New statistical methods enhance imaging of cameleon fluorescence resonance energy transfer in cultured zebrafish spinal neurons

Journal of Biomedical Optics

Volumn 12, Issue 3, 2007, Pages

  Fan, Xiang ^a   Majumder, Anirban ^a   Reagin, Sean S ^a   Porter, Erika L ^a   Sornborger, Andrew T ^a,b   Keith, Charles H ^a,b   Lauderdale, James D ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b Faculty of Engineering   (United States)

Author keywords

Calcium; Confocal microscopy; Ratiometry; Zebrafish

Indexed keywords

CONFOCAL MICROSCOPY; ENERGY TRANSFER; FLUORESCENCE; OPTIMIZATION; STATISTICAL METHODS;

CAMELEON; FLUORESCENCE RESONANCE ENERGY TRANSFER; NEURAL ACTIVITY; RATIOMETRY; ZEBRAFISH SPINAL NEURONS;

NEURONS;

ANIMALIA; CAENORHABDITIS ELEGANS; DANIO RERIO; VERTEBRATA;

CALCIUM; CALCIUM BINDING PROTEIN; FLUORESCENT DYE; HYBRID PROTEIN;

ALGORITHM; ANIMAL; ARTICLE; CALCIUM SIGNALING; CELL CULTURE; CYTOLOGY; EVALUATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HISTOLOGY; METABOLISM; METHODOLOGY; NERVE CELL; PHYSIOLOGY; STATISTICAL ANALYSIS; ZEBRA FISH;

ALGORITHMS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; DATA INTERPRETATION, STATISTICAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; NEURONS; RECOMBINANT FUSION PROTEINS; ZEBRAFISH;

EID: 34547859982     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.2745263     Document Type: Article

References (45)

1. A. Takahashi et al., "Measurement of intracellular calcium", Physiol. Rev. 79(4), 1089-1125 (1999). (Pubitemid 29473312)
2. J. Zhang et al., "Creating new fluorescent probes for cell biology", Nat. Rev. Mol. Cell Biol. 3(12), 906-918 (2002). (Pubitemid 35477369)
3. A. Miyawaki, "Innovations in the imaging of brain functions using fluorescent proteins", Neuron 48(2), 189-199 (2005). (Pubitemid 41476353)
4. A. Miyawaki et al., "Development of genetically encoded fluorescent indicators for calcium", Methods Enzymol. 360, 202-225 (2003). (Pubitemid 36207266)
5. G. Miesenböck, "Genetic methods for illuminating the function of neural circuits", Curr. Opin. Neurobiol. 14(3), 395-402 (2004). (Pubitemid 38759872)
6. G. Miesenböck and I. G. Kevrekidis, "Optical imaging and control of genetically designated neurons in functioning circuits", Annu. Rev. Neurosci. 28, 533-563 (2005). (Pubitemid 41098914)
7. S. Higashijima et al., "Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator", J. Neurophysiol. 90(6), 3986-3997 (2003). (Pubitemid 37541929)
8. A. Miyawaki et al., "Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin", Nature (London) 388(6645), 882-887 (1997). (Pubitemid 27377061)
9. R. Y. Tsien, "The green fluorescent protein", Annu. Rev. Biochem. 67, 509-544 (1998). (Pubitemid 28411137)
10. G. H. Patterson, D. W. Piston, and B. G. Barisas, "Forster distances between green fluorescent protein pairs", Anal. Biochem. 284(2), 438-440 (2000).
11. S. Habuchi et al., "Resonance energy transfer in a calcium concentration-dependent cameleon protein", Biophys. J. 83(6), 3499-3506 (2002). (Pubitemid 36041966)
12. K. Truong et al., "FRET-based in vivo Ca2+ imaging by a new calmodulin-GFP fusion molecule", Nat. Struct. Biol. 8(12), 1069-1073 (2001). (Pubitemid 33101629)
13. T. Nagai et al., "Expanded dynamic range of fluorescent indicators for Ca (2+) by circularly permuted yellow fluorescent proteins", Proc. Natl. Acad. Sci. U. S. A. 101(29), 10554-10559 (2004). (Pubitemid 38955780)
14. D. F. Reiff et al., "In vivo performance of genetically encoded indicators of neural activity in flies", J. Neurosci. 25(19), 4766-4778 (2005). (Pubitemid 40664125)
15. G. Guerrero et al., "Heterogeneity in synaptic transmission along a Drosophila larval motor axon", Nat. Neurosci. 8(9), 1188-1196 (2005). (Pubitemid 43348137)
16. H. Suzuki et al., "In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation", Neuron 39(6), 1005-1017 (2003). (Pubitemid 37130215)
17. A. Miyawaki, "Visualization of the spatial and temporal dynamics of intracellular signaling", Dev. Cell 4(3), 295-305 (2003). (Pubitemid 36342356)
18. A. Miyawaki et al., "Dynamic and quantitative Ca2+ measurements using improved cameleons", Proc. Natl. Acad. Sci. U. S. A. 96(5), 2135-2140 (1999). (Pubitemid 29117880)
19. A. E. Palmer et al., "Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor", Proc. Natl. Acad. Sci. U. S. A. 101(50), 17404-17409 (2004). (Pubitemid 39657417)
20. N. Heim and O. Griesbeck, "Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein", J. Biol. Chem. 279(14), 14280-14286 (2004). (Pubitemid 38468968)
21. M. T. Hasan et al., "Functional fluorescent Ca2+ indicator proteins in transgenic mice under TET control", PLoS Biol. 2(6), 763-775 (2004).
22. T. Nagai et al., "Circularly permuted green fluorescent proteins engineered to sense Ca2+", Proc. Natl. Acad. Sci. U. S. A. 98(6), 3197-3202 (2001). (Pubitemid 32220822)
23. J. Nakai, M. Ohkura, and K. Imoto, "A high signal-to-noise Ca (2+) probe composed of a single green fluorescent protein", Nat. Biotechnol. 19(2), 137-141 (2001). (Pubitemid 32144441)
24. O. Griesbeck et al., "Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications", J. Biol. Chem. 276(31), 29188-29194 (2001).
25. T. A. Pologruto, R. Yasuda, and K. Svoboda, "Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators", J. Neurosci. 24(43), 9572-9579 (2004). (Pubitemid 39441511)
26. J. Li et al., "Early development of functional spatial maps in the zebrafish olfactory bulb", J. Neurosci. 25(24), 5784-5795 (2005). (Pubitemid 40847891)
27. J. Broder et al., "Estimating weak ratiometric signals in imaging data I: Dual-channel data", J. Opt. Soc. Am. A (in press).
28. M. Westerfield, Ed., The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4 ed., University of Oregon Press, Eugene (2000).
29. C. B. Kimmel et al., "Stages of embryonic development of the zebrafish", Dev. Dyn. 203(3), 253-310 (1995).
30. S. S. Andersen, "Preparation of dissociated zebrafish spinal neuron cultures", Methods Cell. Sci. 23(4), 205-209 (2001). (Pubitemid 34863293)
31. J. Hanks, "Hanks' balanced salt solution and pH control", Tissue Culture Association Manual, Vol. 3, pp. 3-15 (1976).
32. H. C. Park et al., "Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons", Dev. Biol. 227(2), 279-293 (2000).
33. G. Piperno and M. T. Fuller, "Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms", J. Cell Biol. 101, 2085-2094 (1985). (Pubitemid 16169938)
34. R. R. Bernhardt et al., "Identification of spinal neurons in the embryonic and larval zebrafish", J. Comp. Neurol. 302(3), 603-616 (1990).
35. A. B. Chitnis and J. Y. Kuwada, "Axonogenesis in the brain of zebrafish embryos", J. Neurosci. 10(6), 1892-1905 (1990).
36. J. D. Lauderdale, N. M. Davis, and J. Y. Kuwada, "Axon tracts correlate with netrin-1a expression in the zebrafish embryo", Mol. Cell. Neurosci. 9(4), 293-313 (1997). (Pubitemid 27349480)
37. D. W. Raible et al., "Segregation and early dispersal of neural crest cells in the embryonic zebrafish", Dev. Dyn. 195(1), 29-42 (1992). (Pubitemid 23034182)
38. P. Lipp and E. Niggli, "Ratiometric confocal Ca (2+)-measurements with visible wavelength indicators in isolated cardiac myocytes", Cell Calcium 14(5), 359-372 (1993). (Pubitemid 23162142)
39. J. Bischofberger and D. Schild, "Different spatial patterns of [Ca2 +] increase caused by N- and L-type Ca2+ channel activation in frog olfactory bulb neurones", J. Physiol. (London) 487(2), 305-317 (1995).
40. T. M. Gomez et al., "Filopodial calcium transients promote substratedependent growth cone turning", Science 291(5510), 1983-1987 (2001). (Pubitemid 32217001)
41. R. J. Miller, "Multiple calcium channels and neuronal function", Science 235(4784), 46-52 (1987). (Pubitemid 17229268)
42. R. W. Tsien et al., "Multiple types of neuronal calcium channels and their selective modulation", Trends Neurosci. 11(10), 431-438 (1988).
43. R. J. Miller, "Calcium signalling in neurons", Trends Neurosci. 11(10), 415-419 (1988).
44. A. Miyawaki, T. Nagai, and H. Mizuno, "Engineering fluorescent proteins", Adv. Biochem. Eng./Biotechnol. 95, 1-15 (2005). (Pubitemid 44617136)
45. P. S. Tsai et al., "All-optical histology using ultrashort laser pulses", Neuron 39(1), 27-41 (2003). (Pubitemid 36830946)