Fluorescence resonance energy transfer imaging of cell signaling from in vitro to in vivo: Basis of biosensor construction, live imaging, and image processing

Development Growth and Differentiation

Volumn 55, Issue 4, 2013, Pages 515-522

  Aoki, Kazuhiro ^a,b   Kamioka, Yuji ^a   Matsuda, Michiyuki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Fluorescence resonance energy transfer; in vivo imaging; Intravital imaging; Two photon microscopy

Indexed keywords

BIOSENSOR; CELL CULTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; NONHUMAN; REVIEW; TRANSPOSON;

ALGORITHMS; ANIMALS; BIOSENSING TECHNIQUES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MICE; MICE, TRANSGENIC; MODELS, STATISTICAL; PHOTONS; SIGNAL TRANSDUCTION; SKIN;

EID: 84877822890     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12039     Document Type: Review

References (44)

1. Aoki, K., Komatsu, N., Hirata, E., Kamioka, Y. & Matsuda, M. 2012. Stable expression of FRET biosensors: a new light in cancer research. Cancer Sci. 103, 614-619.
2. Aoki, K. & Matsuda, M. 2009. Visualization of small GTPase activity with fluorescence resonance energy transfer-based biosensors. Nat. Protoc. 4, 1623-1631.
3. Aoki, K., Yamada, M., Kunida, K., Yasuda, S. & Matsuda, M. 2011. Processive phosphorylation of ERK MAP kinase in mammalian cells. Proc. Natl Acad. Sci. USA 108, 12675-12680.
4. Ashworth, S. L., Sandoval, R. M., Tanner, G. A. & Molitoris, B. A. 2007. Two-photon microscopy: visualization of kidney dynamics. Kidney Int. 72, 416-421.
5. Cahalan, M. D. & Parker, I. 2008. Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu. Rev. Immunol. 26, 585-626.
6. Camirand, G., Li, Q., Demetris, A. J., Watkins, S. C., Sholmchik, W. D., Rothstein, D. M. & Lakkis, F. G. 2011. Multiphoton intravital microscopy of the transplanted mouse kidney. Am. J. Transplant. 11, 2067-2074.
7. Cao, L., Kobayakawa, S., Yoshiki, A. & Abe, K. 2012. High resolution intravital imaging of subcellular structures of mouse abdominal organs using a microstage device. PLoS ONE 7, e33876.
8. Ding, S., Wu, X., Li, G., Han, M., Zhuang, Y. & Xu, T. 2005. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122, 473-483.
9. Egawa, G., Honda, T., Tanizaki, H., Doi, H., Miyachi, Y. & Kabashima, K. 2011. In vivo imaging of T-cell motility in the elicitation phase of contact hypersensitivity using two-photon microscopy. J. Invest. Dermatol. 131, 977-979.
10. Giepmans, B. N., Adams, S. R., Ellisman, M. H. & Tsien, R. Y. 2006. The fluorescent toolbox for assessing protein location and function. Science 312, 217-224.
11. Grienberger, C. & Konnerth, A. 2012. Imaging calcium in neurons. Neuron 73, 862-885.
12. Ishii, M., Egen, J. G., Klauschen, F., Meier-Schellersheim, M., Saeki, Y., Vacher, J., Proia, R. L. & Germain, R. N. 2009. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 458, 524-528.
13. Itoh, R. E., Kurokawa, K., Ohba, Y., Yoshizaki, H., Mochizuki, N. & Matsuda, M. 2002. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell Biol. 22, 6582-6591.
14. Jares-Erijman, E. A. & Jovin, T. M. 2003. FRET imaging. Nat. Biotechnol. 21, 1387-1395.
15. Kamioka, Y., Sumiyama, K., Mizuno, R., Sakai, Y., Hirata, E., Kiyokawa, E. & Matsuda, M. 2012. Live imaging of protein kinase activities in transgenic mice expressing FRET biosensors. Cell Struct. Funct. 37, 65-73.
16. Kamioka, Y., Yasuda, S., Fujita, Y., Aoki, K. & Matsuda, M. 2010. Multiple decisive phosphorylation sites for the negative feedback regulation of SOS1 via ERK. J. Biol. Chem. 285, 33540-33548.
17. Kawakami, K. & Noda, T. 2004. Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells. Genetics 166, 895-899.
18. Kedrin, D., Wyckoff, J., Sahai, E., Condeelis, J. & Segall, J. E. 2007. Imaging tumor cell movement in vivo. In: Current Protocols in Cell Biology/Editorial Board.(ed. Bonifacino J. S.) et al. New York: John Wiley and Sons. pp. 19.7.1-19.7.17 Chapter 19, Unit 19 17.
19. Kitano, M., Moriyama, S., Ando, Y., Hikida, M., Mori, Y., Kurosaki, T. & Okada, T. 2011. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 34, 961-972.
20. Kiyokawa, E., Aoki, K., Nakamura, T. & Matsuda, M. 2011. Spatiotemporal regulation of small GTPases as revealed by probes based on the principle of Forster Resonance Energy Transfer (FRET): implications for signaling and pharmacology. Annu. Rev. Pharmacol. Toxicol. 51, 337-358.
21. Komatsu, N., Aoki, K., Yamada, M., Yukinaga, H., Fujita, Y., Kamioka, Y. & Matsuda, M. 2011. Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 22, 4647-4656.
22. Kurokawa, K., Mochizuki, N., Ohba, Y., Mizuno, H., Miyawaki, A. & Matsuda, M. 2001. A pair of fluorescent resonance energy transfer-based probes for tyrosine phosphorylation of the CrkII adaptor protein in vivo. J. Biol. Chem. 276, 31305-31310.
23. Le Devedec, S. E., Van Roosmalen, W., Pont, C., Lalai, R., De Bont, H. & Van De Water, B. 2011. Two-photon intravital multicolour imaging to study metastatic behaviour of cancer cells in vivo. Methods Mol. Biol. 769, 331-349.
24. Li, W., Nava, R. G., Bribriesco, A. C., Zinselmeyer, B. H., Spahn, J. H., Gelman, A. E., Krupnick, A. S., Miller, M. J. & Kreisel, D. 2012. Intravital 2-photon imaging of leukocyte trafficking in beating heart. J. Clin. Invest. 122, 2499-2508.
25. Looney, M. R., Thornton, E. E., Sen, D., Lamm, W. J., Glenny, R. W. & Krummel, M. F. 2011. Stabilized imaging of immune surveillance in the mouse lung. Nat. Methods 8, 91-96.
26. Mcdole, J. R., Wheeler, L. W., Mcdonald, K. G., Wang, B., Konjufca, V., Knoop, K. A., Newberry, R. D. & Miller, M. J. 2012. Goblet cells deliver luminal antigen to CD103 + dendritic cells in the small intestine. Nature 483, 345-349.
27. Miyawaki, A. 2003. Visualization of the spatial and temporal dynamics of intracellular signaling. Dev. Cell 4, 295-305.
28. Miyawaki, A. 2011. Development of probes for cellular functions using fluorescent proteins and fluorescence resonance energy transfer. Annu. Rev. Biochem. 80, 357-373.
29. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M. & Tsien, R. Y. 1997. Fluorescent indicators for Ca2 + based on green fluorescent proteins and calmodulin. Nature 388, 882-887.
30. Mochizuki, N., Yamashita, S., Kurokawa, K., Ohba, Y., Nagai, T., Miyawaki, A. & Matsuda, M. 2001. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068.
31. Molitoris, B. A. & Sandoval, R. M. 2005. Intravital multiphoton microscopy of dynamic renal processes. Am. J. Physiol. Renal Physiol. 288, F1084-F1089.
32. Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M. & Miyawaki, A. 2004. Expanded dynamic range of fluorescent indicators for Ca(2 + ) by circularly permuted yellow fluorescent proteins. Proc. Natl Acad. Sci. USA 101, 10554-10559.
33. Nakamura, T., Aoki, K. & Matsuda, M. 2005. Monitoring spatio-temporal regulation of Ras and Rho GTPase with GFP-based FRET probes. Methods 37, 146-153.
34. Noguchi, J., Nagaoka, A., Watanabe, S., Ellis-Davies, G. C. R., Kitamura, K., Kano, M., Matsuzaki, M. & Kasai, H. 2011. In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice. J. Physiol. 589, 2447-2457.
35. Okada, T., Miller, M. J., Parker, I., Krummel, M. F., Neighbors, M., Hartley, S. B., O'Garra, A., Cahalan, M. D. & Cyster, J. G. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3, e150.
36. Sato, M., Ueda, Y., Takagi, T. & Umezawa, Y. 2003. Production of PtdInsP3 at endomembranes is triggered by receptor endocytosis. Nat. Cell Biol. 5, 1016-1022.
37. Sumiyama, K., Kawakami, K. & Yagita, K. 2010. A simple and highly efficient transgenesis method in mice with the Tol2 transposon system and cytoplasmic microinjection. Genomics 95, 306-311.
38. Takemoto, K., Nagai, T., Miyawaki, A. & Miura, M. 2003. Spatio-temporal activation of caspase revealed by indicator that is insensitive to environmental effects. J. Cell Biol. 160, 235-243.
39. Tanaka, K., Toiyama, Y., Inoue, Y., Uchida, K., Araki, T., Mohri, Y., Mizoguchi, A. & Kusunoki, M. 2012. Intravital imaging of gastrointestinal diseases in preclinical models using two-photon laser scanning microscopy. Surg. Today.
40. Tay, S., Hughey, J. J., Lee, T. K., Lipniacki, T., Quake, S. R. & Covert, M. W. 2010. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271.
41. Toiyama, Y., Mizoguchi, A., Okugawa, Y., Koike, Y., Morimoto, Y., Araki, T., Uchida, K., Tanaka, K., Nakashima, H., Hibi, M., Kimura, K., Inoue, Y., Miki, C. & Kusunoki, M. 2010. Intravital imaging of DSS-induced cecal mucosal damage in GFP-transgenic mice using two-photon microscopy. J. Gastroenterol. 45, 544-553.
42. Tsien, R. Y. & Harootunian, A. T. 1990. Practical design criteria for a dynamic ratio imaging system. Cell Calcium 11, 93-109.
43. Yusa, K., Rad, R., Takeda, J. & Bradley, A. 2009. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat. Methods 6, 363-369.
44. Zhang, J., Ma, Y., Taylor, S. S. & Tsien, R. Y. 2001. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl Acad. Sci. USA 98, 14997-15002.