Molecular Basis of Spectral Diversity in Near-Infrared Phytochrome-Based Fluorescent Proteins

Chemistry and Biology

Volumn 22, Issue 11, 2015, Pages 1540-1551

  Shcherbakova, Daria M ^a   Baloban, Mikhail ^a   Pletnev, Sergei ^b   Malashkevich, Vladimir N ^a   Xiao, Hui ^a   Dauter, Zbigniew ^b   Verkhusha, Vladislav V ^a,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANILINE; FLUORESCENT DYE; MUTANT PROTEIN; PHYTOCHROME; BACTERIAL PROTEIN; CYSTEINE; PHOTOPROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CHROMATOPHORE; DEINOCOCCUS RADIODURANS; FILM; FLOW CYTOMETRY; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; HUMAN; HYDROGEN BOND; ISOMERIZATION; NEAR INFRARED SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; CONFOCAL MICROSCOPY; GENETICS; HELA CELL LINE; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTAGENESIS; PROTEIN TERTIARY STRUCTURE; RHODOPSEUDOMONAS; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; BACTERIAL PROTEINS; CYSTEINE; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHYTOCHROME; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RHODOPSEUDOMONAS; SEQUENCE ALIGNMENT; SPECTROSCOPY, NEAR-INFRARED;

EID: 84947915622     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.10.007     Document Type: Article

References (50)

1. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D. Biol. Crystallogr. 58 2002 1948 1954
2. P.V. Afonine, N.W. Moriarty, M. Mustyakimov, O.V. Sobolev, T.C. Terwilliger, D. Turk, A. Urzhumtsev, and P.D. Adams FEM: feature-enhanced map Acta Crystallogr. D. Biol. Crystallogr. 71 2015 646 666
3. M.E. Auldridge, and K.T. Forest Bacterial phytochromes: more than meets the light Crit. Rev. Biochem. Mol. Biol. 46 2011 67 88
4. M.E. Auldridge, K.A. Satyshur, D.M. Anstrom, and K.T. Forest Structure-guided engineering enhances a phytochrome-based infrared fluorescent protein J. Biol. Chem. 287 2012 7000 7009
5. D. Bellini, and M.Z. Papiz Structure of a bacteriophytochrome and light-stimulated protomer swapping with a gene repressor Structure 20 2012 1436 1446
6. S. Bhattacharya, M.E. Auldridge, H. Lehtivuori, J.A. Ihalainen, and K.T. Forest Origins of fluorescence in evolved bacteriophytochromes J. Biol. Chem. 289 2014 32144 32152
7. S.H. Bhoo, S.J. Davis, J. Walker, B. Karniol, and R.D. Vierstra Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore Nature 414 2001 776 779
8. B. Borucki, S. Seibeck, M.P. Heyn, and T. Lamparter Characterization of the covalent and noncovalent adducts of Agp1 phytochrome assembled with biliverdin and phycocyanobilin by circular dichroism and flash photolysis Biochemistry 48 2009 6305 6317
9. E.S. Burgie, A.N. Bussell, J.M. Walker, K. Dubiel, and R.D. Vierstra Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome Proc. Natl. Acad. Sci. USA 111 2014 10179 10184
10. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D. Biol. Crystallogr. 60 2004 2126 2132
11. L.O. Essen, J. Mailliet, and J. Hughes The structure of a complete phytochrome sensory module in the Pr ground state Proc. Natl. Acad. Sci. USA 105 2008 14709 14714
12. G.S. Filonov, and V.V. Verkhusha A near-infrared BiFC reporter for in vivo imaging of protein-protein interactions Chem. Biol. 20 2013 1078 1086
13. G.S. Filonov, K.D. Piatkevich, L.M. Ting, J. Zhang, K. Kim, and V.V. Verkhusha Bright and stable near-infrared fluorescent protein for in vivo imaging Nat. Biotechnol. 29 2011 757 761
14. A.J. Fischer, and J.C. Lagarias Harnessing phytochrome's glowing potential Proc. Natl. Acad. Sci. USA 101 2004 17334 17339
15. A.J. Fischer, N.C. Rockwell, A.Y. Jang, L.A. Ernst, A.S. Waggoner, Y. Duan, H. Lei, and J.C. Lagarias Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes Biochemistry 44 2005 15203 15215
16. S. Franzen, and S.G. Boxer On the origin of heme absorption band shifts and associated protein structural relaxation in myoglobin following flash photolysis J. Biol. Chem. 272 1997 9655 9660
17. G.A. Gambetta, and J.C. Lagarias Genetic engineering of phytochrome biosynthesis in bacteria Proc. Natl. Acad. Sci. USA 98 2001 10566 10571
18. E. Giraud, and A. Vermeglio Bacteriophytochromes in anoxygenic photosynthetic bacteria Photosynth. Res. 97 2008 141 153
19. C. Jiguet-Jiglaire, M. Cayol, S. Mathieu, C. Jeanneau, C. Bouvier-Labit, L. Ouafik, and A. El-Battari Noninvasive near-infrared fluorescent protein-based imaging of tumor progression and metastases in deep organs and intraosseous tissues J. Biomed. Opt. 19 2014 16019
20. J. Kapitulnik, and M.D. Maines The role of bile pigments in health and disease: effects on cell signaling, cytotoxicity, and cytoprotection Front. Pharmacol. 3 2012 136
21. B. Karniol, J.R. Wagner, J.M. Walker, and R.D. Vierstra Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors Biochem. J. 392 2005 103 116
22. T. Lamparter, N. Michael, O. Caspani, T. Miyata, K. Shirai, and K. Inomata Biliverdin binds covalently to agrobacterium phytochrome Agp1 via its ring A vinyl side chain J. Biol. Chem. 278 2003 33786 33792
23. T. Lamparter, M. Carrascal, N. Michael, E. Martinez, G. Rottwinkel, and J. Abian The biliverdin chromophore binds covalently to a conserved cysteine residue in the N-terminus of Agrobacterium phytochrome Agp1 Biochemistry 43 2004 3659 3669
24. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
25. M.Z. Lin, M.R. McKeown, H.L. Ng, T.A. Aguilera, N.C. Shaner, R.E. Campbell, S.R. Adams, L.A. Gross, W. Ma, T. Alber, and et al. Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals Chem. Biol. 16 2009 1169 1179
26. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D. Biol. Crystallogr. 67 2011 355 367
27. W. Otwinowski, and F. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
28. K.D. Piatkevich, F.V. Subach, and V.V. Verkhusha Engineering of bacterial phytochromes for near-infrared imaging, sensing, and light-control in mammals Chem. Soc. Rev. 42 2013 3441 3452
29. K.D. Piatkevich, F.V. Subach, and V.V. Verkhusha Far-red light photoactivatable near-infrared fluorescent proteins engineered from a bacterial phytochrome Nat. Commun. 4 2013 2153
30. B. Quest, and W. Gartner Chromophore selectivity in bacterial phytochromes: dissecting the process of chromophore attachment Eur. J. Biochem. 271 2004 1117 1126
31. N.C. Rockwell, and J.C. Lagarias A brief history of phytochromes Chemphyschem 11 2010 1172 1180
32. T.A. Sanders, E. Llagostera, and M. Barna Specialized filopodia direct long-range transport of SHH during vertebrate tissue patterning Nature 497 2013 628 632
33. R. Sens, and K.H. Drexhage Fluorescence quantum yield of oxazine and carbazine laser dyes J. Lumin. 24 1981 709 712
34. D.M. Shcherbakova, and V.V. Verkhusha Near-infrared fluorescent proteins for multicolor in vivo imaging Nat. Methods 10 2013 751 754
35. D.M. Shcherbakova, M. Baloban, and V.V. Verkhusha Near-infrared fluorescent proteins engineered from bacterial phytochromes Curr. Opin. Chem. Biol. 27 2015 52 63
36. X. Shu, A. Royant, M.Z. Lin, T.A. Aguilera, V. Lev-Ram, P.A. Steinbach, and R.Y. Tsien Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome Science 324 2009 804 807
37. H. Takala, A. Bjorling, O. Berntsson, H. Lehtivuori, S. Niebling, M. Hoernke, I. Kosheleva, R. Henning, A. Menzel, J.A. Ihalainen, and et al. Signal amplification and transduction in phytochrome photosensors Nature 509 2014 245 248
38. K.C. Toh, E.A. Stojkovic, I.H. van Stokkum, K. Moffat, and J.T. Kennis Fluorescence quantum yield and photochemistry of bacteriophytochrome constructs Phys. Chem. Chem. Phys. 13 2011 11985 11997
39. M.T. Tran, J. Tanaka, M. Hamada, Y. Sugiyama, S. Sakaguchi, M. Nakamura, S. Takahashi, and Y. Miwa In vivo image analysis using iRFP transgenic mice Exp. Anim. 63 2014 311 319
40. A. Vagin, and A. Teplyakov Molecular replacement with MOLREP Acta Crystallogr. D. Biol. Crystallogr. 66 2010 22 25
41. J.R. Wagner, J.S. Brunzelle, K.T. Forest, and R.D. Vierstra A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome Nature 438 2005 325 331
42. J.R. Wagner, J. Zhang, J.S. Brunzelle, R.D. Vierstra, and K.T. Forest High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution J. Biol. Chem. 282 2007 12298 12309
43. J.R. Wagner, J. Zhang, D. von Stetten, M. Gunther, D.H. Murgida, M.A. Mroginski, J.M. Walker, K.T. Forest, P. Hildebrandt, and R.D. Vierstra Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes J. Biol. Chem. 283 2008 12212 12226
44. R. Weissleder A clearer vision for in vivo imaging Nat. Biotechnol. 19 2001 316 317
45. S.H. Wu, and J.C. Lagarias Defining the bilin lyase domain: lessons from the extended phytochrome superfamily Biochemistry 39 2000 13487 13495
46. X. Yang, J. Kuk, and K. Moffat Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction Proc. Natl. Acad. Sci. USA 105 2008 14715 14720
47. X. Yang, J. Kuk, and K. Moffat Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome Proc. Natl. Acad. Sci. USA 106 2009 15639 15644
48. D. Yu, W.C. Gustafson, C. Han, C. Lafaye, M. Noirclerc-Savoye, W.P. Ge, D.A. Thayer, H. Huang, T.B. Kornberg, A. Royant, and et al. An improved monomeric infrared fluorescent protein for neuronal and tumour brain imaging Nat. Commun. 5 2014 3626
49. D. Yu, M.A. Baird, J.R. Allen, E.S. Howe, M.P. Klassen, A. Reade, K. Makhijani, Y. Song, S. Liu, Z. Murthy, and et al. A naturally monomeric infrared fluorescent protein for protein labeling in vivo Nat. Methods 12 2015 763 765
50. B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M.A. Hall, S.C. Ghosh, K.L. Pinkston, A. Azhdarinia, B.R. Harvey, and E.M. Sevick-Muraca Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP Mol. Imaging Biol. 15 2013 560 568