A genetically encoded Förster resonance energy transfer biosensor for two-photon excitation microscopy

Analytical Biochemistry

Volumn 413, Issue 2, 2011, Pages 192-199

  Kumagai, Yuka ^a   Kamioka, Yuji ^a   Yagi, Shunsuke ^a   Matsuda, Michiyuki ^a   Kiyokawa, Etsuko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Cyst; F rster resonance energy transfer; Phosphoinositides; sREACh; TFP

Indexed keywords

AMINO ACIDS; BIOSENSORS; CELL MEMBRANES; ENERGY TRANSFER; FORSTER RESONANCE ENERGY TRANSFER; PHOSPHOLIPIDS; PHOTONS; PROTEINS; RESONANCE; SIGNAL TO NOISE RATIO; SIGNAL TRANSDUCTION;

CYST; PHOSPHOINOSITIDES; RESONANCE ENERGY TRANSFER; SREACH; THREE-DIMENSIONAL ENVIRONMENT; THREE-DIMENSIONAL STRUCTURE; TWO-PHOTON EXCITATION MICROSCOPIES; YELLOW FLUORESCENT PROTEINS;

LANTHANUM COMPOUNDS;

EPIDERMAL GROWTH FACTOR; FLUORESCENT DYE; KEIMA PROTEIN; MONOMERIC TEAL FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PROTEIN; PROTEIN TYROSINE KINASE; SUPER RESONANCE ENERGY ACCEPTING CHROMOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; BIOSENSOR; CELL MEMBRANE; CELL STIMULATION; CELL STRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELL; HUMAN; HUMAN CELL; MULTIPHOTON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TWO PHOTON EXCITATION MICROSCOPY;

EID: 79955469443     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2011.02.021     Document Type: Article

References (37)

1. E. Kiyokawa, K. Aoki, T. Nakamura, and M. Matsuda Spatiotemporal regulation of small GTPases as revealed by probes based on the principle of Förster resonance energy transfer (FRET): implications for signaling and pharmacology Annu. Rev. Pharmacol. Toxicol. 51 2010 337 358
2. E.A. Jares-Erijman, and T.M. Jovin Imaging molecular interactions in living cells by FRET microscopy Curr. Opin. Chem. Biol. 10 2006 409 416 (Pubitemid 44375073)
3. 2+ by circularly permuted yellow fluorescent proteins Proc. Natl. Acad. Sci. USA 101 2004 10554 10559 (Pubitemid 38955780)
4. M. Ouyang, J. Sun, S. Chien, and Y. Wang Determination of hierarchical relationship of Src and Rac at subcellular locations with FRET biosensors Proc. Natl. Acad. Sci. USA 105 2008 14353 14358
5. H.W. Ai, K.L. Hazelwood, M.W. Davidson, and R.E. Campbell Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors Nat. Methods 5 2008 401 403 (Pubitemid 351619097)
6. K. Aoki, and M. Matsuda Visualization of small GTPase activity with fluorescence resonance energy transfer-based biosensors Nat. Protoc. 4 2009 1623 1631
7. T. Okada, M.J. Miller, I. Parker, M.F. Krummel, M. Neighbors, S.B. Hartley, A. O'Garra, M.D. Cahalan, and J.G. Cyster Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells PLoS Biol. 3 2005 e150
8. C.D. Allen, T. Okada, H.L. Tang, and J.G. Cyster Imaging of germinal center selection events during affinity maturation Science 315 2007 528 531 (Pubitemid 46175759)
9. I. Majoul, M. Straub, R. Duden, S.W. Hell, and H.D. Soling Fluorescence resonance energy transfer analysis of protein-protein interactions in single living cells by multifocal multiphoton microscopy J. Biotechnol. 82 2002 267 277 (Pubitemid 34179605)
10. W.R. Zipfel, R.M. Williams, and W.W. Webb Nonlinear magic: multiphoton microscopy in the biosciences Nat. Biotechnol. 21 2003 1369 1377 (Pubitemid 37356624)
11. R. Yasuda Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy Curr. Opin. Neurobiol. 16 2009 551 561 (Pubitemid 44466401)
12. S. Ganesan, S.M. Ameer-Beg, T.T. Ng, B. Vojnovic, and F.S. Wouters A dark yellow fluorescent protein (YFP)-based resonance energy-accepting chromoprotein (REACh) for Forster resonance energy transfer with GFP Proc. Natl. Acad. Sci. USA 103 2006 4089 4094
13. T. Kogure, S. Karasawa, T. Araki, K. Saito, M. Kinjo, and A. Miyawaki A fluorescent variant of a protein from the stony coral Montipora facilitates dual-color single-laser fluorescence cross-correlation spectroscopy Nat. Biotechnol. 24 2006 577 581
14. A.L. Szymczak, C.J. Workman, Y. Wang, K.M. Vignali, S. Dilioglou, E.F. Vanin, and D.A. Vignali Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector Nat. Biotechnol. 22 2004 589 594 (Pubitemid 38585911)
15. N. Mochizuki, S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda Spatio-temporal images of growth-factor-induced activation of Ras and Rap1 Nature 411 2001 1065 1068 (Pubitemid 32612332)
16. M. Sato, Y. Ueda, T. Takagi, and Y. Umezawa Production of PtdInsP3 at endomembranes is triggered by receptor endocytosis Nat. Cell Biol. 5 2003 1016 1022 (Pubitemid 37406916)
17. H. Murakoshi, S.J. Lee, and R. Yasuda Highly sensitive and quantitative FRET-FLIM imaging in single dendritic spines using improved non-radiative YFP Brain Cell Biol. 36 2008 31 42
18. H. Ai, J.N. Henderson, S.J. Remington, and R.E. Campbell Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging Biochem. J. 400 2006 531 540 (Pubitemid 44974465)
19. T. Akagi, T. Shishido, K. Murata, and H. Hanafusa v-Crk activates the phosphoinositide 3-kinase/AKT pathway in transformation Proc. Natl. Acad. Sci. USA 97 2000 7290 7295 (Pubitemid 30431456)
20. K. Kurokawa, N. Mochizuki, Y. Ohba, H. Mizuno, A. Miyawaki, and M. Matsuda A pair of fluorescent resonance energy transfer-based probes for tyrosine phosphorylation of the CrkII adaptor protein in vivo J. Biol. Chem. 276 2001 31305 31310 (Pubitemid 37385001)
21. H. Yoshizaki, Y. Ohba, K. Kurokawa, R.E. Itoh, T. Nakamura, N. Mochizuki, K. Nagashima, and M. Matsuda Activity of Rho-family GTPases during cell division as visualized with FRET-based probes J. Cell Biol. 162 2003 223 232 (Pubitemid 36928836)
22. F. Martin-Belmonte, A. Gassama, A. Datta, W. Yu, U. Rescher, V. Gerke, and K. Mostov PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42 Cell 128 2007 383 397 (Pubitemid 46123512)
23. A.L. Pollack, R.B. Runyan, and K.E. Mostov Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis Dev. Biol. 204 1998 64 79 (Pubitemid 28563865)
24. T. Nagai, K. Ibata, E.S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications Nat. Biotechnol. 20 2002 87 90 (Pubitemid 34044921)
25. K. Aoki, T. Nakamura, K. Fujikawa, and M. Matsuda Local phosphatidylinositol 3,4,5-trisphosphate accumulation recruits Vav2 and Vav3 to activate Rac1/Cdc42 and initiate neurite outgrowth in nerve growth factor-stimulated PC12 cells Mol. Biol. Cell 16 2005 2207 2217 (Pubitemid 40632206)
26. T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells Mol. Biol. Cell 19 2008 4213 4223
27. K. Aoki, T. Nakamura, T. Inoue, T. Meyer, and M. Matsuda An essential role for the SHIP2-dependent negative feedback loop in neuritogenesis of nerve growth factor-stimulated PC12 cells J. Cell Biol. 177 2007 817 827 (Pubitemid 46873088)
28. H.W. Ai, S. Olenych, P. Wong, M. Davidson, and R. Campbell Hue-shifted monomeric variants of Clavularia cyan fluorescent protein: identification of the molecular determinants of color and applications in fluorescence imaging BMC Biol. 6 2008 13
29. N.C. Shaner, P.A. Steinbach, and R.Y. Tsien A guide to choosing fluorescent proteins Nat. Methods 2 2005 905 909 (Pubitemid 43108726)
30. L.E. O'Brien, T.S. Jou, A.L. Pollack, Q. Zhang, S.H. Hansen, P. Yurchenco, and K.E. Mostov Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly Nat. Cell Biol. 3 2001 831 838 (Pubitemid 32842689)
31. P.S. Tsai, B. Friedman, A.I. Ifarraguerri, B.D. Thompson, V. Lev-Ram, C.B. Schaffer, Q. Xiong, R.Y. Tsien, J.A. Squier, and D. Kleinfeld All-optical histology using ultrashort laser pulses Neuron 39 2003 27 41 (Pubitemid 36830946)
32. H. Kawano, T. Kogure, Y. Abe, H. Mizuno, and A. Miyawaki Two-photon dual-color imaging using fluorescent proteins Nat. Methods 5 2008 373 374 (Pubitemid 351619086)
33. K.D. Piatkevich, J. Hulit, O.M. Subach, B. Wu, A. Abdulla, J.E. Segall, and V.V. Verkhusha Monomeric red fluorescent proteins with a large Stokes shift Proc. Natl. Acad. Sci. USA 107 2010 5369 5374
34. S.E. Tillo, T.E. Hughes, N.S. Makarov, A. Rebane, and M. Drobizhev A new approach to dual-color two-photon microscopy with fluorescent proteins BMC Biotechnol. 10 2010 6
35. S. Yoshiki, R. Matsunaga-Udagawa, K. Aoki, Y. Kamioka, E. Kiyokawa, and M. Matsuda Ras and calcium signaling pathways converge at Raf1 via the Shoc2 scaffold protein Mol. Biol. Cell 21 2010 1088 1096
36. E. Sahai, J. Wyckoff, U. Philippar, J.E. Segall, F. Gertler, and J. Condeelis Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy BMC Biotechnol. 5 2005 14
37. M.L. Craske, M. Fivaz, N.N. Batada, and T. Meyer Spines and neurite branches function as geometric attractors that enhance protein kinase C action J. Cell Biol. 170 2005 1147 1158 (Pubitemid 41362646)