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1 Microscopic Fluorescence Resonance Energy Transfer 2 1 Fluorescence Resonance Energy Transfer FRET FRET Microscopic FRET FRET FRET DNA DNA FRET Microscopic FRET DNA DNA RNA 1 8 Fluorescence Resonance Energy Transfer FRET fluorescence lifetime DNA FRET 2 donor acceptor 100Å donor acceptor 13 FRET 2 2 FRET 1940 Förster 14 Stryer Haugland 15,16
2 94 green fluorescent protein GFP FRET Microscopic FRET 9,10 FRET 11,12,13 DNA DNA FRET Microscopic FRET FRET 13,17 1a t 0 N 0 I 0 k f, k nr t N t I t I t k fn t k f N 0 exp [ k f k nr t] I 0 exp t/τ 1 k f k nr 1/τ 2 1 a FRET b FRET τ fluorescence lifetime I t τ FRET time-domain frequency-domain 13 ω φ m 2 11,12 τ φ ω 1 tan φ 3 τ m ω 1 [ 1 m 2 1 ] 1/2 4
3 Microscopic FRET 95 2 frequency-domain ω φ m τ φ phase lifetime τ m modulation lifetime τ φ τ m FRET FRET donor acceptor 1 b donor acceptor FRET FRET donor acceptor donor acceptor 1 1 single donor and acceptor model 1 donor acceptor multiple acceptor model 13 single donor and acceptor model Förster 18 single donor and acceptor model FRET Förster 19 3 DNA Ho PI A F spectral overlap donor acceptor 23 k ret 9000(ln 10) κ π 5 n 4 N A r 6 J k f 5 n N A κ 2 orientation factor J spectral overlap donor acceptor r donor acceptor FRET donor acceptor spectral overlap 3 donor acceptor 100Å acceptor FRET 5 k ret donor acceptor r 6 FRET donor acceptor multiple acceptor model donor acceptors FRET 13 donor acceptor donor acceptor
4 96 Lakowicz Blumen 20 21,22 Blumen Tris-HCl DNA 2 DNA Hoechst Ho; donor Propidium iodide PI; acceptor FRET 23 3 Ho PI Förster distance R Å Ho PI FRET donor-acceptor pair 23 donor-acceptor pair multiple acceptor model 1 donor 100Å acceptor Ho donor PI acceptor Ho PI FRET donor 4 23 donor PI 23 4 DNA 200 µm Ho 4 µm PI FRET PI 0, 2, 10, 20, 30, 40, 50 µm 350nm 23 PI Ho 350nm 23 Comcentrations 1 Component 2 Component 3 Component [PI] τ i(ns) f i χ R 2 τ i(ns) f i χ R 2 τ i (ns) f i mτ (ns) χ R 2 00 µm µm µm µm µm µm µm mτ : mean lifetime
5 Microscopic FRET 97 PI 1 Ho 100Å PI multi-exponential decay 23 FRET k ret, k f, k nr, FRET τ da 2 k f k nr k ret 1 /τ da 6 E E 1 τ da/τ d 7 1 D da/d d 8 13,17 D d τ d donor FRET D da τ da donor acceptor FRET single donor and acceptor model 5 donor acceptor r donor acceptor r FRET donor acceptor FRET FRET 1 acceptor donor 8 donor D d acceptor donor D da 24,25 acceptor donor donor acceptor donor D da acceptor acceptor FRET donor D d 26 2 donor acceptor FRET donor D da FRET acceptor F da F da/ D da 27 3 acceptor donor ns fluorescence lifetime imaging microscopy; FLIM 11,12 FRET 7 donor acceptor donor FRET 24,25 FRET DNA DNA FRET
6 98 mouse fibroblasts, 3T3-Swiss albino, ATCC no. CCL-92 Adenine-Thymine AT DNA Ho Guanine-Cytosine GC DNA 7-aminoactinomysin D 7- AAD Ho donor 7-AAD acceptor FRET 24,25 Ho FLIM 7-AAD 5 24,25 Ho 7-AAD Ho 5a b Ho 2 phase lifetime τ φ modulation lifetime τ m 5c d e f Ho 7- AAD phase lifetime modulation lifetime 6 24 donor multiexponential decay 24 DNA Ho 7-AAD multiple acceptor FRET Ho 7-AAD Ho AT DNA GC DNA 5h 5g AT 5a AT GC DNA DNA 50 Ho 7- AAD FRET 7 25 S G2/M 5 Ho 0.4 µm 7-AAD 0.8 µm mouse fibroblasts, 3T3- Swiss albino, ATCC no. CCL-92 a), b) Ho c), d), e), f) Ho Ho g) b) a) Dda/Dd h) FRET d ns ns 24, 25
7 Microscopic FRET Ho modulation lifetime phase lifetime 24 7 Ho 7-AAD FRET 25 DNA FRET Ho Ho Ho 7-AAD Ho FRET 5g f 1 FRET donor acceptor donor FRET donor FRET acceptor donor acceptor FRET donor-acceptor FRET donor FRET FRET acceptor donor 2 FRET
8 FRET donor acceptor donor acceptor donor acceptor donor acceptor cross excitation donor acceptor cross talk 3 donor donor donor filter set donor FRET acceptor FRET filter set acceptor acceptor acceptor filter set 3 donor acceptor donor acceptor 9 9 FRET 28,30 corrected FRET Fda Dda Fd/Dd Ada Fa/Aa 9 F da, D da, Ada donor acceptor FRET filter set donor filter set acceptor filter set F d, D d, A d donor FRET filter set donor filter set acceptor filter set Fa Da Aa acceptor FRET filter set donor filter set acceptor filter set 4 single donor and acceptor model donor acceptor 1 1 donor acceptor multiple acceptor model acceptor donor donor acceptor acceptor donor FRET donor acceptor donor acceptor FRET FRET donor FRET donor acceptor 9 corrected FRET donor acceptor normalized FRET 30 normalized FRET corrected FRET G Dda Ada 10 G corrected FRET G Ho 7-AAD FRET 8 5g 8a donor acceptor FRET donor-acceptor 8b donor acceptor AT DNA DNA GC Ho 7-AAD
9 Microscopic FRET DNA Ho 7-AAD 9 10 FRET Ho 7-AAD a b a b DNA 3,6 8,29 DNA FRET DNA DNA FRET DNA 1 Ashihara T, Kamachi M, Urata Y, Kusuzaki K, Takeshita H, Kagawa K: Multiparametric analysis using autostage cytofluorometry. Acta. Histochem. Cytochem., 19: 51 59, Malignant insulinoma :, 6, , DNA, 7, , , 29, , Urata Y, Itoi H., Murata S, Konishi E, Ueda K, Azumi Y, and Ashihara T: From cytofluorometry to fluorescence image analysis. Acta Histochem. Cytochem., 24, , DNA, 100, , ,,, 39, 79 83, , 1 5, Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY: Fluorescent indicators for Ca2+ based on green fluorescent pro-
10 102 teins and calmodulin. Nature, 28; 388: 882 7, Mochizuki N, Yamashita S, Kurokawa K, Ohba Y, Nagai T, Miyawaki A, Matsuda M: Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature, 28; 411; , Lakowicz, JR, and Berndt, K W: Lifetime-selective fluorescence imaging using an rf phase-sensitive camera. Rev. Sci. Instrum., 62: , (Reprinted in SPIE Milestone Series on Optical Tomography, Murata S, Herman P, and Lakowicz JR: Texture analysis of fluorescence lifetime images of ATand GC-rich regions in nuclei. J. Histochem. Cytochem., 49(11): , Lakowicz, JR: Principles of Fluorescence Spectroscopy, 2nd Edition, Plenum Publishers, New York, Förster Th: Intermolecular energy migration and fluorescence. Ann. Phys. 2:55-75, 1948 Translated by R. S. Knox, Department of Physics and Astronomy, University of Rochester, Rochester, NY Stryer L: Fluorescence energy transfer as a spectroscopic ruler. Annu Rev Biochem., 47: Stryer L, Haugland RP: Energy transfer: a spectroscopic ruler. Proc Natl Acad Sci U S A., 58 2 : , , Clegg R M: Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol., 211: , Förster Th: Modern quantum chemistry. O. Sinanoglu (ed., Academic Press, New York, p93, Blumen A, Manz J: On the concentration and time dependence of the energy transfer to randomly distributed acceptors. J. Chemi. Phys., Maliwal BP, Kusba J, Lakowicz JR: Fluorescence energy transfer in one dimension: frequency-domain fluorescence study of DNA-fluorophore complexes. Biopolymers., 35(2 : , Li L, Gryczynski I, Lakowicz JR: Resonance energy transfer study using a rhenium metal-ligand lipid conjugate as the donor in a model membrane. Chem Phys Lipids, 101(2 : , Murata S, Kusba J, Piszczek G, Gryczynski I, and Lakowicz JR: Donor fluorescence decay analysis for energy transfer in double-helical DNA with various acceptor concentration Biopolymers, 57(5 : , Murata S, Herman P, Lin HJ, Lakowicz JR: Fluorescence lifetime imaging of nuclear DNA: effect of fluorescence resonance energy transfer. Cytometry, 41 3 : , Murata S, Herman P, Lakowicz JR: Texture analysis of fluorescence lifetime images of nuclear DNA with effect of fluorescence resonance energy transfer. Cytometry., 43(2 : , Miyawaki A, Tsien RY: Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol., 327: , Uchiyama H, Hirano K, Kashiwasake-Jibu M, Taira K: Detection of undergraded oligonucleotides in vivo by fluorescence resonance energy transfer. J. Biol. Chem., 271( , Jovin TM, and DJ Arndt-Jovin: FRET microscopy: digital imaging of fluorescence resonance energy transfer. Application in cell biology. In cell structure and function by microspectrofluorometry. E. Kohen, J. S. Ploem, and J. G. Hirschberg. Editors. Academic Press, Orlando. FL , , Gordon GW, Berry G, Liang XH, Levine B, Herman B: Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys J., 74 5 : , 1998.
11 Microscopic FRET 103 Microscopic Fluorescence Resonance Energy Transfer on Nuclear DNA Shin-ichi MURATA, Kunio MOCHIZUKI, Tadao NAKAZAWA, Tetsuo KONDO, Nobuki NAKAMURA and Ryohei KATOH Department of Pathology, Yamanashi Medical University, Yamanashi , Japan Abstract: DNA fluorescence dyes have been used to study DNA dynamics, chromatin structure and cell cycle analysis. However, most microscopic fluorescence studies of nuclear DNA have been using the steady state approach and have not taken advantage of additional information content of the fluorescence resonance energy transfer (FRET). FRET is the transfer of the excited-state energy from the initially excited donor to an acceptor. As FRET efficiency depends on the distance between donor and acceptor, microscopic FRET is a useful technique used for quantifying the distance between donor and acceptor in the cells. However, microscopic FRET measurements can suffer from several causes of distortion, which include fluorescence cross talk and the dependence of FRET on the concentration of donor and acceptor. We used frequency-domain fluorescence lifetime measurement as well as the steady state approach to study the spatial distribution of DNA-bound donor Hoechst 33258: Ho and acceptor 7-aminoactinomycin D: 7-AAD on nuclear DNA. Additions of the 7-AAD acceptor resulted in a spatially non-homogeneous decrease in fluorescence intensity and the lifetime of the Ho-stained nuclei. The spatially dependent phase and modulation values of Ho in the presence of 7-AAD, also showed that the Ho decay becomes non-exponential. Key words: fluorescence resonance energy transfer, fluorescence lifetime, microscopy, cell cycle, DNA
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