Green fluorescent protein: A perspective

Protein Science

Volumn 20, Issue 9, 2011, Pages 1509-1519

  Remington, S James ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Chromophore; Crystallography; Excited state proton transfer; Fluorescence spectroscopy; Photochemistry; Protein structure

Indexed keywords

CHROMOPROTEIN; GREEN FLUORESCENT PROTEIN; POLYPEPTIDE; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

BIOSENSOR; FLUORESCENCE; NONHUMAN; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTON TRANSPORT; REVIEW;

ANIMALS; BIOSENSING TECHNIQUES; FLUORESCENCE; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS;

ANIMALIA; ANTHOZOA;

EID: 84860390150     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.684     Document Type: Review

References (90)

1. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. (1994) Green fluorescent protein as a marker for gene expression. Science 263:802805.
2. Yang F., Moss L.G., Phillips G.N.J. (1996) The molecular structure of green fluorescent protein. Nature Biotech 14:1246-1251. (Pubitemid 26332784)
3. Ormo M., Cubitt A.B., Kallio K., Gross L.A., Tsien R.Y., Remington S.J. (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273:1392-1395. (Pubitemid 26296528)
4. Tsien R.Y. (1998) The green fluorescent protein. Annu Rev Biochem 67:509-544.
5. Ghosh I., Hamilton A.D., Regan L. (2000) Antiparallel leucine zipper-directed protein reassembly: Application to the green fluorescent protein. J Am Chem Soc 122: 5658-5659. (Pubitemid 30431094)
6. Kent K.P., ChildsW., Boxer S.G. (2008) Deconstructing green fluorescent protein. J Am Chem Soc 130:9664-9665.
7. Baird G.S., Zacharias D.A., Tsien R.Y. (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci USA 96: 11241-11246. (Pubitemid 29487365)
8. Topell S., Hennecke J., Glockshuber R. (1999) Circularly permuted variants of the green fluorescent protein. FEBS Lett 457:283-289. (Pubitemid 29401943)
9. Zimmer M. (2002) Green fluorescent protein (GFP): Applications, structure and related photophysical behavior. Chem Rev 102:759-781.
10. Remington S.J. (2006) Fluorescent proteins: Maturation, photochemistry and photophysics. Curr Opin Struct Biol 16:714-721.
11. Bokman S.H., Ward W.W. (1981) Renaturation of Aequorea green-fluorescent protein. Biochem Biophys Res Commun 101:1372-1380.
12. McCapra F., Razavi Z., Neary A.P. (1988) The fluorescence of the chromophore of the green fluorescent protein of Aequorea and Renilla. J Chem Soc Chem Commun 12:790-791.
13. Cody C.W., Prasher D.C., Westler W.M., Prendergast F.G., Ward W.W. (1993) Chemical structure of the hexapeptide chromophore of the Aequorea green-fluorescent protein. Biochemistry 32:1212-1218. (Pubitemid 23070642)
14. Petersen J., Wilmann P.G., Beddoe T., Oakley A.J., Devenish R.J., Prescott M., Rossjohn J. (2003) The 2.0A crystal structure of eqFP611, a far-red fluorescent protein from the sea anemone Entacmaea quadricolor. J Biol Chem 278:44626-44631. (Pubitemid 37377217)
15. Weber W., Helms V., McCammon J.A., Langhoff P.W. (1999) Shedding light on the dark and weakly fluorescent states of green fluorescent proteins. Proc Natl Acad Sci U S A 96:6177-6182. (Pubitemid 29256639)
16. Heim R., Prasher D.C., Tsien R.Y. (1994) Wavelength mutations and postranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci USA 91: 12501-12504.
17. Kummer A.D., Kompa C., Lossau H., Pollinger-Dammer F., Michel-Beyerle M.E., Silva C.M., Bylina E.J., Coleman W.J., Yang M.M., Youvan D.C. (1998) Dramatic reduction in fluorescence quantum yield in mutants of green fluorescent protein due to fast internal conversion. Chem Phys 237:183-193.
18. Megley C.M., Dickson L.A., Maddalo S.L., Chandler G.J., Zimmer M. (2009) Photophysics and dihedral freedom of the chromophore in yellow, blue, and green fluorescent protein. J Phys Chem B 113:302-308.
19. Wachter R.M. (2007) Chromogenic cross-link Formation in green fluorescent protein. Acc Chem Res 40:120-127.
20. Wachter R.M., Watkins J.L., Kim H. (2010) Mechanistic diversity of red fluorescence acquisition by GFP-like proteins. Biochemistry 49:7417-7427.
21. Ward W.W., Prentice H.J., Roth A.F., Cody C.W., Reeves S.C. (1982) Spectral perturbations of the Aequorea greenfluorescent protein. Photochem Photobiol 35:803-808.
22. Patterson G.H., Lippincott-Schwartz J. (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-1877. (Pubitemid 35024347)
23. Henderson J.N., Gepshtein R., Heenan J.R., Kallio K., Huppert D., Remington S.J. (2009) Structure and mechanism of the photoactivatable green fluorescent protein. J Am Chem Soc 131:4176-4177.
24. Hasegawa J., Ise T., Fujimoto K.J., Kikuchi A., Fukumura E., Miyawaki A., Shiro Y. (2010) Excited states of fluorescent proteins, mKO and DsRed: Chromophore-protein electrostatic interaction behind the color variations. J Phys Chem B 114:2971-2979.
25. Chattoraj M., King B.A., Bublitz G.U., Boxer S.G. (1996) Ultra-fast excited state dynamics in green fluorescent protein: Multiple states and proton transfer. Proc Natl Acad Sci USA 93:8362-8367. (Pubitemid 26269563)
26. Bent D.V., Hayon E. (1975) Excited state chemistry of aromatic amino acids and related peptides. I. Tyrosine. J Am Chem Soc 97:2599-2606.
27. Tolbert L.M., Solntsev K.M. (2002) Excited-state proton transfer: From constrained systems to "super" photoacids to superfast proton transfer. Acc Chem Res 35: 19-27.
28. Kennis J.T., Larsen D.S., Van Stokkum I.H., Vengris M., Van Thor J.J., Van Grondelle R. (2004) Uncovering the hidden ground state of green fluorescent protein. Proc Natl Acad Sci U S A 101:17988-17993. (Pubitemid 40054062)
29. Van Thor J.J., Ronayne K.L., Towrie M., Sage J.T. (2008) Balance between ultrafast parallel reactions in the green fluorescent protein has a structural origin. Biophys J 95:1902-1912.
30. Stoner-Ma D., Jaye A.A., Matousek P., Towrie M., Meech S.R., Tonge P.J. (2005) Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy. J Am Chem Soc 127: 2864-2865. (Pubitemid 40349859)
31. Lossau H., Kummer A., Heinecke R., Poellinger-Dammer F., Kompa C., Bieser G., Jonsson T., Silva C.M., Yang M.M., Youvan D.C., Michel-Beyerle M.E. (1996) Time-resolved spectroscopy of wild-type and mutant Green Fluorescent Proteins reveals excited state deprotonation consistent with fluorophore-protein interactions. Chem Phys 213:1-16.
32. Agmon N. (2005) Proton pathways in green fluorescence protein. Biophys J 88:2452-2461.
33. Brejc K., Sixma T.K., Kitts P.A., Kain S.R., Tsien R.Y., Ormo M., Remington,S.J. (1997) Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein. Proc Natl Acad Sci USA 94: 2306-2311. (Pubitemid 27136870)
34. Shu X., Leiderman P., Gepshtein R., Smith N.R., Kallio K., Huppert D., Remington S.J. (2007) An alternative excited-state proton transfer pathway in green fluorescent protein variant S205V. Protein Sci 16:2703-2710. (Pubitemid 350172756)
35. Stoner-Ma D., Jaye A.A., Ronayne K.L., Nappa J., Meech S.R., Tonge P.J. (2008) An alternate proton acceptor for excited-state proton transfer in green fluorescent protein: Rewiring GFP. J Am Chem Soc 130:1227-1235. (Pubitemid 351171001)
36. Palmer A.E., Qin Y., Park J.G., McCombs J.E. (2011) Design and application of genetically encoded biosensors. Trends Biotechnol 29:144-152.
37. Grynkiewicz G., Martin P., Tsien R.Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450. (Pubitemid 15114340)
38. Miesenbock G., De Angelis D.A., Rothman J.E. (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195. (Pubitemid 28325974)
39. Hanson G.T., MCananey T.B., Park E.S., Rendell M., Yarbrough D.K., Chu S., Xi L., Boxer S.G., Montrose M.H., Remington S.J. (2002) Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminary application. Biochemistry 41:15477-15488. (Pubitemid 36062453)
40. McAnaney T.B., Park E.S., Hanson G.T., Remington S.J., Boxer S.G. (2002) Green fluorescent protein variants as ratiometric dual emission pH sensors. 2. Excited-state dynamics. Biochemistry 41:15489-15495.
41. McAnaney T.B., Shi X., Abbyad P., Jung H., Remington S.J., Boxer S.G. (2005) Green fluorescent protein variants as ratiometric dual emission pH sensors: 3. Temperature dependence of proton transfer. Biochemistry 44: 8701-8711. (Pubitemid 40840436)
42. Mank M., Griesbeck O. (2008) Genetically encoded calcium indicators. Chem Rev 108:1550-1564. (Pubitemid 351796397)
43. Ostergaard H., Henriksen A., Hansen F.G., Winther J.R. (2001) Shedding light on disulfide bond formation: Engineering a redox switch in green fluorescent protein. EMBO J 20:5853-5862. (Pubitemid 33049261)
44. Hanson G.T., Aggeler R., Oglesbee D., Canon M., Capaldi R.A., Tsien R.Y., Remington S.J. (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279: 13044-13053. (Pubitemid 38445882)
45. Lohman J.R., Remington S.J. (2008) Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry 47:8678-8688.
46. Cannon M.B., Remington S.J. (2008) Redox-sensitive green fluorescent protein: Probes for intracellular redox responses. A review. Methods Mol Biol 476:51-65.
47. Meyers A., Dick T.P. (2010) Genetically encoded redox probes. Antioxidants Redox Signal 13:1-30.
48. Wachter R., King B.A., Heim R., Kallio K., Tsien R.Y., Boxer S.G., Remington S.J. (1997) Crystal structure and photodynamic behavior of the blue emission variant Y66H/Y145F of green fluorescent protein. Biochemistry 36:9759-9765. (Pubitemid 27364686)
49. Matz M.V., Arkady F.F., Labas Y.A., Savitsky A.P., Zaraisky A.G., Markelov M.L., Lukyanov S.A. (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nature Biotech 17:969-973. (Pubitemid 29474851)
50. Alieva N.O., Konzen K.A., Field S.F., Meleshkevitch E.A., Hunt M.E., Beltran-Ramirez V., Miller D.J., Wiedenmann J., Salih A., Matz M.V. (2008) Diversity and evolution of coral fluorescent proteins. PLoS One 3:e2680.
51. Hopf M., Gohring W., Ries A., Timpl R., Hohenester E. (2001) Crystal structure and mutational analysis of a perlecan-binding fragment of nidogen-1. Nat Struct Biol 8:573-574.
52. Lukyanov K.A., Fradkov A.F., Gurskaya N.G., Matz M.V., Labas Y.A., Savitsky A.P., Markelov M.L., Zaraisky A.G., Zhao X., Fang Y., Tan W., Lukyanov S.A. (2000) Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog. J Biol Chem 275:25879-25882.
53. Salih A., Larkum A., Cox G., Kuehl M., Hoegh-Guldberg O. (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850-853. (Pubitemid 32016093)
54. Baird G.S., Zacharias D.A., Tsien R.Y. (2000) Biochemistry, mutagenesis and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA 97: 11984-11989.
55. Zhou J., Lin J., Zhou C., Deng X., Xia B. (2011) Cytotoxicity of red fluorescent protein DsRed is associated with the suppression of Bcl-xL translation. FEBS Lett 585: 821-827.
56. Dixit R., Cyr R. (2003) Cell damage and reactive oxygen species production induced by fluorescence microscopy: Effect on mitosis and guidelines for non-invasive fluorescence microscopy. Plant J 36:280-290. (Pubitemid 37293067)
57. Bulina M.E., Chudakov D.M., Britanova O.V., Yanushevich Y.G., Staroverov D.B., Chepurnykh T.V., Merzlyak E.M., Shkrob M.A., Lukyanov S., Lukyanov K.A. (2006) A genetically encoded photosensitizer. Nat Biotechnol 24: 95-99. (Pubitemid 43083172)
58. Gross L.A., Baird G.S., Hoffman R.C., Baldridge K.K., Tsien R.Y. (2000) The structure of the chromophore within DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA 87:11990-11995.
59. He X., Bell A.F., Tonge P.J. (2002) Synthesis and spectroscopic studies of model red fluorescent protein chromophores. Org Lett 9:1523-1526.
60. Remington S.J., Wachter R.M., Yarbrough D.K., Branchaud B., Anderson D.C., Kallio K., Lukyanov K.A. (2005) zFP538, a yellow fluorescent protein from Zoanthus, contains a novel three-ring chromophore. Biochemistry 44:202-212. (Pubitemid 40095722)
61. Pletneva N.V., Pletnev SV, MCD, VTT, Popov VO, Martynov VI, Wlodawer A, Dauter Z, Pletnev VZ (2007) Three-dimensional structure of yellow fluorescent protein zYFP538 from Zoanthus sp. at the resolution 1.8 angstrom. Bioorg Khim 33:421-430.
62. Subach O.M., Malashkevich V.N., Zencheck WD, SMK, Piatkevich KD, CAS, Verkhusha VV (2010) Structural characterization of acylimine-containing blue and red chromophores in mTagBFP and TagRFP fluorescent proteins. Chem Biol 17:333-341.
63. Strack R.L., Strongin D.E., Mets L., Glick B.S., Keenan R.J. (2010) Chromophore formation in DsRed occurs by a branched pathway. J Am Chem Soc 132:8496-8505.
64. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., Tsien R.Y. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99: 7877-7882. (Pubitemid 34650973)
65. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nature Biotechnol 22:1567-1572. (Pubitemid 40039460)
66. Wang L., Jackson W.C., Steinbach P.A., Tsien R.Y. (2004) Evolution of new nonantibody proteins via iterative somatic hypermutation. Proc Natl Acad Sci U S A 101: 16745-16749. (Pubitemid 39601309)
67. Shu X., Shaner N.C., Yarbrough C.A., Tsien R.Y., Remington S.J. (2006) Structural basis for spectral variations in mFruits: Monomeric orange and red fluorescent proteins. Biochemistry 45:9639-9647.
68. Kikuchi A., Fukumura E., Karasawa S., Mizuno H., Miyawaki A., Shiro Y. (2008) Structural characterization of a thiazoline-containing chromophore in an orange fluorescent protein, monomeric Kusabira Orange. Biochemistry 47:11573-11580.
69. Ai H.W., Henderson J.N., Remington S.J., Campbell R.E. (2006) Directed evolution of a monomeric, bright, and photostable version of Clavularia cyan fluorescent protein: Structural characterization and applications in fluorescence imaging. Biochem J 400: 531-540. (Pubitemid 44974465)
70. Nienhaus G.U., Nienhaus K., Holzle A., Ivanchenko S., Renzi F., Oswald F., Wolff M., Schmitt F., Rocker C., Vallone B., Weidemann W., Heilker R., Nar H., Wiedenmann J. (2006) Photoconvertible fluorescent protein EosFP: Biophysical properties and cell biology applications. Photochem Photobiol 82:351-358.
71. Kogure T., Karasawa S., Arkai T., Saito K., Kinjo M., Miyawaki A. (2006) A fluorescent variant of a protein from the stony coral Montipora facilitates dual-color single-laser fluorescence cross-correlation spectroscopy. Nature Biotechnol 24:577-581.
72. Henderson J.N., Osborne M.F., Koon N., Gepshtein R., Huppert D., Remington S.J. (2009) Excited State Proton Transfer in the Red Fluorescent Protein mKeima. J Am Chem Soc 131:13212-13213.
73. Shaner N.C., Steinbach P.A., Tsien R.Y. (2005) A guide to choosing fluorescent proteins. Nat Methods 2:905-909. (Pubitemid 43108726)
74. Dove S., Takabayashi M., Hoegh-Guldberg O. (1995) Isolation and characterization of the pink and blue pigments of Pocilloporid and Acroporid corals. Biol Bull 189:288-297.
75. Prescott M., Ling M., Beddoe T., Oakley A.J., Hoegh-Guldberg O., Devenish R.J., Rossjohn J. (2003) The 2.2 A crystal structure of a pocilloporin pigment reveals a nonplanar chromophore conformation. Structure 11: 275-284. (Pubitemid 36287692)
76. Wilmann P.G., Petersen J., Dvenish R.J., Prescott M., Rossjohn J. (2005) A polypeptide fragmentation within the chromophore revealed in the 2.1 A crystal structure of a nonfluorescent chromoprotein from anemonia sulcata. J Biol Chem 280:2401-2404. (Pubitemid 40189337)
77. Quillin M.L., Anstrom D.M., Shu X., O'Leary S., Kallio K., Lukyanov K.A., Remington S.J. (2005) The kindling fluorescent protein from Anemonia sulcata: Dark state structure at 1.38 Angstroms resolution. Biochemistry 44:5774-5787. (Pubitemid 40525114)
78. Gepshtein R., Huppert D., Agmon N. (2006) Deactivation mechanism of the green fluorescent chromophore. J Phys Chem B 110:4434-4442.
79. Yampolsky I.V., Remington S.J., Martynov V.I., Potapov V.K., Lukyanov S., Lukyanov K.A. (2005) Synthesisand properties of the chromophore of asFP595 chromoprotein from Anemonia sulcata. Biochemistry 44: 5788-5793. (Pubitemid 40525115)
80. Chudakov D.M., Belousov V.V., Zaraisky A.G., Novoselov V.V., Staroverov D.B., Zorov D.B., Lukyanov S., Lukyanov K.A. (2003) Kindling fluorescent proteins for precise in vivo photolabeling. Nature Biotech 21:191-194. (Pubitemid 36188220)
81. Chudakov D.M., Foefanov A.V., Mudrik N.N., Lukyanov S., Lukyanov K.A. (2003) Chromophore environment provides clue to "kindling fluorescent protein" riddle. J Biol Chem 278:7215-7219. (Pubitemid 36800721)
82. Stiel A.C., Trowitzsch S., Weber G., Andresen M., Eggeling C., Hell S.W., Jakobs S., Wahl M.C. (2007) 1.8 A bright-state structure of a reversibly photoswitchable fluorescent protein Dronpa guides the generation of fast switching mutants. Biochem J 402:35-42.
83. Wilmann P.G., Turcic K., Battad J.M., Wilce M.C., Devenish R.J., Prescott M., Rossjohn J. (2006) The 1.7 A crystal structure of Dronpa: A photoswitchable green fluorescent protein. J Mol Biol 364:213-224. (Pubitemid 44649252)
84. Andresen M., Stiel A.C., Trowitzsch S., Weber G., Eggeling C., Wahl M.C., Hell S.W., Jakobs S. (2007) Structural basis for reversible photoswitching in Dronpa. Proc Natl Acad Sci U S A 104:13005-13009. (Pubitemid 351737583)
85. Henderson J.N., Ai H.W., Campbell R.E., Remington S.J. (2007) Structural basis for reversible photobleaching in a green fluorescent protein homologue. Proc Natl Acad Sci U S A 104:6672-6677. (Pubitemid 47175559)
86. Ando R., Mizuno H., Miyawaki A. (2004) Regulated fast nucleoplasmic shuttling observed by reversible protein highlighting. Science 306:1370-1373. (Pubitemid 39532513)
87. Chudakov D.M., Verkhusha V.V., Staroverov D.B., Souslova E.A., Lukyanov S., Lukyanov K.A. (2004) Photoswitchable cyan fluorescent protein for protein tracking. Nature Biotechnol 22:1435-1439. (Pubitemid 39482864)
88. Hofmann M., Eggeling C., Jakobs S., Hell S.W. (2005) Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci U S A 102: 17565-17569. (Pubitemid 41803537)
89. Betzig E., Patterson G.H., Sougrat R., Lindwasser O.W., Olenych S., Bonifacino J.S., Davidson M.W., Lippincott-Schwartz J., Hess H.F. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645. (Pubitemid 44414039)
90. Dickson R.M., Cubitt A.B., Tsien R.Y., Moerner W.E. (1997) On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388:356-358.