Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions

Biophysical Journal

Volumn 88, Issue 2, 2005, Pages 1224-1237

  Peter, Marion ^a   Ameer Beg, Simon M ^a,b   Hughes, Michael K Y ^a   Keppler, Melanie D ^a   Prag, Søren ^a   Marsh, Mark ^c   Vojnovic, Borivoj ^b   Ng, Tony ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b MOUNT VERNON HOSPITAL   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; ENHANCED GREEN FLUORESCENT PROTEIN; MEMBRANE RECEPTOR; PROTEIN KINASE; PROTEIN KINASE C ALPHA; RED FLUORESCENT PROTEIN; RED FLUORESCENT PROTEIN 1; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN; PROTEIN KINASE C;

ARTICLE; CANCER CELL; CELL VACUOLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME LOCALIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MULTIPHOTON FLUORESCENCE LIFETIME IMAGING MICROSCOPY; MULTIPHOTON MICROSCOPY; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; TECHNIQUE; BREAST TUMOR; COMPARATIVE STUDY; EVALUATION; METABOLIC CLEARANCE RATE; METABOLISM; METHODOLOGY; PATHOLOGY; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; TISSUE DISTRIBUTION; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; METABOLIC CLEARANCE RATE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; PROTEIN KINASE C; RECEPTORS, CXCR4; RECOMBINANT FUSION PROTEINS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TISSUE DISTRIBUTION;

EID: 21244478918     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.050153     Document Type: Article

References (67)

1. Ameer-Beg, S. M., P. R. Barber, R. J. Hodgkiss, R. J. Locke, R. G. Newman, G. M. Tozer, B. Vojnovic, and S. Wilson. 2002. Application of multiphoton steady-state and lifetime imaging to mapping of tumour vascular architecture in vivo. Proc SPIE. 4620:85-95.
2. Ameer-Beg, S. M., N. Edme, M. Peter, P. R. Barber, and T. B. V. Ng. 2003. Imaging protein-protein interactions by multiphoton FLIM. Proc. SPIE. 5139:180-189.
3. Anilkumar, N., M. Parsons, R. Monk, T. Ng, and J. C. Adams. 2003. Interaction of fascin and protein kinase Cα: a novel intersection in cell adhesion and motility. EMBO J. 22:5390-5402.
4. Bastiaens, P. I., and R. Pepperkok. 2000. Observing proteins in their natural habitat: the living cell. Trends Biochem. Sci. 25:631-637.
5. Becker, W., K. Benndorf, A. Bergmann, C. Biskup, K. König, U. Tirlapur, and T. Zimmer. 2001. FRET measurements by TCSPC laser scanning microscopy. Proc. SPIE. 4431:414-419.
6. Beechem, J. M., and L. Brand. 1986. Global analysis of fluorescence decay: applications to some unusual experimental and theoretical studies. Photochem. Photobiol. 44:323-330.
7. Beechem, J. M., and E. Haas. 1989. Simultaneous determination of intramolecular distance distributions and conformational dynamics by global analysis of energy transfer measurements. Biophys. J. 55:1225-1236.
8. Bivona, T. G., and M. R. Philips. 2003. Ras pathway signaling on endomembranes. Curr. Opin. Cell Biol. 15:136-142.
9. Brown, C. M., and N. O. Petersen. 1998. An image correlation analysis of the distribution of clathrin associated adaptor protein (AP-2) at the plasma membrane. J. Cell Sci. 111:271-281.
10. Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
11. Ellenberg, J., J. Lippincott-Schwartz, and J. F. Presley. 1998. Two-color green fluorescent protein time-lapse imaging. Biotechniques. 25:838-846.
12. Erickson, M. G., D. L. Moon, and D. T. Yue. 2003. DsRed as a potential FRET partner with CFP and GFP. Biophys. J. 85:599-611.
13. Förster, T. 1948. Intermolecular energy migration and fluorescence. Annals Phys. 6:55-75.
14. Gadella, T. W., Jr., and T. M. Jovin. 1995. Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy. A stereochemical model for tyrosme I kinase receptor activation. J. Cell Biol. 129:1543-1558.
15. Gordon, G. W., G. Berry, X. H. Liang, B. Levine, and B. Herman. 1998. Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74:2702-2713.
16. Guinamard, R., N. Signoret, M. Ishiai, M. Marsh, T. Kurosaki, J. V. Ravetch, and I. Masamichi. 1999. B cell antigen receptor engagement inhibits stromal cell-derived factor (SDF)-1α chemotaxis and promotes protein kinase C (PKC)-induced internalization of CXCR4. J. Exp. Med. 189:1461-1466.
17. Heikal, A. A., S. T. Hess, and W. W. Webb. 2001. Multiphoton molecular spectroscopy and excited state dynamics of enhanced green fluorescent protein (EGFP): acid-base specificity. Chem. Phys. 274:37-55.
18. Herreros, J., T. Ng, and G. Schiavo. 2001. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell. 12:2947-2960.
19. Johnsen, S., and E. A. Widder. 1999. The physical basis of transparency in biological tissue: ultrastructure and the minimization of light scattering. J. Theor. Biol. 199:181-198.
20. Kneen, M., J. Farinas, Y. Li, and A. S. Verkman. 1998. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J. 74:1591-1599.
21. Lakowicz, J. 1999. Principles of fluorescence spectroscopy. Kluwer Academic/Plenum Publishers, New York.
22. Legg, J. W., C. A. Lewis, M. Parsons, T. Ng, and C. M. Isacke. 2002. A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4:399-407.
23. Lippincott-Schwartz, J., and G. H. Patterson. 2003. Development and use of fluorescent protein markers in living cells. Science. 300:87-91.
24. Malvezzi-Campeggi, F., M. Jahnz, K. G. Heinze, P. Dittrich, and P. Schwille. 2001. Light-induced flickering of DsRed provides evidence for distinct and interconvertible fluorescent states. Biophys. J. 81:1776-1785.
25. Miyawaki, A. 2003. Visualisation of the spatial and temporal dynamics of intracellular signaling. Dev. Cell. 4:295-305.
26. Mizuno, H., A. Sawano, P. Eli, H. Hama, and A. Miyawaki. 2001. Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry. 40:2502-2510.
27. Moore, M. A. 2001. The role of chemoattraction in cancer metastases. Bioessays. 23:674-676.
28. Morton, P. E., T. C. Ng, S. A. Roberts, B. Vojnovic, and S. M. Ameer-Beg. 2003. Time-resolved multiphoton imaging of the interaction between the PKC and the NFkB cell signalling pathway. Proc. SPIE. 5139:216-222.
29. Muller, A., B. Homey, H. Soto, N. Ge, D. Catron, M. E. Buchanan, T. McClanahan, E. Murphy, W. Yuan, S. N. Wagner, J. L. Barrera, A. Mohar, E. Verastegui, and A. Zlotnik. 2001. Involvement of chemokine receptors in breast cancer metastasis. Nature. 410:50-56.
30. Neil, M. A., A. Squire, R. Juskaitis, P. I. Bastiaens, and T. Wilson. 2000. Wide-field optically sectioning fluorescence microscopy with laser illumination. J. Microsc. 197:1-4.
31. Nelsestuen, G. L., and M. D. Bazzi. 1991. Activation and regulation of protein kinase C enzymes. J. Bioenerg. Biomembr. 23:43-61.
32. Ng, T., M. Parsons, W. E. Hughes, J. Monypenny, D. Zicha, A. Gautreau, M. Arpin, S. Gschmeissner, P. J. Verveer, P. I. Bastiaens, and Peter J. Parker. 2001. Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 20:2723-2741.
33. Ng, T., D. Shima, A. Squire, P. I. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker. 1999a. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18:3909-3923.
34. Ng, T., A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker. 1999b. Imaging protein kinase Cα activation in cells. Science. 283:2085-2089.
35. Oancea, E., and T. Meyer. 1998. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell. 95:307-318.
36. O'Connor, D. V., and D. Phillips. 1984. Time Correlated Single Photon Counting. Academic Press, London, UK.
37. Parker, P. J., and J. Murray-Rust. 2004. PKC at a slance. J. Cell Sci. 117:131-132.
38. Parsons, M., S. M. Ameer-Beg, and B. Vojnovic. 2004. Imaging protein-protein interactions in cell motility using FRET. Biochem. Soc. Trans. 32:431-433.
39. Parsons, M., M. D. Keppler, A. Kline, A. Messent, M. J. Humphries, R. Gilchrist, I. R. Hart, C. Quittau-Prevostel, W. E. Hughes, P. J. Parker, and T. Ng. 2002. Site-directed perturbation of protein kinase C-integrin interaction blocks carcinoma cell chemotaxis. Mol. Cell. Biol. 22:5897-5911.
40. Patterson, G., R. N. Day, and D. Piston. 2001. Fluorescent protein spectra. J. Cell Sci. 114:837-838.
41. Patterson, G. H., S. M. Knobel, W. D. Sharif, S. R. Kain, and D. W. Piston. 1997. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys. J. 73:2782-2790.
42. Periasamy, A. 2001. Fluorescence resonance energy transfer microscopy: a mini review. J. Biomed. Opt. 6:287-291.
43. Peter, M., and S. M. Ameer-Beg. 2004. Imaging molecular interactions by multiphoton FLIM. Biol. Cell. 96:231-236.
44. Pollock, B. A., and R. Heim. 1999. Using GFP in FRET-based applications. Trends Cell Biol. 9:57-60.
45. Polo, S., S. Pece, and P. P. Di Fiore. 2004. Endocytosis and cancer. Curr. Opin. Cell Biol. 16:156-161.
46. Rizzo, M. A., G. H. Springer, B. Granada, and D. W. Piston. 2004. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22:445-449.
47. Roberts, M., S. Barry, A. Woods, P. van der Sluijs, and J. Norman. 2001. PDGF-regulated rab4-dependent recycling of αvβ3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11:1392-1402.
48. Schonle, A., M. Glatz, and S. W. Hell. 2000. Four-dimensional multiphoton microscopy with time-correlated single-photon counting. Appl. Optics. 39:6306-6311.
49. Selvin, P. R. 2000. The renaissance of fluorescence resonance energy transfer. Nat. Struct. Biol. 7:730-734.
50. Seto, E. S., H. J. Bellen, and T. E. Lloyd. 2002. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16:1314-1336.
51. Signoret, N., J. Oldridge, A. Pelchen-Matthews, P. J. Klasse, T. Tran, L. F. Brass, M. M. Rosenkilde, T. W. Schwartz, W. Holmes, W. Dallas, and M. A. Luther, T. N. Wells. I. A. Hoxie, and M. Marsh. 1997. Phorbol esters and SDF-1 induce rapid endocytosis and down-modulation of the chemokine receptor CXCR4. J. Cell Biol. 139:651-664.
52. Signoret, N., M. M. Rosenkilde, P. J. Klasse, T. W. Schwartz, M. H. Malim, J. A. Hoxie, and M. Marsh. 1998. Differential reaulation of CXCR4 and CCR5 endocytosis. J. Cell Sci. 111:2819-2830.
53. Slater, S. J., J. L. Seiz, A. C. Cook, C. J. Buzas, S. A. Malinowski, J. L. Kershner, B. A. Stagliano, and C. D. Stubbs. 2002. Regulation of PKCα activity by C1-C2 domain interactions. J. Biol. Chem. 277:15277-15285.
54. Squire, A., and P. I. Bastiaens. 1999. Three-dimensional image restoration in fluorescence lifetime imaging microscopy. J. Microsc. 193:36-49.
55. Stryer, L. 1978. Fluorescence energy transfer as a spectroscopic ruler. Ann. Rev. Biochem. 47:819-846.
56. Suhling, K., I. Siegel, D. Phillips, P. M. French, S. Leveque-Fort, S. E. Webb, and D. M. Davis. 2002. Imaging the environment of green fluorescent protein. Biophys. J. 83:3589-3595.
57. Taunton, J. 2001. Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr. Opin. Cell Biol. 13:85-91.
58. Taunton, J., B. A. Rowning, M. L. Coughlin, M. Wu, R. T. Moon, T. J. Mitchison, and C. A. Larabell. 2000. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148:519-530.
59. Tramier, M., I. Gautier, T. Piolot, S. Ravalet, K. Kemnitz, J. Coppey, C. Durieux, V. Mignotte, and M. Coppey-Moisan. 2002. Picosecond-hetero-FRET microscopy to probe protein-protein interactions in live cells. Biophys. J. 83:3570-3577.
60. Tsien, R. Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544.
61. van Weert, A. W., H. J. Geuze, and W. S. B. Groothuis. 2000. Primaquine interferes with membrane recycling from endosomes to the plasma membrane through a direct interaction with endosomes which does not involve neutralisation of endosomal pH nor osmotic swelling of endosomes. Eur. J. Cell Biol. 79:394-399.
62. Verveer, P. J., and P. I. Bastiaens. 2003. Evaluation of global analysis algorithms for single frequency fluorescence lifetime imaging microscopy data. J. Microsc. 209:1-7.
63. Verveer, P. J., A. Squire, and P. I. Bastiaens. 2000a. Global analysis of fluorescence lifetime imaging microscopy data. Biophys. J. 78:2127-2137.
64. Verveer, P. J., A. Squire, and P. I. Bastiaens. 2001. Improved spatial discrimination of protein reaction states in cells by global analysis and deconvolution of fluorescence lifetime imaging microscopy data. J. Microsc. 202:451-456.
65. Verveer, P. J., F. S. Wouters, A. R. Reynolds, and P. I. Bastiaens. 2000b. Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. Science. 290:1567-1570.
66. Wouters, F. S., P. J. Verveer, and P. I. Bastiaens. 2001. Imaging biochemistry inside cells. Trends Cell Biol. 11:203-211.
67. Zhang, J., R. E. Campbell, A. Y. Ting, and R. Y. Tsien. 2002. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3:906-918.