Identification of Critical Amino Acids in an immunodominant IgE epitope of pen c 13, a major allergen from penicillium citrinum

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Chen, Jui Chieh ^a   Chiu, Li Li ^a   Lee, Kuang Lun ^b   Huang, Wei Ning ^c   Chuang, Jiing Guang ^a   Liao, Hsin Kai ^a   Chow, Lu Ping ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c YUANPEI UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; FUNGUS ANTIGEN; IMMUNOGLOBULIN E; PEN C 13; SERINE PROTEINASE; UNCLASSIFIED DRUG; AMINO ACID; EPITOPE; FUNGAL PROTEIN; PEN N 13 ALLERGEN;

ADULT; AGED; ALLERGY; AMINO ACID ANALYSIS; ANTIBODY COMBINING SITE; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CHILD; CLIENT SERVER APPLICATION; COMPUTER MODEL; COMPUTER PREDICTION; CONTROLLED STUDY; EPITOPE MAPPING; EXPERIMENTAL STUDY; FEMALE; FUNGUS ALLERGY; HUMAN; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; MOLECULAR MODEL; NONHUMAN; PENICILLIUM CITRINUM; PEPTIDE ANALYSIS; SCHOOL CHILD; SCREENING TEST; SITE DIRECTED MUTAGENESIS; SKIN TEST; THEORETICAL STUDY; CHEMISTRY; HYPERSENSITIVITY; IMMUNOLOGY; METABOLISM; METHODOLOGY; PENICILLIUM;

PENICILLIUM CITRINUM;

ALLERGENS; AMINO ACIDS; ANTIGENS, FUNGAL; BINDING SITES, ANTIBODY; EPITOPE MAPPING; EPITOPES, B-LYMPHOCYTE; FUNGAL PROTEINS; HUMANS; HYPERSENSITIVITY; IMMUNODOMINANT EPITOPES; IMMUNOGLOBULIN E; MUTAGENESIS, SITE-DIRECTED; PENICILLIUM;

EID: 84859626384     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034627     Document Type: Article

References (68)

1. Horner WE, Helbling A, Salvaggio JE, Lehrer SB, (1995) Fungal allergens. Clin Microbiol Rev 8: 161-179.
2. Kurup VP, Shen HD, Banerjee B, (2000) Respiratory fungal allergy. Microbes Infect 2: 1101-1110.
3. Yu CJ, Chen YM, Su SN, Forouhar F, Lee SH, et al. (2002) Molecular and immunological characterization and IgE epitope mapping of Pen n 18, a major allergen of Penicillium notatum. Biochem J 363: 707-715.
4. Simon-Nobbe B, Denk U, Poll V, Rid R, Breitenbach M, (2008) The spectrum of fungal allergy. Int Arch Allergy Immunol 145: 58-86.
5. Shen HD, Lin WL, Liaw SF, Tam MF, Han SH, (1997) Characterization of the 33-kilodalton major allergen of Penicillium citrinum by using MoAbs and N-terminal amino acid sequencing. Clin Exp Allergy 27: 79-86.
6. Su NY, Yu CJ, Shen HD, Pan FM, Chow LP, (1999) Pen c 1, a novel enzymic allergen protein from Penicillium citrinum. Purification, characterization, cloning and expression. Eur J Biochem 261: 115-123.
7. Chiu LL, Perng DW, Yu CH, Su SN, Chow LP, (2007) Mold allergen, Pen c 13, induces IL-8 expression in human airway epithelial cells by activating protease-activated receptor 1 and 2. J Immunol 178: 5237-5244.
8. Chiu LL, Lee KL, Lin YF, Chu CY, Su SN, et al. (2008) Secretome analysis of novel IgE-binding proteins from Penicillium citrinum. Proteomics Clin Appl 2: 33-45.
9. Chen JC, Chuang JG, Su YY, Chiang BL, Lin YS, et al. (2011) The protease allergen Pen c 13 induces allergic airway inflammation and changes in epithelial barrier integrity and function in a murine model. J Biol Chem 286: 26667-26679.
10. Sokol CL, Barton GM, Farr AG, Medzhitov R, (2008) A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat Immunol 9: 310-318.
11. Kouzaki H, O'Grady SM, Lawrence CB, Kita H, (2009) Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 183: 1427-1434.
12. Paul WE, Zhu J, (2010) How are T(H)2-type immune responses initiated and amplified? Nat Rev Immunol 10: 225-235.
13. Vrtala S, Ball T, Spitzauer S, Pandjaitan B, Suphioglu C, et al. (1998) Immunization with purified natural and recombinant allergens induces mouse IgG1 antibodies that recognize similar epitopes as human IgE and inhibit the human IgE-allergen interaction and allergen-induced basophil degranulation. J Immunol 160: 6137-6144.
14. Mothes N, Heinzkill M, Drachenberg KJ, Sperr WR, Krauth MT, et al. (2003) Allergen-specific immunotherapy with a monophosphoryl lipid A-adjuvanted vaccine: reduced seasonally boosted immunoglobulin E production and inhibition of basophil histamine release by therapy-induced blocking antibodies. Clin Exp Allergy 33: 1198-1208.
15. Nouri-Aria KT, Wachholz PA, Francis JN, Jacobson MR, Walker SM, et al. (2004) Grass pollen immunotherapy induces mucosal and peripheral IL-10 responses and blocking IgG activity. J Immunol 172: 3252-3259.
16. Wachholz PA, Durham SR, (2004) Mechanisms of immunotherapy: IgG revisited. Curr Opin Allergy Clin Immunol 4: 313-318.
17. Reisinger J, Horak F, Pauli G, van Hage M, Cromwell O, et al. (2005) Allergen-specific nasal IgG antibodies induced by vaccination with genetically modified allergens are associated with reduced nasal allergen sensitivity. J Allergy Clin Immunol 116: 347-354.
18. Ball T, Linhart B, Sonneck K, Blatt K, Herrmann H, et al. (2009) Reducing allergenicity by altering allergen fold: a mosaic protein of Phl p 1 for allergy vaccination. Allergy 64: 569-580.
19. Campana R, Vrtala S, Maderegger B, Jertschin P, Stegfellner G, et al. (2010) Hypoallergenic derivatives of the major birch pollen allergen Bet v 1 obtained by rational sequence reassembly. J Allergy Clin Immunol 126: 1024-1031, 1031 e1021-1028.
20. Saarne T, Neimert-Andersson T, Gronlund H, Jutel M, Gafvelin G, et al. (2011) Treatment with a Fel d 1 hypoallergen reduces allergic responses in a mouse model for cat allergy. Allergy 66: 255-263.
21. Sharma V, Singh BP, Arora N, (2011) Cur l 3, a Major Allergen of Curvularia Lunata Derived Short Synthetic Peptides Show Promise for Successful Immunotherapy. Am J Respir Cell Mol Biol.
22. Chow LP, Liu SL, Yu CJ, Liao HK, Tsai JJ, et al. (2000) Identification and expression of an allergen Asp f 13 from Aspergillus fumigatus and epitope mapping using human IgE antibodies and rabbit polyclonal antibodies. Biochem J 346 (Pt 2): 423-431.
23. Kammerer R, Kettner A, Chvatchko Y, Dufour N, Tiercy JM, et al. (1997) Delineation of PLA2 epitopes using short or long overlapping synthetic peptides: interest for specific immunotherapy. Clin Exp Allergy 27: 1016-1026.
24. Shreffler WG, Lencer DA, Bardina L, Sampson HA, (2005) IgE and IgG4 epitope mapping by microarray immunoassay reveals the diversity of immune response to the peanut allergen, Ara h 2. J Allergy Clin Immunol 116: 893-899.
25. Hantusch B, Krieger S, Untersmayr E, Scholl I, Knittelfelder R, et al. (2004) Mapping of conformational IgE epitopes on Phl p 5a by using mimotopes from a phage display library. J Allergy Clin Immunol 114: 1294-1300.
26. Lai HY, Tam MF, Chou H, Lee SS, Tai HY, et al. (2004) Molecular and structural analysis of immunoglobulin E-binding epitopes of Pen ch 13, an alkaline serine protease major allergen from Penicillium chrysogenum. Clin Exp Allergy 34: 1926-1933.
27. Ferreira F, Ebner C, Kramer B, Casari G, Briza P, et al. (1998) Modulation of IgE reactivity of allergens by site-directed mutagenesis: potential use of hypoallergenic variants for immunotherapy. FASEB J 12: 231-242.
28. Vrtala S, Fohr M, Campana R, Baumgartner C, Valent P, et al. (2011) Genetic engineering of trimers of hypoallergenic fragments of the major birch pollen allergen, Bet v 1, for allergy vaccination. Vaccine 29: 2140-2148.
29. Niespodziana K, Focke-Tejkl M, Linhart B, Civaj V, Blatt K, et al. (2011) A hypoallergenic cat vaccine based on Fel d 1-derived peptides fused to hepatitis B PreS. J Allergy Clin Immunol 127: 1562-1570 e1566.
30. Ivanciuc O, Schein CH, Garcia T, Oezguen N, Negi SS, et al. (2009) Structural analysis of linear and conformational epitopes of allergens. Regul Toxicol Pharmacol 54: S11-19.
31. Pomes A, (2010) Relevant B cell epitopes in allergic disease. Int Arch Allergy Immunol 152: 1-11.
32. Robotham JM, Teuber SS, Sathe SK, Roux KH, (2002) Linear IgE epitope mapping of the English walnut (Juglans regia) major food allergen, Jug r 1. J Allergy Clin Immunol 109: 143-149.
33. Garcia-Casado G, Pacios LF, Diaz-Perales A, Sanchez-Monge R, Lombardero M, et al. (2003) Identification of IgE-binding epitopes of the major peach allergen Pru p 3. J Allergy Clin Immunol 112: 599-605.
34. Chan SL, Ong TC, Gao YF, Tiong YS, de Wang Y, et al. (2008) Nuclear magnetic resonance structure and IgE epitopes of Blo t 5, a major dust mite allergen. J Immunol 181: 2586-2596.
35. Larsen JE, Lund O, Nielsen M, (2006) Improved method for predicting linear B-cell epitopes. Immunome Res 2: 2.
36. Bui HH, Sidney J, Li W, Fusseder N, Sette A, (2007) Development of an epitope conservancy analysis tool to facilitate the design of epitope-based diagnostics and vaccines. BMC Bioinformatics 8: 361.
37. Sharma V, Singh BP, Gaur SN, Pasha S, Arora N, (2009) Bioinformatics and immunologic investigation on B and T cell epitopes of Cur l 3, a major allergen of Curvularia lunata. J Proteome Res 8: 2650-2655.
38. Rapin N, Lund O, Bernaschi M, Castiglione F, (2010) Computational immunology meets bioinformatics: the use of prediction tools for molecular binding in the simulation of the immune system. PLoS One 5: e9862.
39. Salimi N, Fleri W, Peters B, Sette A, (2010) Design and utilization of epitope-based databases and predictive tools. Immunogenetics 62: 185-196.
40. Durham SR, Till SJ, (1998) Immunologic changes associated with allergen immunotherapy. J Allergy Clin Immunol 102: 157-164.
41. Durham SR, Walker SM, Varga EM, Jacobson MR, O'Brien F, et al. (1999) Long-term clinical efficacy of grass-pollen immunotherapy. N Engl J Med 341: 468-475.
42. Moller C, Dreborg S, Ferdousi HA, Halken S, Host A, et al. (2002) Pollen immunotherapy reduces the development of asthma in children with seasonal rhinoconjunctivitis (the PAT-study). J Allergy Clin Immunol 109: 251-256.
43. Larche M, Akdis CA, Valenta R, (2006) Immunological mechanisms of allergen-specific immunotherapy. Nat Rev Immunol 6: 761-771.
44. Liang L, Meng Z, Ye F, Yang J, Liu S, et al. (2010) The crystal structures of two cuticle-degrading proteases from nematophagous fungi and their contribution to infection against nematodes. FASEB J 24: 1391-1400.
45. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
46. Yang X, Yu X, (2009) An introduction to epitope prediction methods and software. Rev Med Virol 19: 77-96.
47. Chou H, Tam MF, Chiang CH, Chou CT, Tai HY, et al. (2011) Transaldolases are novel and immunoglobulin E cross-reacting fungal allergens. Clin Exp Allergy 41: 739-749.
48. Chou H, Tam MF, Lee SS, Tang RB, Lin TH, et al. (2011) Asp159 is a critical core amino acid of an IgE-binding and cross-reactive epitope of a dust mite allergen Der f 7. Mol Immunol 48: 2130-2134.
49. Trevino MA, Palomares O, Castrillo I, Villalba M, Rodriguez R, et al. (2008) Solution structure of the C-terminal domain of Ole e 9, a major allergen of olive pollen. Protein Sci 17: 371-376.
50. Razzera G, Gadermaier G, de Paula V, Almeida MS, Egger M, et al. (2010) Mapping the interactions between a major pollen allergen and human IgE antibodies. Structure 18: 1011-1021.
51. Niemi M, Jylha S, Laukkanen ML, Soderlund H, Makinen-Kiljunen S, et al. (2007) Molecular interactions between a recombinant IgE antibody and the beta-lactoglobulin allergen. Structure 15: 1413-1421.
52. Padavattan S, Schirmer T, Schmidt M, Akdis C, Valenta R, et al. (2007) Identification of a B-cell epitope of hyaluronidase, a major bee venom allergen, from its crystal structure in complex with a specific Fab. J Mol Biol 368: 742-752.
53. Karisola P, Mikkola J, Kalkkinen N, Airenne KJ, Laitinen OH, et al. (2004) Construction of hevein (Hev b 6.02) with reduced allergenicity for immunotherapy of latex allergy by comutation of six amino acid residues on the conformational IgE epitopes. J Immunol 172: 2621-2628.
54. Chan SL, Ong ST, Ong SY, Chew FT, Mok YK, (2006) Nuclear magnetic resonance structure-based epitope mapping and modulation of dust mite group 13 allergen as a hypoallergen. J Immunol 176: 4852-4860.
55. Satoh R, Koyano S, Takagi K, Nakamura R, Teshima R, (2010) Identification of an IgE-binding epitope of a major buckwheat allergen, BWp16, by SPOTs assay and mimotope screening. Int Arch Allergy Immunol 153: 133-140.
56. Li M, Gustchina A, Alexandratos J, Wlodawer A, Wunschmann S, et al. (2008) Crystal structure of a dimerized cockroach allergen Bla g 2 complexed with a monoclonal antibody. J Biol Chem 283: 22806-22814.
57. Beezhold DH, Hickey VL, Sussman GL, (2001) Mutational analysis of the IgE epitopes in the latex allergen Hev b 5. J Allergy Clin Immunol 107: 1069-1076.
58. Wiedermann U, Herz U, Baier K, Vrtala S, Neuhaus-Steinmetz U, et al. (2001) Intranasal treatment with a recombinant hypoallergenic derivative of the major birch pollen allergen Bet v 1 prevents allergic sensitization and airway inflammation in mice. Int Arch Allergy Immunol 126: 68-77.
59. Norman PS, Ohman JL Jr, Long AA, Creticos PS, Gefter MA, et al. (1996) Treatment of cat allergy with T-cell reactive peptides. Am J Respir Crit Care Med 154: 1623-1628.
60. von Garnier C, Astori M, Kettner A, Dufour N, Heusser C, et al. (2000) Allergen-derived long peptide immunotherapy down-regulates specific IgE response and protects from anaphylaxis. Eur J Immunol 30: 1638-1645.
61. Oldfield WL, Kay AB, Larche M, (2001) Allergen-derived T cell peptide-induced late asthmatic reactions precede the induction of antigen-specific hyporesponsiveness in atopic allergic asthmatic subjects. J Immunol 167: 1734-1739.
62. Campbell JD, Buckland KF, McMillan SJ, Kearley J, Oldfield WL, et al. (2009) Peptide immunotherapy in allergic asthma generates IL-10-dependent immunological tolerance associated with linked epitope suppression. J Exp Med 206: 1535-1547.
63. Holm J, Gajhede M, Ferreras M, Henriksen A, Ipsen H, et al. (2004) Allergy vaccine engineering: epitope modulation of recombinant Bet v 1 reduces IgE binding but retains protein folding pattern for induction of protective blocking-antibody responses. J Immunol 173: 5258-5267.
64. Gafvelin G, Parmley S, Neimert-Andersson T, Blank U, Eriksson TL, et al. (2007) Hypoallergens for allergen-specific immunotherapy by directed molecular evolution of mite group 2 allergens. J Biol Chem 282: 3778-3787.
65. Muller U, Akdis CA, Fricker M, Akdis M, Blesken T, et al. (1998) Successful immunotherapy with T-cell epitope peptides of bee venom phospholipase A2 induces specific T-cell anergy in patients allergic to bee venom. J Allergy Clin Immunol 101: 747-754.
66. Vrtala S, Akdis CA, Budak F, Akdis M, Blaser K, et al. (2000) T cell epitope-containing hypoallergenic recombinant fragments of the major birch pollen allergen, Bet v 1, induce blocking antibodies. J Immunol 165: 6653-6659.
67. Oldfield WL, Larche M, Kay AB, (2002) Effect of T-cell peptides derived from Fel d 1 on allergic reactions and cytokine production in patients sensitive to cats: a randomised controlled trial. Lancet 360: 47-53.
68. Karamloo F, Schmid-Grendelmeier P, Kussebi F, Akdis M, Salagianni M, et al. (2005) Prevention of allergy by a recombinant multi-allergen vaccine with reduced IgE binding and preserved T cell epitopes. Eur J Immunol 35: 3268-3276.