Solution Structure, Copper Binding and Backbone Dynamics of Recombinant Ber e 1-The Major Allergen from Brazil Nut

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Rundqvist, Louise ^a   Tengel, Tobias ^a   Zdunek, Janusz ^b   Björn, Erik ^a   Schleucher, Jürgen ^a   Alcocer, Marcos J C ^c   Larsson, Göran ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b Protein Constructor Developers Company   (Sweden)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ION; IMMUNOGLOBULIN E; RECOMBINANT ALLERGEN; RECOMBINANT BER E 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BRAZIL; CONTROLLED STUDY; COPPER BINDING; ELECTRIC POTENTIAL; HYDROPHOBICITY; METAL BINDING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUT; PROTEIN BINDING; PROTEIN STRUCTURE;

2S ALBUMINS, PLANT; ANTIGENS, PLANT; BERTHOLLETIA; COPPER; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

BERTHOLLETIA EXCELSA; HUMAN ECHOVIRUS 1; MUS; ZIZIPHUS MAURITIANA;

EID: 84867114770     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046435     Document Type: Article

References (70)

1. Sampson HA, (2004) Update on food allergy. J Allergy Clin Immunol 113: 805-819.
2. Radauer C, Bublin M, Wagner S, Mari A, Breiteneder H, (2008) Allergens are distributed into few protein families and possess a restricted number of biochemical functions. J Allergy Clin Immunol 121: 847-852 e847.
3. Ruiter B, Shreffler WG, (2012) The role of dendritic cells in food allergy. Journal of Allergy and Clinical Immunology 129: 921-928.
4. Radauer C, Breiteneder H, (2007) Evolutionary biology of plant food allergens. J Allergy Clin Immunol 120: 518-525.
5. Kreis M, Forde BG, Rahman S, Miflin BJ, Shewry PR, (1985) Molecular evolution of the seed storage proteins of barley, rye and wheat. J Mol Biol 183: 499-502.
6. Moreno FJ, Clemente A, (2008) 2S Albumin Storage Proteins: What Makes them Food Allergens? Open Biochem J 2: 16-28.
7. Pastorello EA, Farioli L, Pravettoni V, Ispano M, Conti A, et al. (1998) Sensitization to the major allergen of Brazil nut is correlated with the clinical expression of allergy. J Allergy Clin Immunol 102: 1021-1027.
8. Bock SA, Munoz-Furlong A, Sampson HA, (2001) Fatalities due to anaphylactic reactions to foods. Journal of Allergy and Clinical Immunology 107: 191-193.
9. Tengel T, Alcocer MJ, Schleucher J, Larsson G, (2005) Complete assignment and secondary structure of the Brazil nut allergen Ber e 1. J Biomol NMR 32: 336.
10. Alcocer M, Rundqvist L, Larsson G, (2012) Ber e 1 protein: the versatile major allergen from Brazil nut seeds. Biotechnol Lett 34: 597-610.
11. Nordlee JA, Taylor SL, Townsend JA, Thomas LA, Bush RK, (1996) Identification of a Brazil-nut allergen in transgenic soybeans. N Engl J Med 334: 688-692.
12. Alcocer MJ, Murtagh GJ, Bailey K, Dumoulin M, Meseguer AS, et al. (2002) The disulphide mapping, folding and characterisation of recombinant Ber e 1, an allergenic protein, and SFA8, two sulphur-rich 2S plant albumins. J Mol Biol 324: 165-175.
13. Brix S, Kjaer TM, Barkholt V, Frokiaer H, (2004) Lipopolysaccharide contamination of beta-lactoglobulin affects the immune response against intraperitoneally and orally administered antigen. Int Arch Allergy Immunol 135: 216-220.
14. Dearman RJ, Alcocer MJ, Kimber I, (2007) Influence of plant lipids on immune responses in mice to the major Brazil nut allergen Ber e 1. Clin Exp Allergy 37: 582-591.
15. Onaderra M, Monsalve RI, Mancheno JM, Villalba M, Delpozo AM, et al. (1994) Food Mustard Allergen Interaction with Phospholipid-Vesicles. European Journal of Biochemistry 225: 609-615.
16. van Wijk F, Nierkens S, Hassing I, Feijen M, Koppelman SJ, et al. (2005) The effect of the food matrix on in vivo immune responses to purified peanut allergens. Toxicol Sci 86: 333-341.
17. Naozuka J, Oliveira PV, (2007) Fe, Mn and Zn distribution in protein fractions of Brazil-nut, cupuassu seed and coconut pulp by solid-liquid extraction and electrothermal atomic absorption spectrometry. Journal of the Brazilian Chemical Society 18: 1547-1553.
18. Larsson G, Schleucher J, Onions J, Hermann S, Grundstrom T, et al. (2005) Backbone dynamics of a symmetric calmodulin dimer in complex with the calmodulin-binding domain of the basic-helix-loop-helix transcription factor SEF2-1/E2-2: a highly dynamic complex. Biophys J 89: 1214-1226.
19. Akke M, Liu J, Cavanagh J, Erickson HP, Palmer AG, (1998) Pervasive conformational fluctuations on microsecond time scales in a fibronectin type III domain. Nature Structural Biology 5: 55-59.
20. Feher VA, Cavanagh J, (1999) Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F. Nature 400: 289-293.
21. Altenbach SB, Pearson KW, Leung FW, Sun SSM, (1987) Cloning and Sequence-Analysis of a Cdna-Encoding a Brazil Nut Protein Exceptionally Rich in Methionine. Plant Molecular Biology 8: 239-250.
22. Pantoja-Uceda D, Bruix M, Gimenez-Gallego G, Rico M, Santoro J, (2003) Solution structure of RicC3, a 2S albumin storage protein from Ricinus communis. Biochemistry 42: 13839-13847.
23. Lehmann K, Schweimer K, Reese G, Randow S, Suhr M, et al. (2006) Structure and stability of 2S albumin-type peanut allergens: implications for the severity of peanut allergic reactions. Biochem J 395: 463-472.
24. Rico M, Bruix M, Gonzalez C, Monsalve RI, Rodriguez R, (1996) H-1 NMR assignment and global fold of napin BnIb, a representative 2S albumin seed protein. Biochemistry 35: 15672-15682.
25. Pantoja-Uceda D, Palomares O, Bruix M, Villalba M, Rodriguez R, et al. (2004) Solution structure and stability against digestion of rproBnIb, a recombinant 2S albumin from rapeseed: relationship to its allergenic properties. Biochemistry 43: 16036-16045.
26. Pantoja-Uceda D, Shewry PR, Bruix M, Tatham AS, Santoro J, et al. (2004) Solution structure of a methionine-rich 2S albumin from sunflower seeds: relationship to its allergenic and emulsifying properties. Biochemistry 43: 6976-6986.
27. Murzin AG, Brenner SE, Hubbard T, Chothia C, (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540.
28. Krebbers E, Herdies L, De Clercq A, Seurinck J, Leemans J, et al. (1988) Determination of the Processing Sites of an Arabidopsis 2S Albumin and Characterization of the Complete Gene Family. Plant Physiol 87: 859-866.
29. Monsalve RI, Lopez-Otin C, Villalba M, Rodriguez R, (1991) A new distinct group of 2 S albumins from rapeseed. Amino acid sequence of two low molecular weight napins. FEBS Lett 295: 207-210.
30. Alcocer MJC, Murtagh GJ, Wilson PB, Progias P, Lin J, et al. (2004) The major human structural IgE epitope of the Brazil nut allergen Ber e 1: A chimaeric and protein microarray approach. Journal of Molecular Biology 343: 759-769.
31. Hernandez M, Ghersi D, Sanchez R, (2009) SITEHOUND-web: a server for ligand binding site identification in protein structures. Nucleic Acids Research 37: W413-W416.
32. Pons JL, de Lamotte F, Gautier MF, Delsuc MA, (2003) Refined solution structure of a liganded type 2 wheat nonspecific lipid transfer protein. Journal of Biological Chemistry 278: 14249-14256.
33. Bansal AS, Chee R, Nagendran V, Warner A, Hayman G, (2007) Dangerous liaison: Sexually transmitted allergic reaction to Brazil nuts. Journal of Investigational Allergology and Clinical Immunology 17: 189-191.
34. Murtagh GJ, Archer DB, Dumoulin M, Ridout S, Matthews S, et al. (2003) In vitro stability and immunoreactivity of the native and recombinant plant food 2S albumins Ber e 1 and SFA-8. Clin Exp Allergy 33: 1147-1152.
35. Koppelman SJ, Hefle SL, Taylor SL, de Jong GAH, (2010) Digestion of peanut allergens Ara h 1, Ara h 2, Ara h 3, and Ara h 6: A comparative in vitro study and partial characterization of digestion-resistant peptides. Molecular Nutrition & Food Research 54: 1711-1721.
36. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Research 38: W545-W549.
37. Aalberse RC, (2000) Structural biology of allergens. Journal of Allergy and Clinical Immunology 106: 228-238.
38. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, et al. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003.
39. Larsson G, Martinez G, Schleucher J, Wijmenga SS, (2003) Detection of nano-second internal motion and determination of overall tumbling times independent of the time scale of internal motion in proteins from NMR relaxation data. J Biomol NMR 27: 291-312.
40. Orekhov VY, Nolde DE, Golovanov AP, Korzhnev DM, Arseniev AS, (1995) Processing of heteronuclear NMR relaxation data with the new software DASHA. Applied Magnetic Resonance 9: 581-588.
41. Palmer AG, Rance M, Wright PE, (1991) Intramolecular Motions of a Zinc Finger DNA-Binding Domain from Xfin Characterized by Proton-Detected Natural Abundance C-12 Heteronuclear Nmr-Spectroscopy. Journal of the American Chemical Society 113: 4371-4380.
42. Mandel AM, Akke M, Palmer AG, (1995) Backbone Dynamics of Escherichia-Coli Ribonuclease Hi- Correlations with Structure and Function in an Active Enzyme. Journal of Molecular Biology 246: 144-163.
43. Korzhnev DM, Salvatella X, Vendruscolo M, Di Nardo AA, Davidson AR, et al. (2004) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430: 586-590.
44. Vallurupalli P, Hansen DF, Kay LE, (2008) Structures of invisible, excited protein states by relaxation dispersion NMR spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 105: 11766-11771.
45. de Lamotte F, Vagner F, Pons JL, Gautier MF, Roumestand C, et al. (2001) Protein dynamics studies on a wheat type 2 lipid transfer protein. Comptes Rendus De L Academie Des Sciences Serie Ii Fascicule C-Chimie 4: 839-843.
46. Ubbink M, Lian LY, Modi S, Evans PA, Bendall DS, (1996) Analysis of the 1H-NMR chemical shifts of Cu(I)-, Cu(II)- and Cd-substituted pea plastocyanin. Metal-dependent differences in the hydrogen-bond network around the copper site. Eur J Biochem 242: 132-147.
47. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
48. Pickford AR, O'Leary JM, (2004) Isotopic labeling of recombinant proteins from the methylotrophic yeast Pichia pastoris. Methods Mol Biol 278: 17-33.
49. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, et al. (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6: 135-140.
50. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
51. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, et al. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59: 687-696.
52. Szyperski T, Luginbuhl P, Otting G, Guntert P, Wuthrich K, (1993) Protein dynamics studied by rotating frame 15N spin relaxation times. J Biomol NMR 3: 151-164.
53. Piotto M, Saudek V, Sklenar V, (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2: 661-665.
54. Grzesiek S, Bax A, (1993) The Importance of Not Saturating H2o in Protein Nmr- Application to Sensitivity Enhancement and Noe Measurements. Journal of the American Chemical Society 115: 12593-12594.
55. Johnson BA, Blevins RA, (1994) Nmr View- a Computer-Program for the Visualization and Analysis of Nmr Data. Journal of Biomolecular Nmr 4: 603-614.
56. Viles JH, Duggan BM, Zaborowski E, Schwarzinger S, Huntley JJA, et al. (2001) Potential bias in NMR relaxation data introduced by peak intensity analysis and curve fitting methods. Journal of Biomolecular Nmr 21: 1-9.
57. Wijmenga SS, Larsson G, Schleucher J, Onions J, Hermann S, et al. (2005) Backbone dynamics of a symmetric calmodulin dimer in complex with the calmodulin-binding domain of the basic-helix-loop-helix transcription factor SEF2-1/E2-2: A highly dynamic complex. Biophysical Journal 89: 1214-1226.
58. Davis DG, Perlman ME, London RE, (1994) Direct measurements of the dissociation-rate constant for inhibitor-enzyme complexes via the T1 rho and T2 (CPMG) methods. J Magn Reson B 104: 266-275.
59. Zdunek J, Martinez GV, Schleucher J, Lycksell PO, Yin Y, et al. (2003) Global structure and dynamics of human apolipoprotein CII in complex with micelles: Evidence for increased mobility of the helix involved in the activation of lipoprotein lipase. Biochemistry 42: 1872-1889.
60. Gangabadage CS, Zdunek J, Tessari M, Nilsson S, Olivecrona G, et al. (2008) Structure and dynamics of human apolipoprotein CIII. Journal of Biological Chemistry 283: 17416-17427.
61. Berjanskii MV, Neal S, Wishart DS, (2006) PREDITOR: a web server for predicting protein torsion angle restraints. Nucleic Acids Research 34: W63-W69.
62. Shen Y, Delaglio F, Cornilescu G, Bax A, (2009) TALOS plus: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. Journal of Biomolecular Nmr 44: 213-223.
63. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM, (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160: 65-73.
64. Schwieters CD, Clore GM, (2001) Internal coordinates for molecular dynamics and minimization in structure determination and refinement. Journal of Magnetic Resonance 152: 288-302.
65. Brünger AT, editor. X-PLOR Version 3.0: a System for X-ray Crystallography and NMR.
66. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 33-38, 27-38.
67. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, et al. (2005) Protein Identification and Analysis Tools on the ExPASy Server. The Proteomics Protocols Handbook 112: 571-607.
68. Hubbard SJ, Thornton JM (1993) NACCESS. pp. Computer program, Department of Biochemistry and Molecular Biology, University College London.
69. Christodoulou J, Larsson G, Fucini P, Connell SR, Pertinhez TA, et al. (2004) Heteronuclear NMR investigations of dynamic regions of intact Escherichia coli ribosomes. Proceedings of the National Academy of Sciences of the United States of America 101: 10949-10954.
70. Moreno FJ, Jenkins JA, Mellon NM, Rigby JSA, Robertson N, et al. (2004) Mass spectrometry and structural characterization of 2S albumin isoforms from Brazil nuts (Bertholletia excelsa) Biochimica et. Biophysica acta 1698: 175-186.