Chromophore-protein interactions in the anthozoan green fluorescent protein asFP499

Biophysical Journal

Volumn 91, Issue 11, 2006, Pages 4210-4220

  Nienhaus, Karin ^a   Renzi, Fabiana ^b   Vallone, Beatrice ^b   Wiedenmann, Jörg ^a   Nienhaus, G Ulrich ^a,c  

^a UNIVERSITY OF ULM   (Germany)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT PROTEIN 499; STRUCTURAL PROTEIN;

ANEMONE; ANTHOZOA; ARTICLE; CHROMATOPHORE; FLUORESCENCE ANALYSIS; HYDROGEN BOND; NONHUMAN; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT;

ACTINIARIA; AEQUOREA VICTORIA; ANEMONIA SULCATA;

EID: 33751087146     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.087411     Document Type: Article

References (70)

1. Wiedenmann, J. Deutsches Patent- und Markenamt, assignee. 1997. Die Anwendung eines fluoreszierenden Proteins und weiterer farbiger Proteine und der zugehörigen Gene aus der Artengruppe Anemonia sp. (sulcata) Pennant, (Cnidaria, Anthozoa, Actinaria) in Gentechnologie und Molekularbiologie. Offenlegungsschrift DE 197 18 640 A1, Deutsches Patent- und Markenamt, 1-18.
2. Matz, M. V., A. F. Fradkov, Y. A. Labas, A. P. Savitsky, A. G. Zaraisky, M. L. Markelov, and S. A. Lukyanov. 1999. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17:969-973.
3. Wiedenmann, J., C. Elke, K. D. Spindler, and W. Funke. 2000. Cracks in the beta-can: fluorescent proteins from Anemonia sulcata (Anthozoa, Actinaria). Proc. Natl. Acad. Sci. USA. 97:14091-14096.
4. Shagin, D. A., E. V. Barsova, Y. G. Yanushevich, A. F. Fradkov, K. A. Lukyanov, Y. A. Labas, T. N. Semenova, J. A. Ugalde, A. Meyers, J. M. Nunez, E. A. Widder, S. A. Lukyanov, and M. V. Matz. 2004. GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. Mol. Biol. Evol. 21:841-850.
5. Dove, S. G., O. Hoegh-Guldberg, and S. Ranganathan. 2001. Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs. 19:197-204.
6. Ormö, M., A. B. Cubitt, K. Kallio, L. A. Gross, R. Y. Tsien, and S. J. Remington. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science. 273:1392-1395.
7. Yang, F., L. G. Moss, and G. N. Phillips Jr. 1996. The molecular structure of green fluorescent protein. Nat. Biotechnol. 14:1246-1251.
8. Prasher, D. C., V. K. Eckenrode, W. W. Ward, F. G. Prendergast, and M. J. Cormier. 1992. Primary structure of the Aequorea victoria green-fluorescent protein. Gene. 111:229-233.
9. Tsien, R. Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544.
10. Reid, B. G., and G. C. Flynn. 1997. Chromophore formation in green fluorescent protein. Biochemistry. 36:6786-6791.
11. Heim, R., D. C. Prasher, and R. Y. Tsien. 1994. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. USA. 91:12501-12504.
12. Waldo, G. S., B. M. Standish, J. Berendzen, and T. C. Terwilliger. 1999. Rapid protein-folding assay using green fluorescent protein. Nat. Biotechnol. 17:691-695.
13. Romoser, V. A., P. M. Hinkle, and A. Persechini. 1997. Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators. J. Biol. Chem. 272:13270-13274.
14. Kneen, M., J. Farinas, Y. Li, and A. S. Verkman. 1998. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J. 74:1591-1599.
15. Miyawaki, A., J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikura, and R. Y. Tsien. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature. 388:882-887.
16. Barondeau, D. P., C. J. Kassmann, J. A. Tainer, and E. D. Getzoff. 2002. Structural chemistry of a green fluorescent protein Zn biosensor. J. Am. Chem. Soc. 124:3522-3524.
17. Remington, S. J. 2000. Structural basis for understanding spectral variations in green fluorescent protein. Methods Enzymol. 305:196-211.
18. Palm, G. J., A. Zdanov, G. A. Gaitanaris, R. Stauber, G. N. Pavlakis, and A. Wlodawer. 1997. The structural basis for spectral variations in green fluorescent protein. Nat. Struct. Biol. 4:361-365.
19. Heim, R., A. B. Cubitt, and R. Y. Tsien. 1995. Improved green fluorescence. Nature. 373:663-664.
20. Yarbrough, D., R. M. Wachter, K. Kallio, M. V. Matz, and S. J. Remington. 2001. Refined crystal structure of DsRed, a red fluorescent protein from coral, at 2.0-Å resolution. Proc. Natl. Acad. Sci. USA. 98:462-467.
21. Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
22. Gross, L. A., G. S. Baird, R. C. Hoffman, K. K. Baldridge, and R. Y. Tsien. 2000. The structure of the chromophore within DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci. USA. 97:11990-11995.
23. Petersen, J., P. G. Wilmann, T. Beddoe, A. J. Oakley, R. J. Devenish, M. Prescott, and J. Rossjohn. 2003. The 2.0-Å crystal structure of eqFP611, a far red fluorescent protein from the sea anemone Entacmaea quadricolor. J. Biol. Chem. 278:44626-44631.
24. Nienhaus, K., B. Vallone, F. Renzi, J. Wiedenmann, and G. U. Nienhaus. 2003. Crystallization and preliminary x-ray diffraction analysis of the red fluorescent protein eqFP611. Acta Crystallogr. D. 59:1253-1255.
25. Ando, R., H. Hama, M. Yamamoto-Hino, H. Mizuno, and A. Miyawaki. 2002. An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:12651-12656.
26. Mizuno, H., T. K. Mal, K. I. Tong, R. Ando, T. Furuta, M. Ikura, and A. Miyawaki. 2003. Photo-induced peptide cleavage in the green-to-red conversion of a fluorescent protein. Mol. Cell. 12:1051-1058.
27. Wiedenmann, J., S. Ivanchenko, F. Oswald, F. Schmitt, C. Röcker, A. Salih, K. D. Spindler, and G. U. Nienhaus. 2004. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc. Natl. Acad. Sci. USA. 101:15905-15910.
28. Nienhaus, K., G. U. Nienhaus, J. Wiedenmann, and H. Nar. 2005. Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP. Proc. Natl. Acad. Sci. USA. 102:9156-9159.
29. Wiedenmann, J., and G. U. Nienhaus. 2006. Live-cell imaging with EosFP and other photoactivatable marker proteins of the GFP family. Expert Rev. Proteomics. 3:361-374.
30. Wiedenmann, J., B. Vallone, F. Renzi, K. Nienhaus, S. Ivanchenko, C. Röcker, and G. U. Nienhaus. 2005. Red fluorescent protein eqFP611 and its genetically engineered dimeric variants. J. Biomed. Opt. 10:14003.
31. Miyawaki, A., T. Nagai, and H. Mizuno. 2005. Engineering fluorescent proteins. Adv. Biochem. Eng. Biotechnol. 95:1-15.
32. Wang, Z., J. V. Shah, Z. Chen, C. H. Sun, and M. W. Berns. 2004. Fluorescence correlation spectroscopy investigation of a GFP mutant-enhanced cyan fluorescent protein and its tubulin fusion in living cells with two-photon excitation. J. Biomed. Opt. 9:395-403.
33. Ivanchenko, S., C. Röcker, F. Oswald, J. Wiedenmann, and G. U. Nienhaus. 2005. Targeted green-to-red photoconversion of EosFP, a fluorescent marker protein. J. Biol. Phys. 31:249-259.
34. Wiedenmann, J., S. Ivanchenko, F. Oswald, and G. U. Nienhaus. 2004. Identification of GFP-like proteins in nonbioluminescent, Azooxanthellate Anthozoa opens new perspectives for bioprospecting. Mar. Biotechnol. (NY). 6:270-277.
35. Otwinowski, Z., and W. Minor. 1997. Data collection and processing. Methods Enzymol. 276:307-326.
36. Bailey, S. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. 50:760-763.
37. QUANTA software. School of Crystallography, B. C., University of London, London, United Kingdom.
38. Emsley, P., and K. Kowtan. 2004. COOT version 0.026 model building and molecular graphics system. Acta Crystallogr. D. 70:2126-2132.
39. PyMOL version 0.97 Molecular Graphics System. DeLano Scientific, South San Francisco, CA.
40. Sniegowski, J. A., J. W. Lappe, H. N. Patel, H. A. Huffman, and R. M. Wachter. 2005. Base catalysis of chromophore formation in Arg96 and Glu222 variants of green fluorescent protein. J. Biol. Chem. 280:26248-26255.
41. Wood, T. I., D. P. Barondeau, C. Hitomi, C. J. Kassmann, J. A. Tainer, and E. D. Getzoff. 2005. Defining the role of arginine 96 in green fluorescent protein fluorophore biosynthesis. Biochemistry. 44:16211-16220.
42. Wachter, R. M., M. A. Elsliger, K. Kallio, G. T. Hanson, and S. J. Remington. 1998. Structural basis of spectral shifts in the yellow-emission variants of green fluorescent protein. Structure. 6:1267-1277.
43. Wiedenmann, J., A. Schenk, C. Röcker, A. Girod, K. D. Spindler, and G. U. Nienhaus. 2002. A far-red fluorescent protein with fast maturation and reduced oligomerization tendency from Entacmaea quadricolor (Anthozoa, Actinaria). Proc. Natl. Acad. Sci. USA. 99:11646-11651.
44. Nienhaus, G. U., K. Nienhaus, A. Hölzle, S. Ivanchenko, F. Renzi, F. Oswald, M. Wolff, F. Schmitt, C. Röcker, B. Vallone, W. Weidemann, R. Heilker, H. Nar, and J. Wiedenmann. 2005. Photoconvertible fluorescent protein EosFP-biophysical properties and cell biology applications. Photochem. Photobiol. 82:351-358.
45. Jung, G., J. Wiehler, and A. Zumbusch. 2005. The photophysics of green fluorescent protein: influence of the key amino acids at positions 65, 203, and 222. Biophys. J. 88:1932-1947.
46. Elsliger, M. A., R. M. Wachter, G. T. Hanson, K. Kallio, and S. J. Remington. 1999. Structural and spectral response of green fluorescent protein variants to changes in pH. Biochemistry. 38:5296-5301.
47. Chattoraj, M., B. A. King, G. U. Bublitz, and S. G. Boxer. 1996. Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. Proc. Natl. Acad. Sci. USA. 93:8362-8367.
48. Creemers, T. M. H., A. J. Lock, V. Subramaniam, T. M. Jovin, and S. Völker. 1999. Three photoconvertible forms of green fluorescent protein identified by spectral hole-burning. Nat. Struct. Biol. 6:557-560.
49. Ward, W. W., and S. H. Bokman. 1982. Reversible denaturation of Aequorea green-fluorescent protein: physical separation and characterization of the renatured protein. Biochemistry. 21:4535-4540.
50. Ward, W. W., H. J. Prentice, A. F. Roth, C. W. Cody, and S. C. Reeves. 1982. Spectral perturbations of the Aequorea green-fluorescent protein. Photochem. Photobiol. 35:803-808.
51. Weber, W., V. Helms, J. A. McCammon, and P. W. Langhoff. 1999. Shedding light on the dark and weakly fluorescent states of green fluorescent proteins. Proc. Natl. Acad. Sci. USA. 96:6177-6182.
52. Voityuk, A. A., M. E. Michel-Beyerle, and N. Rösch. 1998. Quantum chemical modeling of structure and absorption spectra of the chromophore in green fluorescent proteins. Chem. Phys. 231:13-25.
53. Cubitt, A. B., R. Heim, S. R. Adams, A. E. Boyd, L. A. Gross, and R. Y. Tsien. 1995. Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci. 20:448-455.
54. Zimmer, M. 2002. Green fluorescent protein (GFP): applications, structure, and related photophysical behavior. Chem. Rev. 102:759-781.
55. Wiehler, J., G. Jung, C. Seebacher, A. Zumbusch, and B. Steipe. 2003. Mutagenic stabilization of the photocycle intermediate of green fluorescent protein (GFP). ChemBioChem. 4:1164-1171.
56. Brejc, K., T. K. Sixma, P. A. Kitts, S. R. Kain, R. Y. Tsien, M. Ormo, and S. J. Remington. 1997. Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein. Proc. Natl. Acad. Sci. USA. 94:2306-2311.
57. Scharnagl, C., R. Raupp-Kossmann, and S. F. Fischer. 1999. Molecular basis for pH sensitivity and proton transfer in green fluorescent protein: protonation and conformational substates from electrostatic calculations. Biophys. J. 77:1839-1857.
58. Schellenberg, P., E. Johnson, A. P. Esposito, P. J. Reid, and W. W. Parson. 2001. Resonance Raman scattering by the green fluorescent protein and an analogue of its chromophore. J. Phys. Chem. B. 105:5316-5322.
59. He, X., A. F. Bell, and P. J. Tonge. 2002. Isotopic labeling and normal-mode analysis of a model green fluorescent protein chromophore. J. Phys. Chem. B. 106:6056-6066.
60. Gurskaya, N. G., A. P. Savitsky, Y. G. Yanushevich, S. A. Lukyanov, and K. A. Lukyanov. 2001. Color transitions in coral's fluorescent proteins by site-directed mutagenesis. BMC Biochem. 2:6.
61. Sinicropi, A., T. Andruniow, N. Ferre, R. Basosi, and M. Olivucci. 2005. Properties of the emitting state of the green fluorescent protein resolved at the CASPT2//CASSCF/CHARMM level. J. Am. Chem. Soc. 127:11534-11535.
62. Tozzini, V., and R. Nifosi. 2001. Ab initio molecular dynamics of the green fluorescent protein (GFP) chromophore: an insight into the photoinduced dynamics of green fluorescent proteins. J. Phys. Chem. B. 105:5797-5803.
63. Marques, M. A., X. Lopez, D. Varsano, A. Castro, and A. Rubio. 2003. Time-dependent density-functional approach for biological chromophores: the case of the green fluorescent protein. Phys. Rev. Lett. 90:258101.
64. Cinelli, R. A., V. Tozzini, V. Pellegrini, F. Beltram, G. Cerullo, M. Zavelani-Rossi, S. De Silvestri, M. Tyagi, and M. Giacca. 2001. Coherent dynamics of photoexcited green fluorescent proteins. Phys. Rev. Lett. 86:3439-3442.
65. Müller, J. D., B. H. McMahon, E. Y. Chien, S. G. Sligar, and G. U. Nienhaus. 1999. Connection between the taxonomic substates and protonation of histidines 64 and 97 in carbonmonoxy myoglobin. Biophys. J. 77:1036-1051.
66. Nienhaus, K., J. M. Kriegl, and G. U. Nienhaus. 2004. Structural dynamics in the active site of murine neuroglobin and its effects on ligand binding. J. Biol. Chem. 279:22944-22952.
67. Creemers, T. M. H., A. J. Lock, V. Subramaniam, T. M. Jovin, and S. Völker. 2000. Photophysics and optical switching in green fluorescent protein mutants. Proc. Natl. Acad. Sci. USA. 97:2974-2978.
68. Cotlet, M., J. Hofkens, M. Maus, T. Gensch, M. Van der Auweraer, J. Michiels, G. Dirix, M. Van Guyse, J. Vanderleyden, A. Visser, and F. C. De Schryver. 2001. Excited-state dynamics in the enhanced green fluorescent protein mutant probed by picosecond time-resolved single photon counting spectroscopy. J. Phys. Chem. B. 105:4999-5006.
69. Striker, G., V. Subramaniam, C. A. M. Seidel, and A. Volkmer. 1999. Photochromicity and fluorescence lifetimes of green fluorescent protein. J. Phys. Chem. B. 103:8612-8617.
70. Seebacher, C., F. W. Deeg, C. Brauchle, J. Wiehler, and B. Steipe. 1999. Stable low-temperature photoproducts and hole burning of green fluorescent protein (GFP). J. Phys. Chem. B. 103:7728-7732.