Near-infrared fluorescent proteins engineered from bacterial phytochromes

Current Opinion in Chemical Biology

Volumn 27, Issue , 2015, Pages 52-63

  Shcherbakova, Daria M ^a   Baloban, Mikhail ^a   Verkhusha, Vladislav V ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

APOPROTEIN; BILIVERDIN; CYAN FLUORESCENT PROTEIN; FLUORESCENT DYE; HEME OXYGENASE; PHYTOCHROME; RED FLUORESCENT PROTEIN; TUMOR MARKER; BACTERIAL PROTEIN; PHOTOPROTEIN;

AMINO ACID SUBSTITUTION; AUTOFLUORESCENCE IMAGING; BASIC RESEARCH; BRIGHTNESS; CANCER DIAGNOSIS; CANCER GROWTH; CANCER LOCALIZATION; CANCER RECURRENCE; CANCER REGRESSION; CANCER STAGING; CELL METABOLISM; CELL POPULATION; CELL PROLIFERATION; CELL SPECIFICITY; CHROMATOPHORE; COMPUTER ASSISTED TOMOGRAPHY; CONCENTRATION (PARAMETERS); CONFORMATION; COVALENT BOND; ECHO PLANAR IMAGING; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE; HIGH THROUGHPUT SCREENING; HISTOLOGY; ILLUMINATION; IMAGE QUALITY; IMAGE RECONSTRUCTION; IN VITRO STUDY; INFRARED RADIATION; LIGHT ABSORPTION; LIGHT SCATTERING; METASTASIS; MOLECULAR STABILITY; NONHUMAN; OPTICAL TOMOGRAPHY; PHENOTYPE; PHOTOACOUSTIC TOMOGRAPHY; PHOTOACOUSTICS; PHOTOACTIVATION; PHOTOCHEMISTRY; PHOTORECEPTOR; POSITRON EMISSION TOMOGRAPHY; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN-FRAGMENT COMPLEMENTATION ASSAY; QUANTUM YIELD; REVIEW; SIGNAL TRANSDUCTION; STEM CELL RESEARCH; SURFACE PROPERTY; TRANSLATIONAL RESEARCH; WHOLE BODY IMAGING; ANIMAL; CHEMISTRY; DIAGNOSTIC IMAGING; GENETICS; NEAR INFRARED SPECTROSCOPY; PROCEDURES;

ANIMALIA; BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIAL PROTEINS; DIAGNOSTIC IMAGING; LUMINESCENT PROTEINS; PHYTOCHROME; PROTEIN ENGINEERING; SPECTROSCOPY, NEAR-INFRARED; WHOLE BODY IMAGING;

EID: 84935005822     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.06.005     Document Type: Review

References (50)

1. Weissleder R. A clearer vision for in vivo imaging. Nat Biotechnol 2001, 19:316-317.
2. Morozova K.S., Piatkevich K.D., Gould T.J., et al. Far-red fluorescent protein excitable with red lasers for flow cytometry and superresolution STED nanoscopy. Biophys J 2010, 99:L13-L15.
3. Piatkevich K.D., Malashkevich V.N., Morozova K.S., et al. Extended Stokes shift in fluorescent proteins: chromophore-protein interactions in a near-infrared TagRFP675 variant. Sci Rep 2013, 3:1847.
4. Subach O.M., Patterson G.H., Ting L.M., et al. A photoswitchable orange-to-far-red fluorescent protein, PSmOrange. Nat Methods 2011, 8:771-777.
5. Shcherbakova D.M., Verkhusha V.V. Chromophore chemistry of fluorescent proteins controlled by light. Curr Opin Chem Biol 2014, 20:60-68.
6. Rockwell N.C., Lagarias J.C. A brief history of phytochromes. Chemphyschem 2010, 11:1172-1180.
7. Fischer A.J., Lagarias J.C. Harnessing phytochrome's glowing potential. Proc Natl Acad Sci U S A 2004, 101:17334-17339.
8. Giraud E., Vermeglio A. Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth Res 2008, 97:141-153.
9. Karniol B., Wagner J.R., Walker J.M., Vierstra R.D. Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem J 2005, 392:103-116.
10. Auldridge M.E., Forest K.T. Bacterial phytochromes: more than meets the light. Crit Rev Biochem Mol Biol 2011, 46:67-88.
11. Kapitulnik J., Maines M.D. The role of bile pigments in health and disease: effects on cell signaling, cytotoxicity, and cytoprotection. Front Pharmacol 2012, 3:136.
12. Piatkevich K.D., Subach F.V., Verkhusha V.V. Engineering of bacterial phytochromes for near-infrared imaging, sensing, and light-control in mammals. Chem Soc Rev 2013, 42:3441-3452.
13. Shcherbakova D.M., Verkhusha V.V. Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat Methods 2013, 10:751-754.
14. Yu D., Gustafson W.C., Han C., et al. An improved monomeric infrared fluorescent protein for neuronal and tumour brain imaging. Nat Commun 2014, 5:3626.
15. Bhattacharya S., Auldridge M.E., Lehtivuori H., et al. Origins of fluorescence in evolved bacteriophytochromes. J Biol Chem 2014, 289:32144-32152.
16. Auldridge M.E., Satyshur K.A., Anstrom D.M., Forest K.T. Structure-guided engineering enhances a phytochrome-based infrared fluorescent protein. J Biol Chem 2012, 287:7000-7009.
17. Filonov G.S., Piatkevich K.D., Ting L.M., et al. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat Biotechnol 2011, 29:757-761.
18. Shu X., Royant A., Lin M.Z., et al. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 2009, 324:804-807.
19. Piatkevich K.D., Subach F.V., Verkhusha V.V. Far-red light photoactivatable near-infrared fluorescent proteins engineered from a bacterial phytochrome. Nat Commun 2013, 4:2153.
20. Filonov G.S., Verkhusha V.V. A near-infrared BiFC reporter for in vivo imaging of protein-protein interactions. Chem Biol 2013, 20:1078-1086.
21. Tchekanda E., Sivanesan D., Michnick S.W. An infrared reporter to detect spatiotemporal dynamics of protein-protein interactions. Nat Methods 2014, 11:641-644.
22. Pandey N., Nobles C.L., Zechiedrich L., et al. Combining random gene fission and rational gene fusion to discover near-infrared fluorescent protein fragments that report on protein-protein interactions. ACS Synth Biol 2015, 4:615-624.
23. Chen M., Li W., Zhang Z., et al. Novel near-infrared BiFC systems from a bacterial phytochrome for imaging protein interactions and drug evaluation under physiological conditions. Biomaterials 2015, 48:97-107.
24. Stepanenko O.V., Bublikov G.S., Shcherbakova D.M., et al. A knot in the protein structure-probing the near-infrared fluorescent protein iRFP designed from a bacterial phytochrome. FEBS J 2014, 281:2284-2298.
25. Yang X., Kuk J., Moffat K. Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction. Proc Natl Acad Sci U S A 2008, 105:14715-14720.
26. Takala H., Bjorling A., Berntsson O., et al. Signal amplification and transduction in phytochrome photosensors. Nature 2014, 509:245-248.
27. Wagner J.R., Zhang J., von Stetten D., et al. Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes. J Biol Chem 2008, 283:12212-12226.
28. Lehtivuori H., Rissanen I., Takala H., et al. Fluorescence properties of the chromophore-binding domain of bacteriophytochrome from Deinococcus radiodurans. J Phys Chem B 2013, 117:11049-11057.
29. Bansal S., Biswas G., Avadhani N.G. Mitochondria-targeted heme oxygenase-1 induces oxidative stress and mitochondrial dysfunction in macrophages, kidney fibroblasts and in chronic alcohol hepatotoxicity. Redox Biol 2014, 2:273-283.
30. Jozkowicz A., Was H., Dulak J. Heme oxygenase-1 in tumors: is it a false friend?. Antioxid Redox Signal 2007, 9:2099-2117.
31. Lu Y., Darne C.D., Tan I.C., et al. In vivo imaging of orthotopic prostate cancer with far-red gene reporter fluorescence tomography and in vivo and ex vivo validation. J Biomed Opt 2013, 18:101305.
32. Jiguet-Jiglaire C., Cayol M., Mathieu S., et al. Noninvasive near-infrared fluorescent protein-based imaging of tumor progression and metastases in deep organs and intraosseous tissues. J Biomed Opt 2014, 19:16019.
33. Agollah G.D., Wu G., Sevick-Muraca E.M., Kwon S. In vivo lymphatic imaging of a human inflammatory breast cancer model. J Cancer 2014, 5:774-783.
34. Zhu B.H., Wu G., Robinson H., et al. Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP. Mol Imaging Biol 2013, 15:560-568.
35. Nedosekin D.A., Sarimollaoglu M., Galanzha E.I., et al. Synergy of photoacoustic and fluorescence flow cytometry of circulating cells with negative and positive contrasts. J Biophotonics 2013, 6:425-434.
36. Condeelis J., Weissleder R. In vivo imaging in cancer. Cold Spring Harbor Perspect Biol 2010, 2:a003848.
37. Wang Y., Zhou M., Wang X., et al. Assessing in vitro stem-cell function and tracking engraftment of stem cells in ischaemic hearts by using novel iRFP gene labelling. J Cell Mol Med 2014, 18:1889-1894.
38. Tran M.T., Tanaka J., Hamada M., et al. In vivo image analysis using iRFP transgenic mice. Exp Anim/Jap Assoc Lab Anim Sci 2014, 63:311-319.
39. Fyk-Kolodziej B., Hellmer C.B., Ichinose T. Marking cells with infrared fluorescent proteins to preserve photoresponsiveness in the retina. BioTechniques 2014, 57:245-253.
40. Calvo-Alvarez E., Stamatakis K., Punzon C., et al. Infrared fluorescent imaging as a potent tool for in vitro, ex vivo and in vivo models of visceral leishmaniasis. PLoS Negl Trop Dis 2015, 9:e0003666.
41. Kuhar R., Gwiazda K.S., Humbert O., et al. Novel fluorescent genome editing reporters for monitoring DNA repair pathway utilization at endonuclease-induced breaks. Nucleic Acids Res 2014, 42:e4.
42. Sanders T.A., Llagostera E., Barna M. Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning. Nature 2013, 497:628-632.
43. Stuker F., Ripoll J., Rudin M. Fluorescence molecular tomography: principles and potential for pharmaceutical research. Pharmaceutics 2011, 3:229-274.
44. James M.L., Gambhir S.S. A molecular imaging primer: modalities, imaging agents, and applications. Physiol Rev 2012, 92:897-965.
45. Deliolanis N.C., Ale A., Morscher S., et al. Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview. Mol Imaging Biol 2014, 16:652-660.
46. Rice W.L., Shcherbakova D.M., Verkhusha V.V., Kumar A.T. In vivo tomographic imaging of deep-seated cancer using fluorescence lifetime contrast. Cancer Res 2015, 75:1236-1243.
47. Wang L.V., Hu S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science 2012, 335:1458-1462.
48. Filonov G.S., Krumholz A., Xia J., et al. Deep-tissue photoacoustic tomography of a genetically encoded near-infrared fluorescent probe. Angew Chem Int Ed Engl 2012, 51:1448-1451.
49. Krumholz A., Shcherbakova D.M., Xia J., et al. Multicontrast photoacoustic in vivo imaging using near-infrared fluorescent proteins. Sci Rep 2014, 4:3939.
50. Tzoumas S., Nunes A., Deliolanis N.C., Ntziachristos V. Effects of multispectral excitation on the sensitivity of molecular optoacoustic imaging. J Biophotonics 2014, 9999.