A Flow Cytometric Method to Detect Protein-Protein Interaction in Living Cells by Directly Visualizing Donor Fluorophore Quenching during CFP→YFP Fluorescence Resonance Energy Transfer (FRET)

Cytometry Part A

Volumn 55, Issue 2, 2003, Pages 71-85

  He, Liusheng ^a,c   Olson, Douglas P ^a   Wu, Xiaoli ^a   Karpova, Tatiana S ^b   McNally, James G ^b   Lipsky, Peter E ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cyan fluorescent protein; Donor quenching; Flow cytometry; Fluorescence resonance energy transfer (FRET); Protein protein interaction; TNF receptor associated factor (TRAF); Yellow fluorescent protein

Indexed keywords

CASPASE INHIBITOR; CYAN FLUORESCENT PROTEIN; HYBRID PROTEIN; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CYTOMETRY; ENERGY TRANSFER; FLOW CYTOMETRY; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

EID: 0346874407     PISSN: 15524922     EISSN: None     Source Type: Journal    
DOI: 10.1002/cyto.a.10073     Document Type: Article

References (47)

1. Matyus L. Fluorescence resonance energy transfer measurements on cell surfaces. A spectroscopic tool for determining protein interactions. J Photochem Photobiol B 1992;12:323-337.
2. Szollosi J, Nagy P, Sebestyen Z, Damjanovicha S, Park JW, Matyus L. Applications of fluorescence resonance energy transfer for mapping biological membranes. J Biotechnol 2002;82:251-266.
3. Didenko W. DNA probes using fluorescence resonance energy transfer (FRET): designs and applications. Biotechniques 2001;31:1106-1116, 1118, 1120-1101.
4. Gordon GW, Berry G, Liang XH, Levine B, Herman B. Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys J 1998;74:2702-2713.
5. Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science 2000;288:2351-2354.
6. Chan FK, Siegel RM, Zacharias D, Swofford R, Holmes KL, Tsien RY, Lenardo MJ. Fluorescence resonance energy transfer analysis of cell surface receptor interactions and signaling using spectral variants of the green fluorescent protein. Cytometry 2001;44:361-368.
7. He L, Bradrick TD, Karpova TS, Wu X, Fox MH, Fischer R, McNally JG, Knutson JR, Grammer AC, Lipsky PE. Flow cytometric measurement of fluorescence (Förster) resonance energy transfer from cyan fluorescent protein to yellow fluorescent protein using single laser excitation at 458 nm. Cytometry 2003;53A:39-54.
8. Llopis J, Westin S, Ricote M, Wang Z, Cho CY, Kurokawa R, Mullen TM, Rose DW, Rosenfeld MG, Tsien RY, Glass CK, Wang J. Ligand-dependent interactions of coactivators steroid receptor coactivator-1 and peroxisome proliferator-activated receptor binding protein with nuclear hormone receptors can be imaged in live cells and are required for transcription. Proc Natl Acad Sci USA 2000;97:4363-4368.
9. Mascarenhas J, Soppa J, Strunnikov AV, Graumann PL. Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 2002;21:3108-3118
10. Onuki R, Nagasaki A, Kawasaki H, Baba T, Uyeda TQ, Taira K. Confirmation by FRET in individual living ceus of the absence of significant amyloid beta-mediated caspase 8 activation. Proc Natl Acad Sci USA 2002;99:14716-14721.
11. Sato M, Ozawa T, Inukai K, Asano T, Umezawa Y. Fluorescent indicators for imaging protein phosphorylation in single living cells. Nat Biotechnol 2002;20:287-294.
12. Siegel RM, Chan FK, Zacharias DA, Swofford R, Holmes KL, Tsien RY, Lenardo MJ. Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein. Sci STKE 2000;2000:PL1.
13. Tertoolen LG, Blanchetot C, Jiang G, Overvoorde J, Gadella Jr TW, Hunter T, den Hertog J. Dimerization of receptor protein-tyrosine phosphatase alpha in living cells. BMC Cell Biol 2001;2:8.
14. Tramier M, Gautier I, Piolot T, Ravalet S, Kemnitz K, Coppey J, Durieux C, Mignotte V, Coppey-Moisan M. Picosecond-hetero-FRET microscopy to probe protein-protein interactions in live cells. Biophys J 2002;83:3570-3577.
15. Yang F, Moss LG, Phillips Jr GN. The molecular structure of green fluorescent protein. Nat Biotechnol 1996;14:1246-1251.
16. Hofmann A, Iwai H, Hess S, Pluckthun A, Wlodawer A. Structure of cyclized green fluorescent protein. Acta Crystallogr D Biol Crystallogr 2002;58:1400-1406.
17. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. Crystal structure of the Aequorea victoria green fluorescent protein. Science 1996;273:1392-1395.
18. Zacharias DA. Sticky caveats in an otherwise glowing report: oligomerizing fluorescent proteins and their use in cell biology. Sci STKE 2002;2002:PE23.
19. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002;296:913-916.
20. Luo KQ, Yu VC, Pu Y, Chang DC. Application of the fluorescence resonance energy transfer method for studying the dynamics of caspase-3 activation during UV-induced apoptosis in living HeLa cells. Biochem Biophys Res Commun 2001;283:1054-1060.
21. Ting AY, Kain KH, Klemke RL, Tsien RY. Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells. Proc Natl Acad Sci USA 2001;98:15003-15008.
22. Xia Z, Liu Y. Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes. Biopbys J 2001;81:2395-2402.
23. Karpova TS, Baumann CT, He L, Wu X, Grammer A, Lipsky P, Hager GL, McNally JG. Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J Microsc 2003;209:56-70.
24. Harpur AG, Wouters FS, Bastiaens PI. Imaging FRET between spectrally similar GFP molecules in single cells. Nat Biotechnol 2001;19:167-169.
25. Haraguchi T, Shimi T, Koujin T, Hashiguchi N, Hiraoka Y. Spectral imaging fluorescence microscopy. Genes Cells 2002;7:881-887.
26. Emptage NJ. Fluorescent imaging in living systems. Curr Opin Pharmacol 2001;1:521-525.
27. Bastiaens PI, Squire A. Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol 1999;9:48-52.
28. Magee T, Pirinen N, Adler J, Pagakis SN, Parmryd I. Lipid rafts: cell surface platforms for T cell signaling. Biol Res 2002;35:127-131.
29. Latif R, Graves P, Davies TF. Ligand-dependent inhibition of oligomerization at the human thyrotropin receptor. J Biol Chem 2002;277:45059-45067.
30. Wouters FS, Bastiaens PI. Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells. Curr Biol 1999;9:1127-1130.
31. Tron L, Szollosi J, Damianovich S, Helliwell SH, Arndt-Jovin DJ, Jovin TM. Flow cytometric measurement of fluorescence resonance energy transfer on cell surfaces. Quantitative evaluation of the transfer efficiency on a cell-by-cell basis. Biophys J 1984;45:939-946.
32. Szollosi J, Tron L, Damjanovich S, Helliwell SH, Arndt-Jovin D, Jovin TM. Fluorescence energy transfer measurements on cell surfaces: a critical comparison of steady-state fluorimetric and flow cytometric methods. Cytometry 1984;5:210-216.
33. Batard P, Szollosi J, Luescher I, Cerottini JC, MacDonald R, Romero P. Use of phycoerythrin and allophycocyanin for fluorescence resonance energy transfer analyzed by flow cytometry: advantages and limitations. Cytometry 2002;48:97-105.
34. Szollosi J, Damjanovich S, Matyus L. Application of fluorescence resonance energy transfer in the clinical laboratory: routine and research. Cytometry 1998;34:159-179.
35. Siegel RM, Frederiksen JK, Zacharias DA, Chan FK, Johnson M, Lynch D, Tsien RY, Lenardo MJ. Fas preassociation required for apoptosis signaling and dominant inhibition by pathogenic mutations. Science 2000;288:2354-2357.
36. McWhirter SM, Pullen SS, Holton JM, Crute JJ, Kehry MR, Alber T. Crystallographic analysis of CD40 recognition and signaling by human TRAF2. Proc Natl Acad Sci USA 1999;96:8408-8413.
37. Park YC, Burkitt V, Villa AR, Tong L, Wu H. Structural basis for self-association and receptor recognition of human TRAF2. Nature 1999;398:533-538.
38. Pullen SS, Miller HG, Everdeen DS, Dang TT, Crute JJ, Kehry MR. CD40-tumor necrosis factor receptor-associated factor (TRAF) interactions: regulation of CD40 signaling through multiple TRAF binding sites and TRAF hetero-oligomerization. Biochemistry 1998;37:11836-11845.
39. Leo E, Welsh K, Matsuzawa S, Zapata JM, Kitada S, Mitchell RS, Ely KR, Reed JC. Differential requirements for tumor necrosis factor receptor-associated factor family proteins in CD40-mediated induction of NF-kappaB and Jun N-terminal kinase activation. J Biol Chem 1999; 274:22414-22422.
40. Brodeur SR, Cheng G, Baltimore D, Thorlev-Lawson DA. Localization of the major NF-kappaB-activating site and the sole TRAF3 binding site of LMP-1 defines two distinct signaling motifs. J Biol Chem 1997;272:19777-19784.
41. Tabata M, Tabata R, Grabowski DR, Bukowski RM, Ganapathi MK, Ganapathi R. Roles of NF-kappaB and 26 S proteasome in apoptotic cell death induced by topoisomerase I and II poisons in human nonsmall cell lung carcinoma. J Biol Chem 2001;276:8029-8036.
42. Leo E, Deveraux QL, Buchholtz C, Welsh K, Matsuzawa S, Stennicke HR, Salvesen GS, Reed JC. TRAF1 is a substrate of caspases activated during tumor necrosis factor receptor-alpha-induced apoptosis. J Biol Chem 2001;276:8087-8093.
43. Ely KR, Li C. Structurally adaptive hot spots at a protein interaction interface on TRAF3. J Mol Recognit 2002;15:286-290.
44. Chung JY, Park YC, Ye H, Wu H. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J Cell Sci 2002;115:679-688.
45. Bradley JR, Pober JS. Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 2001;20:6482-6491.
46. Gravallese EM, Galson DL, Goldring SR, Auron PE. The role of TNF-receptor family members and other TRAF-dependent receptors in bone resorption. Arthritis Res 2001;3:6-12.
47. Inoue J, Ishida T, Tsukamoto N, Kobayashi N, Naito A, Azuma S, Yamamoto T. Tumor necrosis factor receptor-associated factor (TRAF) family: adapter proteins that mediate cytokine signaling. Exp Cell Res 2000;254:14-24.