Russian Journal of Bioorganic Chemistry

, Volume 33, Issue 4, pp 390–398 | Cite as

Three-dimensional structure of yellow fluorescent protein zYFP538 from Zoanthus sp. at the resolution 1.8 Å

  • N. V. Pletneva
  • S. V. Pletnev
  • D. M. Chudakov
  • T. V. Tikhonova
  • V. O. Popov
  • V. I. Martynov
  • A. Wlodawer
  • Z. Dauter
  • V. Z. Pletnev
Article

Abstract

The three-dimensional structure of yellow fluorescent proteins zYFP538 (zFP538) from the button polyp Zoanthus sp. was determined at a resolution of 1.8 Å by X-ray analysis. The monomer of zYFP538 adopts a structure characteristic of the green fluorescent protein (GFP) family, a β-barrel formed from 11 antiparallel β segments and one internal α helix with a chromophore embedded into it. Like the TurboGFP, the β-barrel of zYFP538 contains a water-filled pore leading to the chromophore Tyr67 residue, which presumably provides access of molecular oxygen necessary for the maturation process. The post-translational modification of the chromophore-forming triad Lys66-Tyr67-Gly68 results in a tricyclic structure consisting of a five-membered imidazolinone ring, a phenol ring of the Tyr67 residue, and an additional six-membered tetrahydropyridine ring. The chromophore formation is completed by cleavage of the protein backbone at the C α -N bond of Lys66. It was suggested that the energy conflict between the buried positive charge of the intact Lys66 side chain in the hydrophobic pocket formed by the Ile44, Leu46, Phe65, Leu204 and Leu219 side chains is the most probable trigger that induces the transformation of the bicyclic green form to the tricyclic yellow form. A stereochemical analysis of the contacting surfaces at the intratetramer interfaces helped reveal a group of conserved key residues responsible for the oligomerization. Along with others, these residues should be taken into account in designing monomeric forms suitable for practical application as markers of proteins and cell organelles.

Key words

GFP-like proteins crystal structure chromophore structure tetramer structure intersubunit interfaces yellow fluorescent protein Zoanthus sp. 

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References

  1. 1.
    Chalfie, M. and Kain, S., GFP Green Fluorescent Protein. Properties, Applications and Protocols, New York: Wiley-Liss, 1998.Google Scholar
  2. 2.
    Tsien, R.Y., Annu. Rev. Biochem., 1998, vol. 67, pp. 509–544.PubMedCrossRefGoogle Scholar
  3. 3.
    Haugwitz, M., Dery, O., Turpin, P., and Fang, Y., Genet. Eng. News, 2003, vol. 23, pp. 36–39.Google Scholar
  4. 4.
    Zubova, N.N., Bulavina, A.Yu., and Savitskii, A.P., Usp. Biol. Khim., 2003, vol. 43, pp. 163–224.Google Scholar
  5. 5.
    Verkhusha, V.V. and Lukyanov, K.K., Nat. Biotechnol., 2004, vol. 22, pp. 289–296.PubMedCrossRefGoogle Scholar
  6. 6.
    Zubova, N.N. and Savitskii, A.P., Usp. Biol. Khim., 2005, vol. 45, pp. 1–66.Google Scholar
  7. 7.
    Tallini, Y.N., Ohkura, M., Choi, B.R., Ji, G., Imoto, K., Doran, R., Lee, J., Plan, P., Wilson, J., Xin, H.B., Sanbe, A., Gulick, J., Mathai, J., Robbins, J., Salama, G., Nakai, J., and Kotlikoff, M.I., Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 4753–4758.PubMedCrossRefGoogle Scholar
  8. 8.
    Barondeau, D.P., Putnam, D.C., Kassmann, C.J., Tainer, J.A., and Getzoff, E.D., Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 12 111–12 116.CrossRefGoogle Scholar
  9. 9.
    Remington, S.J., Wacher, R.M., Yarbrough, D.K., Branchaud, B., Anderson, D.C., Kallio, K., and Lukyanov, K.A., Biochemistry, 2005, vol. 44, pp. 202–212.PubMedCrossRefGoogle Scholar
  10. 10.
    Barondeau, D.P., Cassmann, C.J., Tainer, J.A., and Getzoff, E.D., J. Am. Chem. Soc., 2006, vol. 128, pp. 4685–4693.PubMedCrossRefGoogle Scholar
  11. 11.
    Pletneva, N., Pletnev, S., Tikhonova, T., Popov, V., Martynov, V., and Pletnev, V., Acta Crystallogr., 2006, vol. D62, pp. 527–532.Google Scholar
  12. 12.
    Gurskaya, N.G., Savitsky, A.P., Yanushevich, Y.G., Lukyanov, S.A., and Lukyanov, K.A., BMC Biochemistry, 2001, vol. 2, p. 6.PubMedCrossRefGoogle Scholar
  13. 13.
    Evdokimov, A.G., Pokross, M.E., Egorov, N.S., Zaraisky, A.G., Yampolsky, I.V., Merzlyak, E.M., Shkoporov, A.N., Sander, I., Lukyanov, K.A., and Chudakov, D.M., EMBO Rep., 2006, vol. 7, pp. 1006–1012.PubMedCrossRefGoogle Scholar
  14. 14.
    Chudakov, D.M., Feofanov, A.V., Mudrik, N.N., Lukyanov, S., and Lukyanov, K.A., J. Biol. Chem., 2003, vol. 278, pp. 7215–7219.PubMedCrossRefGoogle Scholar
  15. 15.
    Andresen, M., Wahl, M.C., Stiel, A.C., Grater, F., Schafer, L.V., Trowitzsch, S., Weber, G., Eggeling, C., Grubmuller, H., Hell, S.W., and Jakobs, S., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 13070–13074.PubMedCrossRefGoogle Scholar
  16. 16.
    Remington, S.J., Curr. Opin. Struct. Biol., 2006, vol. 16, pp. 1–8.CrossRefGoogle Scholar
  17. 17.
    Wood, T.I., Barondeau, P., Hitomi, C., Kassmann, C.J., Tainer, J.A., and Getzoff, E.D., Biochemistry, 2005, vol. 44, pp. 16 211–16 220.Google Scholar
  18. 18.
    Zagranichny, V.E., Rudenko, N.V., Gorokhovatsky, A.Yu., Zakharov, M.V., Shenkarev, Z.O., Balashova, T.A., and Arseniev, A.S., Biochemistry, 2004, vol. 43, pp. 4764–4772.PubMedCrossRefGoogle Scholar
  19. 19.
    Henderson, J.N. and Remington, S.J., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 12 712–12 717.CrossRefGoogle Scholar
  20. 20.
    Vondrasek, J., Bendova, L., Klusak, V., and Hobza, P., J. Am. Chem. Soc., 2005, vol. 127, pp. 2615–2619.PubMedCrossRefGoogle Scholar
  21. 21.
    Tubbs, J.L., Tainer, J.A., and Getzoff, E.D., Biochemistry, 2005, vol. 44, pp. 9833–9840.PubMedCrossRefGoogle Scholar
  22. 22.
    van Thor, J.J., Gensch, T., Hellingwer, K.J., and Johnson, L.N., Nat. Struct. Biol., 2002, vol. 9, pp. 37–41.PubMedCrossRefGoogle Scholar
  23. 23.
    Quillin, M.L., Anstrom, D.M., Shu, X., O’Leary, S., Kallio, K., Chudakov, D.M., and Remington, S.J., Biochemistry, 2005, vol. 44, pp. 5774–5787.PubMedCrossRefGoogle Scholar
  24. 24.
    Nienhaus, K., Nienhaus, G.U., Wiedenmann, J., and Nar, H., Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 9156–9159.PubMedCrossRefGoogle Scholar
  25. 25.
    Campbell, R.E., Tour, O., Palmer, A.E., Stainbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y., Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 7877–7882.PubMedCrossRefGoogle Scholar
  26. 26.
    Karasawa, S., Araki, T., Yamamoto-Hino, M., and Miyawaki, A., J. Biol. Chem., 2003, vol. 278, pp. 34167–34171.PubMedCrossRefGoogle Scholar
  27. 27.
    Karasawa, S., Araki, T., Nagai, T., Mizuno, H., and Miyawaki, A., Biochem. J., 2004, vol. 381, pp. 307–312.PubMedCrossRefGoogle Scholar
  28. 28.
    Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E., and Tsien, R.Y., Nature Biotechnol., 2004, vol. 22, pp. 1567–1572.CrossRefGoogle Scholar
  29. 29.
    Ando, R., Mizuno, H., and Miyawaki, A., Science, 2004, vol. 306, pp. 1370–1373.PubMedCrossRefGoogle Scholar
  30. 30.
    Wiedenmann, J., Ivanchenko, S., Oswald, F., Schmitt, F., Rocker, C., Salih, A., Spindler, K.D., and Nienhaus, G.U., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 15 905–15 910.CrossRefGoogle Scholar
  31. 31.
    Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R., Gene, 1989, vol. 77, pp. 51–59.PubMedCrossRefGoogle Scholar
  32. 32.
    Otwinowski, Z. and Minor, W., Methods Enzymol., 1997, vol. 276, pp. 307–326.CrossRefGoogle Scholar
  33. 33.
    Vagin, A. and Teplyakov, A., J. Appl. Crystallogr., 1997, vol. 30, pp. 1022–1025.CrossRefGoogle Scholar
  34. 34.
    Collaborative Computational Project Number 4, Acta. Cryst., 1994, vol. D50,Part 5, pp. 760–763.Google Scholar
  35. 35.
    Murshudov, G.N., Vagin, A.A., and Dodson, E.J., Acta Crystallogr., 1997, vol. D53, pp. 240–255.Google Scholar
  36. 36.
    Emsley, P. and Cowtan, K., Acta Crystallogr., 2004, vol. D60, pp. 2126–2132.Google Scholar
  37. 37.
    Perrakis, A., Sixma, T.K., Wilson, K.S., and Lamzin, V.S., Acta Crystallogr., 1997, vol. D53, pp. 448–455.Google Scholar
  38. 38.
    Laskowski, R.A., MacArthur M.W., Moss D.S., Thornton J.M., J. Appl. Crystallogr., 1993, vol. 26, pp. 283–291.CrossRefGoogle Scholar
  39. 39.
    Evans, S.V., J. Mol. Graphics, 1993, vol. 11, pp. 134–138.CrossRefGoogle Scholar
  40. 40.
    Wallace, A.C., Laskowski, R.A., and Thornton, J.M., Protein Eng., 1995, vol. 8, pp. 127–134.PubMedCrossRefGoogle Scholar
  41. 41.
    McDonald, I.K. and Thornton, J.M., J. Mol. Biol., 1994, vol. 238, pp. 777–793.PubMedCrossRefGoogle Scholar
  42. 42.
    DeLano, W.L., in http://www.pymol.org, 2002.
  43. 43.
    Cambridge Soft Corporation, http://www.camsoft.com.

Copyright information

© Pleiades Publishing, Inc. 2007

Authors and Affiliations

  • N. V. Pletneva
    • 1
  • S. V. Pletnev
    • 3
  • D. M. Chudakov
    • 1
  • T. V. Tikhonova
    • 2
  • V. O. Popov
    • 2
  • V. I. Martynov
    • 2
  • A. Wlodawer
    • 4
  • Z. Dauter
    • 3
  • V. Z. Pletnev
    • 1
  1. 1.Shemyakin-Ovchinnikov Institute of Bioorganic ChemistryRussian Academy of SciencesMoscowRussia
  2. 2.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia
  3. 3.Synchrotron Radiation Research Section, Laboratory of Macromolecular CrystallographyNational Cancer InstituteArgonneUSA
  4. 4.Protein Structure Section, Laboratory of Macromolecular CrystallographyNational Cancer InstituteFrederickUSA

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