Advertisement

Journal of Fluorescence

, Volume 25, Issue 1, pp 87–94 | Cite as

Tryptophan Residue of the D-Galactose/D-Glucose-Binding Protein from E. Coli Localized in its Active Center Does not Contribute to the Change in Intrinsic Fluorescence Upon Glucose Binding

  • Olga V. Stepanenko
  • Alexander V. Fonin
  • Olesya V. Stepanenko
  • Maria Staiano
  • Sabato D’Auria
  • Irina M. Kuznetsova
  • Konstantin K. Turoverov
ORIGINAL PAPER

Abstract

Changes of the characteristics of intrinsic tryptophan fluorescence of the wild type of D-galactose/D-glucose-binding protein from Escherichia coli (GGBPwt) induced by D-glucose binding were examined by the intrinsic UV-fluorescence of proteins, circular dyhroism in the near-UV region, and acrylamide-induced fluorescence quenching. The analysis of the different characteristics of GGBPwt and its mutant form GGBP-W183A together with the analysis of the microenvironment of tryptophan residues of GGBPwt revealed that Trp 183, which is directly involved in sugar binding, has the least influence on the provoked by D-glucose blue shift and increase in the intensity of protein intrinsic fluorescence in comparison with other tryptophan residues of GGBP.

Keywords

Intrinsic fluorescence of proteins Tryptophan residue Microenvironment of tryptophan residues 

Abbreviations

GGBPwt

Wild type of D-galactose/D-glucose-binding protein from Escherichia coli

GGBPwt/Glc

Complex of GGBPwt with D-glucose

PBP

Ligand-binding proteins of the bacterial periplasm

Notes

Acknowledgments

This work was supported in part by the Program MCB RAS (K.K. Turoverov), the Scholarships from the President of RF (Olga V. Stepanenko SP-563.2012.4 and A.V. Fonin SP-2390.2012.4), and the Program of Cooperation between RAS and CNR (S. D’Auria and K.K. Turoverov). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Supplementary material

10895_2014_1483_MOESM1_ESM.doc (269 kb)
ESM 1 (DOC 269 KB)

References

  1. 1.
    Fukami-Kobayashi K, Tateno Y, Nishikawa K (1999) Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history. J Mol Biol 286(1):279–290. doi: 10.1006/jmbi.1998.2454 PubMedCrossRefGoogle Scholar
  2. 2.
    Dwyer MA, Hellinga HW (2004) Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr Opin Struct Biol 14(4):495–504PubMedCrossRefGoogle Scholar
  3. 3.
    Anraku Y (1968) Transport of sugars and amino acids in bacteria. II. Properties of galactose- and leucine-binding proteins. J Biol Chem 243(11):3123–3127PubMedGoogle Scholar
  4. 4.
    Stepanenko O, Fonin A, Kuznetsova I, Turoverov K (2012) Ligand-binding proteins: structure, stability and practical application. Protein structure. InTech, Rijeka, pp 265–290Google Scholar
  5. 5.
    Hazelbauer GL, Adler J (1971) Role of the galactose binding protein in chemotaxis of Escherichia coli toward galactose. Nat New Biol 230(12):101–104PubMedCrossRefGoogle Scholar
  6. 6.
    Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415(6871):545–549. doi: 10.1038/415545a PubMedCrossRefGoogle Scholar
  7. 7.
    Borrok MJ, Kiessling LL, Forest KT (2007) Conformational changes of glucose/galactose-binding protein illuminated by open, unliganded, and ultra-high-resolution ligand-bound structures. Protein Sci 16(6):1032–1041. doi: 10.1110/ps.062707807 PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Shilton BH, Flocco MM, Nilsson M, Mowbray SL (1996) Conformational changes of three periplasmic receptors for bacterial chemotaxis and transport: the maltose-, glucose/galactose- and ribose-binding proteins. J Mol Biol 264(2):350–363. doi: 10.1006/jmbi.1996.0645 PubMedCrossRefGoogle Scholar
  9. 9.
    Tolosa L (2010) On the design of low-cost fluorescent protein biosensors. Adv Biochem Eng Biotechnol 116:143–157. doi: 10.1007/10_2008_39 Google Scholar
  10. 10.
    Vyas NK, Vyas MN, Quiocho FA (1988) Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science 242(4883):1290–1295PubMedCrossRefGoogle Scholar
  11. 11.
    Vyas NK, Vyas MN, Quiocho FA (1991) Comparison of the periplasmic receptors for L-arabinose, D-glucose/D-galactose, and D-ribose. Structural and functional similarity. J Biol Chem 266(8):5226–5237PubMedGoogle Scholar
  12. 12.
    Vyas MN, Vyas NK, Quiocho FA (1994) Crystallographic analysis of the epimeric and anomeric specificity of the periplasmic transport/chemosensory protein receptor for D-glucose and D-galactose. Biochemistry 33(16):4762–4768PubMedCrossRefGoogle Scholar
  13. 13.
    Amiss TJ, Sherman DB, Nycz CM, Andaluz SA, Pitner JB (2007) Engineering and rapid selection of a low-affinity glucose/galactose-binding protein for a glucose biosensor. Protein Sci 16(11):2350–2359. doi: 10.1110/ps.073119507 PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    de Lorimier RM, Smith JJ, Dwyer MA, Looger LL, Sali KM, Paavola CD, Rizk SS, Sadigov S, Conrad DW, Loew L, Hellinga HW (2002) Construction of a fluorescent biosensor family. Protein Sci 11(11):2655–2675. doi: 10.1110/ps.021860 PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Deuschle K, Okumoto S, Fehr M, Looger LL, Kozhukh L, Frommer WB (2005) Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci 14(9):2304–2314. doi: 10.1110/ps.051508105 PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Fehr M, Lalonde S, Lager I, Wolff MW, Frommer WB (2003) In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J Biol Chem 278(21):19127–19133. doi: 10.1074/jbc.M301333200 PubMedCrossRefGoogle Scholar
  17. 17.
    Ge X, Rao G, Tolosa L (2008) On the possibility of real-time monitoring of glucose in cell culture by microdialysis using a fluorescent glucose binding protein sensor. Biotechnol Prog 24(3):691–697. doi: 10.1021/bp070411k PubMedCrossRefGoogle Scholar
  18. 18.
    Ge X, Tolosa L, Rao G (2004) Dual-labeled glucose binding protein for ratiometric measurements of glucose. Anal Chem 76(5):1403–1410. doi: 10.1021/ac035063p PubMedCrossRefGoogle Scholar
  19. 19.
    Hsieh HV, Pfeiffer ZA, Amiss TJ, Sherman DB, Pitner JB (2004) Direct detection of glucose by surface plasmon resonance with bacterial glucose/galactose-binding protein. Biosens Bioelectron 19(7):653–660PubMedCrossRefGoogle Scholar
  20. 20.
    Khan F, Gnudi L, Pickup JC (2008) Fluorescence-based sensing of glucose using engineered glucose/galactose-binding protein: a comparison of fluorescence resonance energy transfer and environmentally sensitive dye labelling strategies. Biochem Biophys Res Commun 365(1):102–106. doi: 10.1016/j.bbrc.2007.10.129 PubMedCrossRefGoogle Scholar
  21. 21.
    Khan F, Saxl TE, Pickup JC (2010) Fluorescence intensity- and lifetime-based glucose sensing using an engineered high-Kd mutant of glucose/galactose-binding protein. Anal Biochem 399(1):39–43. doi: 10.1016/j.ab.2009.11.035 PubMedCrossRefGoogle Scholar
  22. 22.
    Sakaguchi-Mikami A, Taneoka A, Yamoto R, Ferri S, Sode K (2008) Engineering of ligand specificity of periplasmic binding protein for glucose sensing. Biotechnol Lett 30(8):1453–1460. doi: 10.1007/s10529-008-9712-7 PubMedCrossRefGoogle Scholar
  23. 23.
    Sakaguchi-Mikami A, Taniguchi A, Sode K, Yamazaki T (2011) Construction of a novel glucose-sensing molecule based on a substrate-binding protein for intracellular sensing. Biotechnol Bioeng 108(4):725–733. doi: 10.1002/bit.23006 PubMedCrossRefGoogle Scholar
  24. 24.
    Saxl T, Khan F, Ferla M, Birch D, Pickup J (2011) A fluorescence lifetime-based fibre-optic glucose sensor using glucose/galactose-binding protein. Analyst 136(5):968–972. doi: 10.1039/c0an00430h PubMedCrossRefGoogle Scholar
  25. 25.
    Saxl T, Khan F, Matthews DR, Zhi ZL, Rolinski O, Ameer-Beg S, Pickup J (2009) Fluorescence lifetime spectroscopy and imaging of nano-engineered glucose sensor microcapsules based on glucose/galactose-binding protein. Biosens Bioelectron 24(11):3229–3234. doi: 10.1016/j.bios.2009.04.003 PubMedCrossRefGoogle Scholar
  26. 26.
    Thomas J, Sherman DB, Amiss TJ, Andaluz SA, Pitner JB (2007) Synthesis and biosensor performance of a near-IR thiol-reactive fluorophore based on benzothiazolium squaraine. Bioconjug Chem 18(6):1841–1846. doi: 10.1021/bc700146r PubMedCrossRefGoogle Scholar
  27. 27.
    Thomas KJ, Sherman DB, Amiss TJ, Andaluz SA, Pitner JB (2006) A long-wavelength fluorescent glucose biosensor based on bioconjugates of galactose/glucose binding protein and Nile Red derivatives. Diabetes Technol Ther 8(3):261–268. doi: 10.1089/dia.2006.8.261 PubMedCrossRefGoogle Scholar
  28. 28.
    Tolosa L, Gryczynski I, Eichhorn LR, Dattelbaum JD, Castellano FN, Rao G, Lakowicz JR (1999) Glucose sensor for low-cost lifetime-based sensing using a genetically engineered protein. Anal Biochem 267(1):114–120. doi: 10.1006/abio.1998.2974 PubMedCrossRefGoogle Scholar
  29. 29.
    Weidemaier K, Lastovich A, Keith S, Pitner JB, Sistare M, Jacobson R, Kurisko D (2011) Multi-day pre-clinical demonstration of glucose/galactose binding protein-based fiber optic sensor. Biosens Bioelectron 26(10):4117–4123. doi: 10.1016/j.bios.2011.04.007 PubMedCrossRefGoogle Scholar
  30. 30.
    Ye K, Schultz JS (2003) Genetic engineering of an allosterically based glucose indicator protein for continuous glucose monitoring by fluorescence resonance energy transfer. Anal Chem 75(14):3451–3459PubMedCrossRefGoogle Scholar
  31. 31.
    Ge X, Lam H, Modi SJ, LaCourse WR, Rao G, Tolosa L (2007) Comparing the performance of the optical glucose assay based on glucose binding protein with high-performance anion-exchange chromatography with pulsed electrochemical detection: efforts to design a low-cost point-of-care glucose sensor. J Diabetes Sci Technol 1(6):864–872PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Veetil JV, Jin S, Ye K (2010) A glucose sensor protein for continuous glucose monitoring. Biosens Bioelectron 26(4):1650–1655. doi: 10.1016/j.bios.2010.08.052 PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Fonin AV, Stepanenko OV, Povarova OI, Volova CA, Philippova EM, Bublikov GS, Kuznetsova IM, Demchenko AP, Turoverov KK (2014) Spectral characteristics of the mutant form GGBP/H152C of D-glucose/D-galactose-binding protein labeled with fluorescent dye BADAN: influence of external factors. PeerJ 2:e275. doi: 10.7717/peerj.275 PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Khan F, Pickup JC (2013) Near-infrared fluorescence glucose sensing based on glucose/galactose-binding protein coupled to 651-blue oxazine. Biochem Biophys Res Commun 438(3):488–492. doi: 10.1016/j.bbrc.2013.07.111 PubMedCrossRefGoogle Scholar
  35. 35.
    Stepanenko OV, Fonin AV, Morozova KS, Verkhusha VV, Kuznetsova IM, Turoverov KK, Staiano M, D’Auria S (2011) New insight in protein-ligand interactions. 2. Stability and properties of two mutant forms of the D-galactose/D-glucose-binding protein from E. coli. J Phys Chem B 115(29):9022–9032. doi: 10.1021/jp204555h PubMedCrossRefGoogle Scholar
  36. 36.
    Stepanenko OV, Povarova OI, Fonin AV, Kuznetsova IM, Turoverov KK, Staiano M, Varriale A, D’Auria S (2011) New insight into protein-ligand interactions. The case of the D-galactose/D-glucose-binding protein from Escherichia coli. J Phys Chem B 115(12):2765–2773. doi: 10.1021/jp1095486 PubMedCrossRefGoogle Scholar
  37. 37.
    Piszczek G, D’Auria S, Staiano M, Rossi M, Ginsburg A (2004) Conformational stability and domain coupling in D-glucose/D-galactose-binding protein from Escherichia coli. Biochem J 381(Pt 1):97–103. doi: 10.1042/BJ20040232 PubMedCentralPubMedGoogle Scholar
  38. 38.
    D’Auria S, Alfieri F, Staiano M, Pelella F, Rossi M, Scire A, Tanfani F, Bertoli E, Grycznyski Z, Lakowicz JR (2004) Structural and thermal stability characterization of Escherichia coli D-galactose/D-glucose-binding protein. Biotechnol Prog 20(1):330–337. doi: 10.1021/bp0341848 PubMedCrossRefGoogle Scholar
  39. 39.
    D’Auria S, Ausili A, Marabotti A, Varriale A, Scognamiglio V, Staiano M, Bertoli E, Rossi M, Tanfani F (2006) Binding of glucose to the D-galactose/D-glucose-binding protein from Escherichia coli restores the native protein secondary structure and thermostability that are lost upon calcium depletion. J Biochem 139(2):213–221. doi: 10.1093/jb/mvj027 PubMedCrossRefGoogle Scholar
  40. 40.
    Scognamiglio V, Scire A, Aurilia V, Staiano M, Crescenzo R, Palmucci C, Bertoli E, Rossi M, Tanfani F, D’Auria S (2007) A strategic fluorescence labeling of D-galactose/D-glucose-binding protein from Escherichia coli helps to shed light on the protein structural stability and dynamics. J Proteome Res 6(11):4119–4126. doi: 10.1021/pr070439r PubMedCrossRefGoogle Scholar
  41. 41.
    Herman P, Vecer J, Barvik I Jr, Scognamiglio V, Staiano M, de Champdore M, Varriale A, Rossi M, D’Auria S (2005) The role of calcium in the conformational dynamics and thermal stability of the D-galactose/D-glucose-binding protein from Escherichia coli. Proteins 61(1):184–195. doi: 10.1002/prot.20582 PubMedCrossRefGoogle Scholar
  42. 42.
    Marabotti A, Herman P, Staiano M, Varriale A, de Champdore M, Rossi M, Gryczynski Z, D’Auria S (2006) Pressure effect on the stability and the conformational dynamics of the D-Galactose/D-Glucose-binding protein from Escherichia coli. Proteins 62(1):193–201. doi: 10.1002/prot.20753 PubMedCrossRefGoogle Scholar
  43. 43.
    Stepanenko OV, Povarova OI, Stepanenko OV, Fonin AV, Kuznetsova IM, Turoverov KK, Staiano M, D’Auria S (2010) Structure and stability of D-galactose/D-glucose-binding protein. The role of D-glucose binding and Ca ion depletion. Spectrosc Int J 24(3–4):355–359CrossRefGoogle Scholar
  44. 44.
    Stepanenko OV, Stepanenko OV, Fonin AV, Verkhusha VV, Kuznetsova IM, Turoverov KK (2012) Protein-ligand interactions of the D-Galactose/D-Glucose-binding protein as a potential sensing probe of glucose biosensors. Spectrosc Int J 27(5–6):373–379CrossRefGoogle Scholar
  45. 45.
    Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685PubMedCrossRefGoogle Scholar
  46. 46.
    Turoverov KK, Kuznetsova IM, Zaitsev VN (1985) The environment of the tryptophan residue in Pseudomonas aeruginosa azurin and its fluorescence properties. Biophys Chem 23(1–2):79–89PubMedCrossRefGoogle Scholar
  47. 47.
    Kuznetsova IM, Turoverov KK (1998) What determines the characteristics of the intrinsic UV-fluorescence of proteins? Analysis of the properties of the microenvironment and features of the localization of their tryptophan residues. Tsitologiia 40(8–9):747–762PubMedGoogle Scholar
  48. 48.
    Förster T (1960) Transfer mechanisms of electronic excitation energy. Radiat Res Suppl 2:326–339CrossRefGoogle Scholar
  49. 49.
    Dale RE, Eisinger J (1974) Intramolecular distances determined by energy transfer. Dependence on orientational freedom of donor and acceptor. Biopolymers 13(8):1573–1605. doi: 10.1002/bip.1974.360130807 CrossRefGoogle Scholar
  50. 50.
    Eisinger J, Feuer B, Lamola AA (1969) Intramolecular singlet excitation transfer. Applications to polypeptides. Biochemistry 8(10):3908–3915PubMedCrossRefGoogle Scholar
  51. 51.
    Steinberg IZ (1971) Long-range nonradiative transfer of electronic excitation energy in proteins and polypeptides. Annu Rev Biochem 40:83–114. doi: 10.1146/annurev.bi.40.070171.000503 PubMedCrossRefGoogle Scholar
  52. 52.
    Turoverov KK, Kuznetsova IM (2003) Intrinsic fluorescence of actin. J Fluoresc 13(1):41–57CrossRefGoogle Scholar
  53. 53.
    Stepanenko OV, Kuznetsova IM, Turoverov KK, Huang C, Wang CC (2004) Conformational change of the dimeric DsbC molecule induced by GdnHCl. A study by intrinsic fluorescence. Biochemistry 43(18):5296–5303PubMedCrossRefGoogle Scholar
  54. 54.
    Giordano A, Russo C, Raia CA, Kuznetsova IM, Stepanenko OV, Turoverov KK (2004) Highly UV-absorbing complex in selenomethionine-substituted alcohol dehydrogenase from Sulfolobus solfataricus. J Proteome Res 3(3):613–620Google Scholar
  55. 55.
    Turoverov KK, Biktashev AG, Dorofeiuk AV, Kuznetsova IM (1998) A complex of apparatus and programs for the measurement of spectral, polarization and kinetic characteristics of fluorescence in solution. Tsitologiia 40(8–9):806–817PubMedGoogle Scholar
  56. 56.
    Fonin AV, Sulatskaya AI, Kuznetsova IM, Turoverov KK (2014) Fluorescence of dyes in solutions with high absorbance. Inner filter effect correction. PLoS One 9(7):e103878. doi: 10.1371/journal.pone.0103878 PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Eftink MR (1994) The use of fluorescence methods to monitor unfolding transitions in proteins. Biophys J 66(2 Pt 1):482–501PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Sulatskaya AI, Povarova OI, Kuznetsova IM, Uversky VN, Turoverov KK (2012) Binding stoichiometry and affinity of fluorescent dyes to proteins in different structural states. Methods Mol Biol 895:441–460PubMedCrossRefGoogle Scholar
  59. 59.
    Stepanenko OV, Stepanenko OV, Kuznetsova IM, Shcherbakova DM, Verkhusha VV, Turoverov KK (2012) Distinct effects of guanidine thiocyanate on the structure of superfolder GFP. PLoS One 7(11):e48809PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Dutta S, Burkhardt K, Young J, Swaminathan GJ, Matsuura T, Henrick K, Nakamura H, Berman HM (2009) Data deposition and annotation at the worldwide protein data bank. Mol Biotechnol 42(1):1–13PubMedCrossRefGoogle Scholar
  61. 61.
    Hsin J, Arkhipov A, Yin Y, Stone JE, Schulten K (2008) Using VMD: an introductory tutorial. Curr Protoc Bioinforma Chapter 5: Unit 5 7Google Scholar
  62. 62.
    Merritt EA, Bacon DJ (1977) Raster3D: photorealistic molecular graphics. Methods Enzymol 277:505–524CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Olga V. Stepanenko
    • 1
  • Alexander V. Fonin
    • 1
  • Olesya V. Stepanenko
    • 1
  • Maria Staiano
    • 3
  • Sabato D’Auria
    • 3
  • Irina M. Kuznetsova
    • 1
    • 2
  • Konstantin K. Turoverov
    • 1
    • 2
  1. 1.Institute of Cytology of the Russian Academy of SciencesSt. PetersburgRussia
  2. 2.St. Petersburg State Polytechnical UniversitySt. PetersburgRussia
  3. 3.IBP-CNR, Laboratory for Molecular SensingNaplesItaly

Personalised recommendations