahl MC, Hell SW, Jakobs S (2007) Structural basis for reversible photoswitching in Dronpa. Proc Natl Acad Sci USA 104:13005–13009. https://doi.org/10.1073/pnas.0700629104 [PMID: 17646653]
Habuchi S, Ando R, Dedecker P, Verheijen W, Mizuno H, Miyawaki A, Hofkens J (2005) Reversible single-molecule photoswitching in the GFP-like fluorescent protein dronpa. Proc Nat Acad Sci 102:9511–9516 [PMID: 15972810]
Stiel AC, Trowitzsch S, Weber G, Andresen M, Eggeling C, Hell SW, Jakobs S, Wahl MC (2007) 1.8 å bright-state structure of the reversibly switchable fluorescent protein Dronpa guides the generation of fast switching variants. Biochem J 402(1):35–42 [PMID: 17117927]
Ando R, Flors C, Mizuno H, Hofkens J, Miyawaki A (2007) Highlighted generation of fluorescence signals using simultaneous two-color irradiation on Dronpa mutants. Biophys J 92:97–99 [DOI: 10.1529/biophysj.107.105882]
Andresen M, Stiel AC, Folling J, Wenzel D, Schonle A, Egner A, Eggeling C, Hell SW, Jakobs S (2008) Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy. Nat Biotechnol 26:1035–1040 [PMID: 18724362]
Oida T, Sako Y, Kusumi A (1993) Fluorescence lifetime imaging microscopy (flimscopy). methodology development and application to studies of endosome fusion in single cells. Biophys J 64(3):676–685 [PMID: 8471720]
Marriott G, Clegg RM, Arndt-Jovin DJ, Jovin TM (1991) Time resolved imaging microscopy. phosphorescence and delayed fluorescence imaging. Biophys J 60:1374–1387 [PMID: 1723311]
Bugiel I, Konig K, Wabnitz H (1989) Investigation of cells by fluorescence laser scanning microscopy with subnanosecond time resolution. Lasers Life Sci 3:47–53
Elson DS, Munro I, Requejo-Isidro J, McGinty J, Dunsby C, Galletly N, Stamp GW, Neil MAA, Lever MJ, Kellett PA, Dymoke-Bradshaw A, Hares J, French PMW (2004) Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier. N J Phys 6:180 [DOI: 10.1088/1367-2630/6/1/180]
Lakowicz JR, Szmacinski H, Nowaczyk K, Johnson ML (1992) Fluorescence lifetime imaging of free and protein-bound NADH. Proc Nat Acad Sci 89:1271–1275 [PMID: 1741380]
Kodama Y (2016) Time gating of chloroplast autofluorescence allows clearer fluorescence imaging in planta. PLOS ONE 11:1–8 [DOI: 10.1371/journal.pone.0152484]
Schlegel G, Bohnenberger J, Potapova I, Mews A (2002) Fluorescence decay time of single semiconductor nanocrystals. Phys Rev Lett 88:137401–137405 [PMID: 11955124]
Zhang K, Chang H, Fu A, Alivisatos A, Yang H (2006) Continuous distribution of emission states from single CdSe/ZnS quantum dots. Nano Lett 6:843–847 [PMID: 16608295]
Dahan M, Laurence T, Pinaud F, Chemla DS, Alivisatos AP, Sauer M, Weiss S (2001) Time-gated biological imaging by use of colloidal quantum dots. Opt Lett 26(11):825–827 [PMID: 18040463]
Grecco H, Lidke K, Heintzmann R, Lidke D, Spagnuolo C, Martinez O, Jares-Erijman E, Jovin T (2004) Ensemble and single particle photophysical properties (two-photon excitation, anisotropy, FRET, lifetime, spectral conversion) of commercial quantum dots in solution and in live cells. Microsc Res Tech 65:169–179 [PMID: 15630694]
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42:313–349 [DOI: 10.1146/annurev.pp.42.060191.001525]
Schneckenburger H, Wagner M, Weber P, Strauss WS, Sailer R (2004) Autofluorescence lifetime imaging of cultivated cells using a UV picosecond laser diode. J Fluoresc 14:649–654 [PMID: 15617271]
Schweitzer D, Gaillard ER, Dillon J, Mullins RF, Russell S, Hoffmann B, Peters S, Hammer M, Biskup C (2012) Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen. Invest Ophthalmol Vis Sci 53:3376 [PMID: 22511622]
Becker W (2012) Fluorescence lifetime imaging—techniques and applications. J Microsc 247:119–136 [PMID: 22621335]
Luo T, Zhou T, Zhao Y, Liu L, Qu J (2018) Multiplexed fluorescence lifetime imaging by concentration-dependent quenching. J Mater Chem B 6:1912–1919 [PMID: 32254357]
Niehörster T, Löschberger A, Gregor I, Krämer B, Rahn HJ, Patting M, Koberling F, Enderlein J, Sauer M (2016) Multi-target spectrally resolved fluorescence lifetime imaging microscopy. Nat Methods 13:257–262 [PMID: 26808668]
Sandén T, Persson G, Thyberg P, Blom H, Widengren J (2007) Monitoring kinetics of highly environment sensitive states of fluorescent molecules by modulated excitation and time-averaged fluorescence intensity recording. Anal Chem 79:3330–3341 [PMID: 17385841]
Sandén T, Persson G, Widengren J (2008) Transient state imaging for microenvironmental monitoring by laser scanning microscopy. Anal Chem 80:9589–9596 [PMID: 19007245]
Widengren J (2010) Fluorescence-based transient state monitoring for biomolecular spectroscopy and imaging. J R Soc Interface 7:1135–1144 [PMID: 20375039]
Marriott G, Mao S, Sakata T, Ran J, Jackson DK, Petchprayoon C, Gomez TJ, Warp E, Tulyathan O, Aaron HL, Isacoff EY, Yan Y (2008) Optical lock-in detection imaging microscopy for contrast-enhanced imaging in living cells. Proc Natl Acad Sci USA 105:17789–17794 [PMID: 19004775]
Richards CI, Hsiang JC, Dickson RM (2010) Synchronously amplified fluorescence image recovery (SAFIRe). J Phys Chem B 114:660–665 [PMID: 19902923]
Hsiang JC, Jablonski AE, Dickson RM (2014) Optically modulated fluorescence bioimaging: visualizing obscured fluorophores in high background. Acc Chem Res 47:1545–1554 [PMID: 24725021]
Quérard J, Markus TZ, Plamont MA, Gauron C, Wang P, Espagne A, Volovitch M, Vriz S, Croquette V, Gautier A, Le Saux T, Jullien L (2015) Photoswitching kinetics and phase-sensitive detection add discriminative dimensions for selective fluorescence imaging. Angew Chem Int Ed 127:2671–2675 [DOI: 10.1002/ange.201408985]
Quérard J, Gautier A, Le Saux T, Jullien L (2015) Expanding discriminative dimensions for analysis and imaging. Chem Sci 6:2968–2978 [PMID: 28706678]
Quérard J, Zhang R, Kelemen Z, Plamont MA, Xie X, Chouket R, Roemgens I, Korepina Y, Albright S, Ipendey E, Volovitch M, Sladitschek HL, Neveu P, Gissot L, Gautier A, Faure JD, Croquette V, Saux TL, Jullien L (2017) Resonant out-of-phase fluorescence microscopy and remote imaging overcome spectral limitations. Nat Comm 8:969 [DOI: 10.1038/s41467-017-00847-3]
Zhang R, Chouket R, Plamont MA, Kelemen Z, Espagne A, Tebo AG, Gautier A, Gissot L, Faure JD, Jullien L, Croquette V, Le Saux T (2018) Macroscale fluorescence imaging against autofluorescence under ambient light. Light Sci Appl 7(1):97 [PMID: 30510693]
Zhang R, Chouket R, Tebo AG, Plamont MA, Kelemen Z, Gissot L, Faure JD, Gautier A, Croquette V, Jullien L, Le Saux T (2019) A simple imaging protocol for autofluorescence elimination and optical sectioning in fluorescence endomicroscopy. Optica 6(8):972–980 [DOI: 10.1364/OPTICA.6.000972]
Yan Y, Petchprayoon C, Mao S, Marriott G (2012) Reversible optical control of cyanine fluorescence in fixed and living cells: optical lock-in detection immunofluorescence imaging microscopy. Philos Trans R Soc Lond B Biol Sci 368:1–9
Du G, Marriott G, Yan Y (2010) An improved optical lock-in detection method for contrast-enhanced imaging in living cells. In: 4th international conference on bioinformatics and biomedical engineering (iCBBE), pp 1–5
Wu L, Dai Y, Jiang X, Petchprayoon C, Lee JE, Jiang T, Yan Y, Marriott G (2013) High-contrast fluorescence imaging in fixed and living cells using optimized optical switches. PLoS ONE 8:e64738 [PMID: 23755140]
Abbandonato G, Storti B, Signore G, Beltram F, Bizzarri R (2016) Quantitative optical lock-in detection for quantitative imaging of switchable and non-switchable components. Microsc Res Tech 79(10):929–937 [PMID: 27447845]
Richards CI, Hsiang JC, Senapati D, Patel S, Yu J, Vosch T, Dickson RM (2009) Optically modulated fluorophores for selective fluorescence signal recovery. J Am Chem Soc 131:4619–4621 [PMID: 19284790]
Richards CI, Hsiang JC, Dickson RM (2010) Synchronously Amplified Fluorescence Image Recovery (SAFIRe). J Phys Chem B 114:660–665 [PMID: 19902923]
Fan C, Hsiang JC, Dickson RM (2012) Optical modulation and selective recovery of Cy5 fluorescence. ChemPhysChem 13:1023–1029 [PMID: 22086764]
Jablonski AE, Hsiang JC, Bagchi P, Hull NP, Richards CI, Fahrni CJ, Dickson RM (2012) Signal discrimination between fluorescent proteins in live cells by long-wavelength optical modulation. J Phys Chem Lett 3(23):3585–3591 [PMID: 23419973]
Jablonski AE, Vegh RB, Hsiang JC, Bommarius BR, Chen YC, Solntsev KM, Bommarius AS, Tolbert LM, Dickson RM (2013) Optically modulatable blue fluorescent proteins. J Am Chem Soc 135 44:16410–7 [PMID: 24099419]
Chen YC, Jablonski AE, Issaeva I, Bourassa D, Hsiang JC, Fahrni CJ, Dickson RM (2015) Optically modulated photoswitchable fluorescent proteins yield improved biological imaging sensitivity. J Am Chem Soc 137:12764–12767 [PMID: 26402244]
Richards CI, Hsiang JC, Khalil AM, Hull NP, Dickson RM (2010) FRET-enabled optical modulation for high sensitivity fluorescence imaging. J Am Chem Soc 132(18):6318–6323 [PMID: 20397664]
Fan C, Hsiang JC, Jablonski AE, Dickson RM (2011) All-optical fluorescence image recovery using modulated stimulated emission depletion. Chem Sci 2(6):1080–1085 [PMID: 22262992]
Hsiang JC, Fleischer BC, Dickson RM (2016) Dark state-modulated fluorescence correlation spectroscopy for quantitative signal recovery. J Phys Chem Lett 7:2496–2501 [PMID: 27299945]
Chen YC, Dickson RM (2017) Improved fluorescent protein contrast and discrimination by optically controlling dark state lifetimes. J Phys Chem Lett 8:733–736 [PMID: 28125231]
Orth A, Ghosh RN, Wilson ER, Doughney T, Brown H, Reineck P, Thompson JG, Gibson BC (2018) Super-multiplexed fluorescence microscopy via photostability contrast. Biomed Opt Express 9(7):2943–2954 [PMID: 29984077]
Gong CSA, Lee YC, Lai JL, Yu CH, Huang LR, Yang CY (2016) The high-efficiency LED driver for visible light communication applications. Sci Rep 6:30991 [PMID: 27498921]
Wu Y, Mao X, Min C, Yan D, Chen H (2018) GaN FET push–pull driver circuit enabling power light emitting diode to be a high-efficiency, high-speed wireless transmitter. IEEE Photon J 10(6):1–10
Rusty Lansford SEF Gregory H Bearman (2001) Resolution of multiple GFP color variants and dyes using two-photon microscopy and imaging spectroscopy. J Biomed Optics 6(3):311–318 [DOI: 10.1117/1.1383780]
Park S, Arumugam P, Purushothaman B, Kim SY, Min DH, Li Jeon N, Song J (2017) Quantum-dot nanoprobes and AOTF based cross talk eliminated six color imaging of biomolecules in cellular system. Anal Chim Acta 985:166–174 [PMID: 28864187]
Jahr W, Schmid B, Schmied C, Fahrbach FO, Huisken J (2015) Hyperspectral light sheet microscopy. Nat Commun 6:7990–7997 [PMID: 26329685]
Ford BK, Descour MR, Lynch RM (2001) Large-image-format computed tomography imaging spectrometer for fluorescence microscopy. Opt Express 9(9):444–453. https://doi.org/10.1364/OE.9.000444 [PMID: 19424362]
Elliott AD, Gao L, Ustione A, Bedard N, Kester R, Piston DW, Tkaczyk TS (2012) Real-time hyperspectral fluorescence imaging of pancreatic-cell dynamics with the image mapping spectromete. J Cell Sci 125(20):4833–4840 [PMID: 22854044]
Moeyaert B, Nguyen Bich N, De Zitter E, Rocha S, Clays K, Mizuno H, van Meervelt L, Hofkens J, Dedecker P (2014) Green-to-red photoconvertible Dronpa mutant for multimodal super-resolution fluorescence microscopy. ACS Nano 8(2):1664–1673 [PMID: 24410188]
Tiwari DK, Arai Y, Yamanaka M, Agetsuma M, Nakano M, Fujita K, Nagai T (2015) A fast- and positively photoswitchable fluorescent protein for ultralow-laser-power RESOLFT nanoscopy. Nat Methods 12:515–521 [PMID: 25894946]
Brakemann T, Weber G, Andresen M, Groenhof G, Stiel AC, Trowitzsch S, Eggeling C, Grubmüller H, Hell SW, Wahl MC, Jakobs S (2010) Molecular basis of the light-driven switching of the photochromic fluorescent protein Padron. J Biol Chem 285:14603–14609 [PMID: 20236929]
Grotjohann T, Testa I, Leutenegger M, Bock H, Urban NT, Lavoie-Cardinal F, Willig KI, Eggeling C, Jakobs S (2011) Diffraction-unlimited all-optical imaging and writing with a photochromic GFP. Nature 478:204–208 [PMID: 21909116]
Grotjohann T, Testa I, Reuss M, Brakemann T, Eggeling C, Hell SW, Jakobs S (2012) rsEGFP2 enables fast RESOLFT nanoscopy of living cells. eLife 1:478–492 [DOI: 10.7554/eLife.00248]
El Khatib M, Martins A, Bourgeois D, Colletier JP, Adam V (2016) Rational design of ultrastable and reversibly photoswitchable fluorescent proteins for super-resolution imaging of the bacterial periplasm. Sci Rep 6:18459–18469 [PMID: 26732634]
Shinoda H, Ma Y, Nakashima R, Sakurai K, Matsuda T, Nagai T (2018) Acid-tolerant monomeric GFP from Olindias formosa. Cell Chem Biol 25:330–338 [PMID: 29290624]
Chang H, Zhang M, Ji W, Chen J, Zhang Y, Liu B, Lu J, Zhang J, Xu P, Xu T (2012) A unique series of reversibly switchable fluorescent proteins with beneficial properties for various applications. Proc Nat Acad Sci 109:4455–4460 [PMID: 22375034]
Zhang X, Chen X, Zeng Z, Zhang M, Sun Y, Xi P, Peng J, Xu P (2015) Development of a reversibly switchable fluorescent protein for super-resolution optical fluctuation imaging (SOFI). ACS Nano 9(3):2659–2667 [PMID: 25695314]
Zhang X, Zhang M, Li D, He W, Peng J, Betzig E, Xu P (2016) Highly photostable, reversibly photoswitchable fluorescent protein with high contrast ratio for live-cell superresolution microscopy. Proc Nat Acad Sci 113(37):10364–10369 [PMID: 27562163]
Duan C, Byrdin M, Khatib ME, Henry X, Adam V, Bourgeois D (2015) Rational design of enhanced photoresistance in a photoswitchable fluorescent protein. Methods Appl Fluoresc 3(1):1–10 [DOI: 10.1088/2050-6120/3/1/014004]
Pletnev S, Subach FV, Dauter Z, Wlodawer A, Verkhusha VV (2012) A structural basis for reversible photoswitching of absorbance spectra in red fluorescent protein rsTagRFP. J Mol Biol 417:144–151 [PMID: 22310052]
Pennacchietti F, Serebrovskaya EO, Faro AR, Shemyakina NG Irina Iand Bozhanova, Kotlobay AA, Gurskaya NG, Bodén A, Dreier J, Chudakov DM, Lukyanov KA, Verkhusha VV, Mishin AS, Testa I (2018) Fast reversibly photoswitching red fluorescent proteins for live-cell RESOLFT nanoscopy. Nat Methods 15:601–604
Durisic N, Laparra-Cuervo L, Sandoval-Álvarez Á, Borbely JS, Lakadamyali M (2014) Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat Methods 11:156–162 [PMID: 24390439]
Stiel AC, Andresen M, Bock H, Hilbert M, Schilde J, Schoenle A, Eggeling C, Egner A, Hell SW, Jakobs S (2008) Generation of monomeric reversibly switchable red fluorescent proteins for far-field fluorescence nanoscopy. Biophys J 95:2989–2997 [PMID: 18658221]
Lavoie-Cardinal F, Jensen NA, Westphal V, Stiel AC, Chmyrov A, Bierwagen J, Testa I, Jakobs S, Hell SW (2014) Two-color resolft nanoscopy with green and red fluorescent photochromic proteins. ChemPhysChem 15(4):655–663 [PMID: 24449030]

MeSH Term

Algorithms
Animals
Fluorescent Antibody Technique
Fluorescent Dyes
Image Processing, Computer-Assisted
Light
Microscopy, Fluorescence, Multiphoton
Models, Theoretical
Optical Imaging
Staining and Labeling

Chemicals

Fluorescent Dyes

Word Cloud

Similar Articles

Cited By