Solution Structure, Dynamics, and Hydrodynamics of the Calcium-bound Cross-reactive Birch Pollen Allergen Bet v 4 Reveal a Canonical Monomeric Two EF-Hand Assembly with a Regulatory Function

Journal of Molecular Biology

Volumn 336, Issue 5, 2004, Pages 1141-1157

  Neudecker, Philipp ^a   Nerkamp, Jörg ^a,d   Eisenmann, Anke ^a   Nourse, Amanda ^b   Lauber, Thomas ^a   Schweimer, Kristian ^a   Lehmann, Katrin ^a   Schwarzinger, Stephan ^a   Ferreira, Fátima ^c   Rösch, Paul ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF SALZBURG   (Austria)

^d NONE   (Germany)

Author keywords

Birch pollen allergen; EF hand; Heteronuclear NMR; Polcalcin; Solution structure

Indexed keywords

ALLERGEN; CALCIUM; CALCIUM BINDING PROTEIN; CALMODULIN; IMMUNOGLOBULIN E;

ALLERGENICITY; ALPHA HELIX; ANTIGEN STRUCTURE; ARTICLE; BIRCH; CIRCULAR DICHROISM; CROSS REACTION; ENZYME CONFORMATION; HYDRODYNAMICS; HYDROPHOBICITY; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLLEN ALLERGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURAL HOMOLOGY;

PHLEUM PRATENSE;

EID: 10744224375     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.12.070     Document Type: Article

References (94)

1. Kuby J. Immunology. 1992;Freeman, New York. pp. 359-372.
2. Breiteneder H., Pettenburger K., Bito A., Valenta R., Kraft D., Rumpold H., et al. The gene coding for the major birch pollen allergen BetvI, is highly homologous to a pea disease resistance response gene. EMBO J. 8:1989;1935-1938.
3. Gajhede M., Osmark P., Poulsen F.M., Ipsen H., Larsen J.N., van Neerven R.J.J., et al. X-ray and NMR structure of Bet v 1, the origin of birch pollen allergy. Nature Struct. Biol. 3:1996;1040-1045.
4. Schweimer K., Sticht H., Nerkamp J., Boehm M., Breitenbach M., Vieths S., Rösch P. NMR spectroscopy reveals common structural features of the birch pollen allergen Bet v 1 and the cherry allergen Pru a 1. Appl. Magn. Reson. 17:1999;449-464.
5. 15N resonance assignments of the major cherry allergen Pru a 1. J. Biomol. NMR. 18:2000;71-72.
6. Neudecker P., Schweimer K., Nerkamp J., Scheurer S., Vieths S., Sticht H., Rösch P. Allergic cross-reactivity made visible. Solution structure of the major cherry allergen Pru av 1. J. Biol. Chem. 276:2001;22756-22763.
7. 15N resonance assignments of SAM22, an allergenic stress-induced protein from soy bean. J. Biomol. NMR. 26:2003;191-192.
8. Neudecker P., Lehmann K., Nerkamp J., Haase T., Wangorsch A., Fötisch K., et al. Mutational epitope analysis of Pru av 1 and Api g 1, the major allergens of cherry and celery: correlating IgE reactivity with three-dimensional structure. Biochem. J. 376:2003;97-107.
9. Vieths S., Scheurer S., Ballmer-Weber B. Current understanding of cross-reactivity of food allergens and pollen. Ann. N. Y. Acad. Sci. 964:2002;47-68.
10. Engel E., Richter K., Obermeyer G., Briza P., Kungl A.J., Simon B., et al. Immunological and biological properties of Bet v 4, a novel birch pollen allergen with two ef-hand calcium-binding domains. J. Biol. Chem. 272:1997;28630-28637.
11. Twardosz A., Hayek B., Seiberler S., Vangelista L., Elfman L., Grönlund H. Molecular characterization, expression in Escherichia coli, and epitope analysis of a two EF-hand calcium-binding birch pollen allergen, Bet v 4. Biochem. Biophys. Res. Commun. 239:1997;197-204.
12. Hayek B., Vangelista L., Pastore A., Sperr W.R., Valent P., Vrtala S., et al. Molecular and immunologic characterization of a highly cross-reactive two EF-hand calcium-binding alder pollen allergen, Aln g 4: structural basis for calcium-modulated IgE recognition. J. Immunol. 161:1998;7031-7039.
13. Batanero E., Villalba M., Ledesma A., Puente J.X., Rodríguez R. Ole e 3, an olive-tree allergen, belongs to a widespread family of pollen proteins. Eur. J. Biochem. 241:1996;772-778.
14. 2+-binding proteins (polcalcins) involved in allergy. Eur. J. Biochem. 258:1998;454-459.
15. 2+-binding proteins. Plant Mol. Biol. 29:1995;1157-1165.
16. Okada T., Swoboda I., Bhalla P.L., Toriyama K., Singh M.B. Engineering of hypoallergenic mutants of the Brassica pollen allergen, Bra r 1, for immunotherapy. FEBS Letters. 434:1998;255-260.
17. Focke M., Hemmer W., Hayek B., Götz M., Jarisch R. Identification of allergens in oilseed rape (Brassica napus) pollen. Int. Arch. Allergy Immunol. 117:1998;105-112.
18. Rozwadowski K., Zhao R., Jackman L., Huebert T., Burkhart W.E., Hemmingsen S.M., et al. Characterization and immunolocalization of a cytosolic calcium-binding protein from Brassica napus and Arabidopsis pollen. Plant Physiol. 120:1999;787-797.
19. Niederberger V., Hayek B., Vrtala S., Laffer S., Twardosz A., Vangelista L., et al. Calcium-dependent immunoglobulin E recognition of the apo- and calcium-bound form of a cross-reactive two EF-hand timothy grass pollen allergen, Phl p 7. FASEB J. 13:1999;843-856.
20. 2+ binding protein as a new Bermuda grass pollen allergen Cyn d 7: IgE cross-reactivity with oilseed rape pollen allergen Bra r 1. Int. Arch. Allergy Immunol. 114:1997;265-271.
21. Suphioglu C., Ferreira F., Knox R.B. Molecular cloning and immunological characterisation of Cyn d 7, a novel calcium-binding allergen from Bermuda grass pollen. FEBS Letters. 402:1997;167-172.
22. King T.P., Hoffman D., Løwenstein H., Marsh D.G., Platts-Mills T.A.E., Thomas W. Allergen nomenclature. Int. Arch. Allergy Immunol. 105:1994;224-233.
23. Valenta R., Hayek B., Seiberler S., Bugajska-Schretter A., Niederberger V., Twardosz A., et al. Calcium-binding allergens: from plants to man. Int. Arch. Allergy Immunol. 117:1998;160-166.
24. 2+-binding protein, Bra r 1, in anthers and pollen tubes. Plant Cell Physiol. 40:1999;1243-1252.
25. Okada T., Sasaki Y., Ohta R., Onozuka N., Toriyama K. Expression of Bra r 1 gene in transgenic tobacco and Bra r 1 promoter activity in pollen of various plant species. Plant Cell Physiol. 41:2000;757-766.
26. Verdino P., Westritschnig K., Valenta R., Keller W. The cross-reactive calcium-binding pollen allergen, Phl p 7, reveals a novel dimer assembly. EMBO J. 21:2002;5007-5016.
27. Grote M., Hayek B., Reichelt R., Kraft D., Valenta R. Immunogold electron microscopic localization of the cross-reactive two-EF-Hand calcium-binding birch pollen allergen Bet v 4 in dry and rehydrated birch pollen. Int. Arch. Allergy Immunol. 120:1999;287-294.
28. Tinghino R., Twardosz A., Barletta B., Puggioni E.M.R., Iacovacci P., Butteroni C., et al. Molecular, structural, and immunologic relationships between different families of recombinant calcium-binding pollen allergens. J. Allergy Clin. Immunol. 109:2002;314-320.
29. 2+-binding motifs involved in the immunoglobulin E-binding of allergens? Olive pollen allergens as model of study. Clin. Expt. Allergy. 32:2002;1476-1483.
30. Lewit-Bentley A., Réty S. EF-hand calcium-binding proteins. Curr. Opin. Struct. Biol. 10:2000;637-643.
31. 15N spectra of larger proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry. 29:1990;4659-4667.
32. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
33. Brünger A.T., Clore G.M., Gronenborn A.M., Saffrich R., Nilges M. Assessing the quality of solution nuclear magnetic resonance structures by complete cross-validation. Science. 261:1993;328-331.
34. Kuboniwa H., Tjandra N., Grzesiek S., Ren H., Klee C.B., Bax A. Solution structure of calcium-free calmodulin. Nature Struct. Biol. 2:1995;768-776.
35. Woessner D.E. Nuclear spin relaxation in ellipsoids undergoing rotational Brownian motion. J. Chem. Phys. 37:1962;647-654.
36. Wilkins D.K., Grimshaw S.B., Receveur V., Dobson C.M., Jones J.A., Smith L.J. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry. 38:1999;16424-16431.
37. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:2000;1606-1619.
38. Schuck P., Perugini M.A., Gonzales N.R., Howlett G.J., Schubert D. Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82:2002;1096-1111.
39. Lauber T., Nourse A., Schulz A., Marx U.C. Native and recombinant proguanylin feature identical biophysical properties and are monomeric in solution. Biochemistry. 41:2002;14602-14612.
40. Perrin F. Mouvement brownien d'un ellipsoïde (I). Dispersion diélectrique pour des molécules ellipsoïdales. J. Phys. Radium. 5:1934;497-511.
41. Perrin F. Mouvement brownien d'un ellipsoïde (II). Rotation libre et dépolarisation des fluorescences. Translation et diffusion de molécules ellipsoïdales. J. Phys. Radium. 7:1936;1-11.
42. 2O. J. Phys. Chem. B103:1999;1991-1994.
43. Håkansson M., Svensson A., Fast J., Linse S. An extended hydrophobic core induces EF-hand swapping. Protein Sci. 10:2001;927-933.
44. 9k. J. Mol. Biol. 231:1993;711-734.
45. 15N-NMR relaxation measurements. Eur. J. Biochem. 230:1995;1014-1024.
46. Zhang M., Tanaka T., Ikura M. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nature Struct. Biol. 9:1995;758-767.
47. Finn B.E., Evenäs J., Drakenberg T., Waltho J.P., Thulin E., Forsén S. Calcium-induced structural changes and domain autonomy in calmodulin. Nature Struct. Biol. 9:1995;777-783.
48. 2+-binding proteins. Nature Struct. Biol. 1:1994;239-245.
49. Hoeflich K.P., Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell. 108:2002;739-742.
50. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning. A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
51. Meyer O., Schlegel H.G. Biology of aerobic carbon monoxide-oxidizing bacteria. Annu. Rev. Microbiol. 37:1983;277-310.
52. Bax A., Grzesiek S. Methodological advances in protein NMR. Acc. Chem. Res. 26:1993;131-138.
53. Sattler M., Schleucher J., Griesinger C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. NMR Spectrosc. 34:1999;93-158.
54. NC′ scalar couplings. J. Am. Chem. Soc. 121:1999;1601-1602.
55. 15N-labeled proteins by sensitivity-enhanced NMR spectroscopy. J. Biomol. NMR. 17:2000;79-82.
56. Hansen M.R., Mueller L., Pardi A. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nature Struct. Biol. 5:1998;1065-1074.
57. Ottiger M., Delaglio F., Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR Spectra. J. Magn. Reson. 131:1998;373-378.
58. 1H groups with pulsed-field gradients and preservation of coherence pathways. J. Magn. Reson. A111:1994;121-126.
59. Jones J.A., Wilkins D.K., Smith L.J., Dobson C.M. Characterisation of protein unfolding by NMR diffusion measurements. J. Biomol. NMR. 10:1997;199-203.
60. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:1995;277-293.
61. Johnson B.A., Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR. 4:1994;603-614.
62. Markley J.L., Bax A., Arata Y., Hilbers C.W., Kaptein R., Sykes B.D., et al. Recommendations for the presentation of NMR structures of proteins and nucleic acids (IUPAC recommendations 1998). Pure Appl. Chem. 70:1998;117-142.
63. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;Wiley, New York.
64. 13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nature Struct. Biol. 4:1997;732-738.
65. Clore G.M., Gronenborn A.M., Bax A. A robust method for determining the magnitude of the fully asymmetric alignment tensor of oriented macromolecules in the absence of structural information. J. Magn. Reson. 133:1998;216-221.
66. Kharrat A., Macias M.J., Gibson T.J., Nilges M., Pastore A. Structure of the dsRNA binding domain of E. coli RNase III. EMBO J. 14:1995;3572-3584.
67. Holak T.A., Nilges M., Oschkinat H. Improved strategies for the determination of protein structures from NMR data: the solution structure of acyl carrier protein. FEBS Letters. 242:1989;218-224.
68. Schwieters C.D., Kuszewski J.J., Tjandra N., Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160:2003;65-73.
69. Brünger A.T. X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. 1992;Yale University Press, New Haven.
70. Engh R.A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
71. Powell M.J.D. Restart procedures for the conjugate gradient method. Math. Progr. 12:1977;241-254.
72. Rao S.T., Wu S., Satyshur K.A., Ling K.-Y., Kung C., Sundaralingam M. Structure of Paramecium tetraurelia calmodulin at 1.8 Å resolution. Protein Sci. 2:1993;436-447.
73. Ban C.B., Ramakrishnan B., Ling K.-Y., Kung C., Sundaralingam M. Structure of the recombinant Paramecium tetraurelia calmodulin at 1.68 Å resolution. Acta Crystallog. sect. D. 50:1994;50-63.
74. Kuszewski J.J., Clore G.M. Sources of and solutions to problems in the refinement of protein NMR structures against torsion angle potentials of mean force. J. Magn. Reson. 146:2000;249-254.
75. Neudecker P., Sticht H., Rösch P. Improving the efficiency of the Gaussian conformational database potential for the refinement of protein and nucleic acid structures. J. Biomol. NMR. 21:2001;373-375.
76. β chemical shifts on protein structure determination by NMR. J. Magn. Reson. B106:1995;92-96.
77. 15N random coil NMR chemical shifts of the common amino acids. I. Investigation of nearest-neighbor effects. J. Biomol. NMR. 5:1995;67-81.
78. Kuszewski J.J., Gronenborn A.M., Clore G.M. Improving the packing and accuracy of NMR structures with a pseudopotential for the radius of gyration. J. Am. Chem. Soc. 121:1999;2337-2338.
79. Lefèvre J.-F., Dayie K.T., Peng J.W., Wagner G. Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry. 35:1996;2674-2686.
80. Bracken C., Carr P.A., Cavanagh J., Palmer A.G. Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: implications for the entropy of association with DNA. J. Mol. Biol. 285:1999;2133-2146.
81. 15N relaxation parameters. J. Biomol. NMR. 20:2001;149-165.
82. Dosset P., Hus J.-C., Blackledge M., Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR. 16:2000;23-28.
83. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:1985;76-85.
84. Laue T.M., Shah B.D., Ridgeway T.M., Pelletier S.L. Analytical Ultracentrifugation in Biochemistry and Polymer Science. 1992;The Royal Society of Chemistry, Cambridge. pp. 90-125.
85. Perkins S.J. X-ray and neutron scattering analyses of hydration shells: a molecular interpretation based on sequence predictions and modelling fits. Biophys. Chem. 93:2001;129-139.
86. Ansevin A.T., Roark D.E., Yphantis D.A. Improved ultracentrifuge cells for high-speed sedimentation equilibrium studies with interference optics. Anal. Biochem. 34:1970;237-261.
87. McRorie D.K., Voelker P. Self-association Systems in the Analytical Ultracentrifuge. 1993;Beckman Instruments, Inc, Fullerton, CA.
88. Laue T.M., Stafford W.F. Modern applications of analytical ultracentrifugation. Annu. Rev. Biophys. Biomol. Struct. 28:1999;75-100.
89. Schmid F.X. Spectral methods of characterizing protein conformation and conformational changes. Creighton T.E. Protein Structure: A Practical Approach. 1990;251-285 IRL Press, Oxford.
90. 1 are strongly altered by the replacement of cis-proline 39 with alanine. J. Mol. Biol. 231:1993;897-912.
91. Barton G.J. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 6:1993;37-40.
92. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
93. Merritt E.A., Murphy M.E.P. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.
94. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.