Non-invasive intravital imaging of cellular differentiation with a bright red-excitable fluorescent protein

Nature Methods

Volumn 11, Issue 5, 2014, Pages 572-578

  Chu, Jun ^a,b   Haynes, Russell D ^b   Corbel, Stéphane Y ^b   Li, Pengpeng ^c   González González, Emilio ^b   Burg, John S ^b   Ataie, Niloufar J ^d   Lam, Amy J ^a,b   Cranfill, Paula J ^e,f   Baird, Michelle A ^e,f   Davidson, Michael W ^e,f   Ng, Ho Leung ^d,g   Garcia, K Christopher ^b,c   Contag, Christopher H ^b   Shen, Kang ^c   Blau, Helen M ^b   Lin, Michael Z ^a,b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF HAWAII   (United States)

^e FLORIDA STATE UNIVERSITY   (United States)

^f FLORIDA STATE UNIVERSITY   (United States)

^g UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RED FLUORESCENT PROTEIN;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL REGENERATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; EXCITATION; FLUORESCENCE IMAGING; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; MUSCLE CELL; MUTAGENESIS; MYOBLAST; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTICS; PRIORITY JOURNAL; PROTEIN STRUCTURE; RED LIGHT; REDUCTION;

ANIMALIA; MUS;

ANIMALS; CELL DIFFERENTIATION; CRYSTALLOGRAPHY, X-RAY; DIAGNOSTIC IMAGING; GENE LIBRARY; HELA CELLS; HEMOGLOBINS; HUMANS; HYDROGEN BONDING; LUMINESCENT PROTEINS; MALE; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUSCLE CELLS; MUSCLE, SKELETAL; MUSCLES; MUTAGENESIS; MYOBLASTS; MYOGLOBIN; NIH 3T3 CELLS; REGENERATION; STEM CELLS;

EID: 84899897163     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2888     Document Type: Article

References (43)

1. Schenkman, K.A., Marble, D.R., Feigl, E.O. & Burns, D.H. Near-infrared spectroscopic measurement of myoglobin oxygen saturation in the presence of hemoglobin using partial least-squares analysis. Appl. Spectrosc. 53, 325-331 (1999).
2. Tromberg, B.J. et al. Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy. Neoplasia 2, 26-40 (2000).
3. Monici, M. Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 11, 227-256 (2005).
4. Deliolanis, N.C. et al. In vivo tomographic imaging of red-shifted fluorescent proteins. Biomed. Opt. Express 2, 887-900 (2011).
5. Kawai, Y., Sato, M. & Umezawa, Y. Single color fluorescent indicators of protein phosphorylation for multicolor imaging of intracellular signal flow dynamics. Anal. Chem. 76, 6144-6149 (2004).
6. Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498 (2008).
7. Lin, M.Z. et al. Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals. Chem. Biol. 16, 1169-1179 (2009).
8. Morozova, K.S. et al. Far-red fluorescent protein excitable with red lasers for flow cytometry and superresolution STED nanoscopy. Biophys. J. 99, L13-L15 (2010).
9. Shcherbo, D. et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem. J. 418, 567-574 (2009).
10. Subach, O.M. et al. A photoswitchable orange-to-far-red fluorescent protein, PSmOrange. Nat. Methods 8, 771-777 (2011).
11. Shu, X. et al. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324, 804-807 (2009).
12. Lin, M.Z. Beyond the rainbow: new fluorescent proteins brighten the infrared scene. Nat. Methods 8, 726-728 (2011).
13. Filonov, G.S. et al. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat. Biotechnol. 29, 757-761 (2011).
14. Shcherbo, D. et al. Near-infrared fluorescent proteins. Nat. Methods 7, 827-829 (2010).
15. Jeffrey, G.A. An Introduction to Hydrogen Bonding (Oxford University Press, New York, 1997).
16. Rice, B.W., Cable, M.D. & Nelson, M.B. In vivo imaging of light-emitting probes. J. Biomed. Opt. 6, 432-440 (2001).
17. Gilbert, P.M. & Blau, H.M. Engineering a stem cell house into a home. Stem Cell Res. Ther. 2, 3 (2011).
18. Schroeder, T. Imaging stem-cell-driven regeneration in mammals. Nature 453, 345-351 (2008).
19. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S. & Blau, H.M. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506 (2008).
20. Contag, C.H. & Bachmann, M.H. Advances in in vivo bioluminescence imaging of gene expression. Annu. Rev. Biomed. Eng. 4, 235-260 (2002).
21. Lam, A.J. et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012 (2012).
22. Condeelis, J. & Weissleder, R. In vivo imaging in cancer. Cold Spring Harb. Perspect. Biol. 2, a003848 (2010).
23. Harms, G.S., Cognet, L., Lommerse, P.H., Blab, G.A. & Schmidt, T. Autofluorescent proteins in single-molecule research: applications to live cell imaging microscopy. Biophys. J. 80, 2396-2408 (2001).
24. Shinde, R., Perkins, J. & Contag, C.H. Luciferin derivatives for enhanced in vitro and in vivo bioluminescence assays. Biochemistry 45, 11103-11112 (2006).
25. Inoue, Y., Kiryu, S., Watanabe, M., Tojo, A. & Ohtomo, K. Timing of imaging after d-luciferin injection affects the longitudinal assessment of tumor growth using in vivo bioluminescence imaging. Int. J. Biomed. Imaging 2010, 471408 (2010).
26. Brunk, U.T. & Terman, A. Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic. Biol. Med. 33, 611-619 (2002).
27. Eldred, G.E. & Katz, M.L. Fluorophores of the human retinal pigment epithelium: separation and spectral characterization. Exp. Eye Res. 47, 71-86 (1988).
28. Murdaugh, L.S. et al. Compositional studies of human RPE lipofuscin. J. Mass Spectrom. 45, 1139-1147 (2010).
29. Nighswander-Rempel, S.P., Kupriyanov, V.V. & Shaw, R.A. Relative contributions of hemoglobin and myoglobin to near-infrared spectroscopic images of cardiac tissue. Appl. Spectrosc. 59, 190-193 (2005).
30. Chalfie, M. & Kain, S.R. Green Fluorescent Protein: Properties, Applications, and Protocols 2nd edn. (Wiley, 2006).
31. Shaner, N.C., Steinbach, P.A. & Tsien, R.Y. A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909 (2005).
32. Walter, T.S. et al. Lysine methylation as a routine rescue strategy for protein crystallization. Structure 14, 1617-1622 (2006).
33. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
34. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
35. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
36. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
37. Pražnikar, J., Afonine, P.V., Guncar, G., Adams, P.D. & Turk, D. Averaged kick maps: less noise, more signal and probably less bias. Acta Crystallogr. D Biol. Crystallogr. 65, 921-931 (2009).
38. Bass, R.B., Strop, P., Barclay, M. & Rees, D.C. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298, 1582-1587 (2002).
39. Vagin, A. & Teplyakov, A. Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25 (2010).
40. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
41. Mello, C.C., Kramer, J.M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970 (1991).
42. Kerr, R. et al. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26, 583-594 (2000).
43. National Research Council (US) Committee on Guidelines for the Use of Animals in Neuroscience and Behavioral Research. Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research (National Academies Press, 2003).