Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging

Nature Neuroscience

Volumn 9, Issue 2, 2006, Pages 283-291

  Yasuda, Ryohei ^a,d   Harvey, Christopher D ^a,b   Zhong, Haining ^a   Sobczyk, Aleksander ^a,c   Van Aelst, Linda ^b   Svoboda, Karel ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FLUORESCENT DYE; RAS PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; EMBRYO; ENZYME ACTIVATION; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; HUMAN; HUMAN CELL; NERVE CELL; NEUROIMAGING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; SUPERSENSITIVITY;

ANIMALS; CALCIUM; CELL LINE; DENDRITIC SPINES; DIAGNOSTIC IMAGING; ENZYME ACTIVATION; HIPPOCAMPUS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PHOTONS; RAS PROTEINS; RATS;

EID: 31544462618     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1635     Document Type: Article

References (50)

1. Kennedy, M.B., Beale, H.C., Carlisle, H.J. & Washburn, L.R. Integration of biochemical signalling in spines. Nat. Rev. Neurosci. 6, 423-434 (2005).
2. Thomas, G.M. & Huganir, R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5, 173-183 (2004).
3. Zhu, J.J., Qin, Y., Zhao, M., Van Aelst, L. & Malinow, R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110, 443-455 (2002).
4. Gallagher, S.M., Daly, C.A., Bear, M.F. & Huber, K.M. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J. Neurosci. 24, 4859-4864 (2004).
5. Wu, G.Y., Deisseroth, K. & Tsien, R.W. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat. Neurosci. 4, 151-158 (2001).
6. Lakowicz, J.R. Principles of Fluorescence Spectroscopy 2nd edn. (Plenum, New York, 1999).
7. Miyawaki, A. Visualization of the spatial and temporal dynamics of intracellular signaling. Dev. Cell 4, 295-305 (2003).
8. Mochizuki, N. et al. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068 (2001).
9. Rocks, O. et al. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752 (2005).
10. Wallrabe, H. & Periasamy, A. Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16, 19-27 (2005).
11. Gordon, G.W., Berry, G., Liang, X.H., Levine, B. & Herman, B. Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74, 2702-2713 (1998).
12. Denk, W. & Svoboda, K. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18, 351-357 (1997).
13. Piston, D.W., Sandison, D.R. & Webb, W.W. Time-resolved fluorescence imaging and background rejection by two-photon excitation in laser-scanning microscopy. in Time-Resolved Laser Spectroscopy in Biochemistry III (ed. Lakowicz, J.R.) 379-389 (SPIE, Seattle, 1992).
14. Gratton, E., Breusegem, S., Sutin, J., Ruan, Q. & Barry, N. Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods. J. Biomed. Opt. 8, 381-390 (2003).
15. Peter, M. et al. Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions. Biophys. J. 88, 1224-1237 (2005).
16. Pologruto, T.A., Sabatini, B.L. & Svoboda, K. ScanImage: flexible software for operating laser-scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
17. Nagai, T. et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90 (2002).
18. Rizzo, M.A., Springer, G.H., Granada, B. & Piston, D.W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449 (2004).
19. Erickson, M.G., Moon, D.L. & Yue, D.T. DsRed as a potential FRET partner with CFP and GFP. Biophys. J. 85, 599-611 (2003).
20. Zacharias, D.A., Violin, J.D., Newton, A.C. & Tsien, R.Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916 (2002).
21. de Rooij, J. & Bos, J.L. Minimal Ras-binding domain of Raf1 can be used as an activation-specific probe for Ras. Oncogene 14, 623-625 (1997).
22. Medema, R.H., de Vries-Smits, A.M., van der Zon, G.C., Maassen, J.A. & Bos, J.L. Ras activation by insulin and epidermal growth factor through enhanced exchange of guanine nucleotides on p21ras. Mol. Cell. Biol. 13, 155-162 (1993).
23. Herrmann, C., Martin, G.A. & Wittinghofer, A. Quantitative analysis of the complex between p21ras and the Ras-binding domain of the human Raf-1 protein kinase. J. Biol. Chem. 270, 2901-2905 (1995).
24. Feig, L.A. & Cooper, G.M. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8, 3235-3243 (1988).
25. McAllister, A.K. Biolistic transfection of neurons. Sci. STKE 2000, pl1 (2000).
26. Dolmetsch, R.E., Pajvani, U., Fife, K., Spotts, J.M. & Greenberg, M.E. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294, 333-339 (2001).
27. Jaitner, B.K. et al. Discrimination of amino acids mediating Ras binding from noninteracting residues affecting raf activation by double mutant analysis. J. Biol. Chem. 272, 29927-29933 (1997).
28. Callaway, J.C. & Ross, W.N. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 74, 1395-1403 (1995).
29. Maravall, M., Mainen, Z.M., Sabatini, B.L. & Svoboda, K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 78, 2655-2667 (2000).
30. Yasuda, R., Sabatini, B.L. & Svoboda, K. Plasticity of calcium channels in dendritic spines. Nat. Neurosci. 6, 948-955 (2003).
31. 2+ indicators. J. Neurosci. 24, 9572-9579 (2004).
32. Bi, G.Q. & Poo, M.M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464-10472 (1998).
33. Yasuda, R. et al. Imaging calcium concentration dynamics in small neuronal compartments. Sci. STKE 2004, pl5 (2004).
34. Farnsworth, C.L. et al. Calcium activation of Ras mediated by neuronal exchange factor Ras-GRF. Nature 376, 524-527 (1995).
35. Chen, H.J., Rojas-Soto, M., Oguni, A. & Kennedy, M.B. A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 20, 895-904 (1998).
36. Kim, J.H., Liao, D., Lau, L.F. & Huganir, R.L. SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20, 683-691 (1998).
37. Chiu, V.K. et al. Ras signalling on the endoplasmic reticulum and the Golgi. Nat. Cell Biol. 4, 343-350 (2002).
38. Goldbeter, A. & Koshland, D.E., Jr. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. USA 78, 6840-6844 (1981).
39. Ebinu, J.O. et al. RasGRP, a Ras guanyl nucleotide- releasing protein with calcium- and diacylglycerol-binding motifs. Science 280, 1082-1086 (1998).
40. 2+-dependent membrane-binding proteins. Evidence for a direct interaction between annexin VI and P120GAP. J. Biol. Chem. 271, 24333-24336 (1996).
41. 2+ oscillations. EMBO J. 23, 1749-1760 (2004).
42. 2+. J. Cell Biol. 170, 183-190 (2005).
43. Dudek, S.M. & Fields, R.D. Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proc. Natl. Acad. Sci. USA 99, 3962-3967 (2002).
44. Helton, T.D., Xu, W. & Lipscombe, D. Neuronal L-type calcium channels open quickly and are inhibited slowly. J. Neurosci. 25, 10247-10251 (2005).
45. Mermelstein, P.G., Bito, H., Deisseroth, K. & Tsien, R.W. Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. J. Neurosci. 20, 266-273 (2000).
46. Campbell, R.E. et al. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882 (2002).
47. Ohba, Y. et al. Rap2 as a slowly responding molecular switch in the Rap1 signaling cascade. Mol. Cell. Biol. 20, 6074-6083 (2000).
48. Bondeva, T., Balla, A., Varnal, P. & Balla, T. Structural determinants of Ras-Raf interaction analyzed in live cells. Mol. Biol. Cell 13, 2323-2333 (2002).
49. Shaner, N.C. et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. (2004).
50. Stoppini, L., Buchs, P.A. & Muller, D.A. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182 (1991).