Persistence and evolution of allergen-specific IgE repertoires during subcutaneous specific immunotherapy

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 5, 2016, Pages 1535-1544

  Levin, Mattias ^a   King, Jasmine J ^b,c   Glanville, Jacob ^b   Jackson, Katherine J L ^c   Looney, Timothy J ^c   Hoh, Ramona A ^c   Mari, Adriano ^d,e   Andersson, Morgan ^f   Greiff, Lennart ^f   Fire, Andrew Z ^b,c   Boyd, Scott D ^c   Ohlin, Mats ^a  

^a LUND UNIVERSITY   (Sweden)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^e Assoct Centers for Molecular Allergology   (Italy)

^f LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Aeroallergens; allergen specific antibodies; clonotype evolution; IgE; immunoglobulin class switch; local immunity; repertoire; specific immunotherapy

Indexed keywords

ALLERGEN; ANTIBODY; IMMUNOGLOBULIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G4; IMMUNOGLOBULIN G;

ADULT; ARTICLE; B LYMPHOCYTE; BLOOD; BLOOD SAMPLING; COMBINATORIAL LIBRARY; DNA SEQUENCE; FEMALE; GENE SEQUENCE; HEAVY CHAIN; HUMAN; HUMAN TISSUE; MALE; NASAL BIOPSY; NOSE MUCOSA; PRIORITY JOURNAL; SUBCUTANEOUS IMMUNOTHERAPY; DESENSITIZATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HYPERSENSITIVITY; IMMUNOLOGY; MIDDLE AGED; SUBCUTANEOUS DRUG ADMINISTRATION; YOUNG ADULT;

ADULT; ALLERGENS; B-LYMPHOCYTES; DESENSITIZATION, IMMUNOLOGIC; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; HYPERSENSITIVITY; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INJECTIONS, SUBCUTANEOUS; MALE; MIDDLE AGED; NASAL MUCOSA; YOUNG ADULT;

EID: 84964859585     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.09.027     Document Type: Article

References (51)

1. H.J. Gould, B.J. Sutton, A.J. Beavil, R.L. Beavil, N. McCloskey, H.A. Coker, and et al. The biology of IGE and the basis of allergic disease Annu Rev Immunol 21 2003 579 628
2. H.J. Gould, and B.J. Sutton IgE in allergy and asthma today Nat Rev Immunol 8 2008 205 217
3. H. Floistrup, J. Swartz, A. Bergstrom, J.S. Alm, A. Scheynius, M. van Hage, and et al. Allergic disease and sensitization in Steiner school children J Allergy Clin Immunol 117 2006 59 66
4. J. Hellgren, A. Cervin, S. Nordling, A. Bergman, and L.O. Cardell Allergic rhinitis and the common cold-high cost to society Allergy 65 2010 776 783
5. S.R. Durham, S.M. Walker, E.M. Varga, M.R. Jacobson, F. O'Brien, W. Noble, and et al. Long-term clinical efficacy of grass-pollen immunotherapy N Engl J Med 341 1999 468 475
6. M. Larche, C.A. Akdis, and R. Valenta Immunological mechanisms of allergen-specific immunotherapy Nat Rev Immunol 6 2006 761 771
7. C.S. Hankin, L. Cox, and A. Bronstone The health economics of allergen immunotherapy Immunol Allergy Clin N Am 31 2011 325 341
8. L. Noon Prophylactic inoculation against hay fever Lancet 1 1911 1572 1573
9. C.A. Akdis Therapies for allergic inflammation: refining strategies to induce tolerance Nat Med 18 2012 736 749
10. J.N. Francis, S.J. Till, and S.R. Durham Induction of IL-10(+)CD4(+)CD25(+) T cells by grass pollen immunotherapy J Allergy Clin Immunol 111 2003 1255 1261
11. M.H. Shamji, and S.R. Durham Mechanisms of immunotherapy to aeroallergens Clin Exp Allergy 41 2011 1235 1246
12. O.U. Soyer, M. Akdis, J. Ring, H. Behrendt, R. Crameri, R. Lauener, and et al. Mechanisms of peripheral tolerance to allergens Allergy 68 2013 161 170
13. E. Gadermaier, J. Staikuniene, S. Scheiblhofer, J. Thalhamer, M. Kundi, K. Westritschnig, and et al. Recombinant allergen-based monitoring of antibody responses during injection grass pollen immunotherapy and after 5 years of discontinuation Allergy 66 2011 1174 1182
14. G.J. Gleich, E.M. Zimmermann, L.L. Henderson, and J.W. Yunginger Effect of immunotherapy on immunoglobulin-E and immunoglobulin-G antibodies to ragweed antigens - a 6-year prospective study J Allergy Clin Immunol 70 1982 261 271
15. E. Gadermaier, M. Levin, S. Flicker, and M. Ohlin The human IgE repertoire Int Arch Allergy Immunol 163 2014 77 91
16. U. Andreasson, S. Flicker, M. Lindstedt, R. Valenta, L. Greiff, M. Korsgren, and et al. The human IgE-encoding transcriptome to assess antibody repertoires and repertoire evolution J Mol Biol 362 2006 212 227
17. J.M. Davies, and R.E. O'Hehir VH gene usage in immunoglobulin E responses of seasonal rhinitis patients allergic to grass pollen is oligoclonal and antigen driven Clin Exp Allergy 34 2004 429 436
18. D.G. Efremov, F.D. Batista, and O.R. Burrone Molecular analysis of Ige H-chain transcripts expressed in-vivo by peripheral-blood lymphocytes from normal and atopic individuals J Immunol 151 1993 2195 2207
19. S. Kerzel, T. Rogosch, B. Struecker, R.F. Maier, and M. Zemlin IgE transcripts in the circulation of allergic children reflect a classical antigen-driven B cell response and not a superantigen-like activation J Immunol 185 2010 2253 2260
20. L.H. Christensen, J. Holm, G. Lund, E. Riise, and K. Lund Several distinct properties of the IgE repertoire determine effector cell degranulation in response to allergen challenge J Allergy Clin Immunol 122 2008 298 304
21. G. Lund, N. Willumsen, J. Holm, L.H. Christensen, P.A. Wurtzen, and K. Lund Antibody repertoire complexity and effector cell biology determined by assays for IgE-mediated basophil and T-cell activation J Immunol Methods 383 2012 4 20
22. Y.C. Wu, L.K. James, J.A. Vander Heiden, M. Uduman, S.R. Durham, S.H. Kleinstein, and et al. Influence of seasonal exposure to grass pollen on local and peripheral blood IgE repertoires in patients with allergic rhinitis J Allergy Clin Immunol 134 2014 604 612
23. Y. Wang, K.J. Jackson, J. Davies, Z. Chen, B.A. Gaeta, J. Rimmer, and et al. IgE-associated IGHV genes from venom and peanut allergic individuals lack mutational evidence of antigen selection PLoS One 9 2014 e89730
24. D. Pomponi, G. Di Zenzo, D. Zennaro, V. Calabresi, R. Eming, S. Zuzzi, and et al. Detection of IgG and IgE reactivity to BP180 using the ISAC (R) microarray system Br J Dermatol 168 2013 1205 1214
25. M. Jutel, L. Jaeger, R. Suck, H. Meyer, H. Fiebig, and O. Cromwell Allergen-specific immunotherapy with recombinant grass pollen allergens J Allergy Clin Immunol 116 2005 608 613
26. P. Parameswaran, Y. Liu, K.M. Roskin, K.K. Jackson, V.P. Dixit, J.Y. Lee, and et al. Convergent antibody signatures in human dengue Cell Host Microbe 13 2013 691 700
27. I. Saggy, Y. Wine, L. Shefet-Carasso, L. Nahary, G. Georgiou, and I. Benhar Antibody isolation from immunized animals: comparison of phage display and antibody discovery via V gene repertoire mining Prot Eng Des Sel 25 2012 539 549
28. A. Horst, N. Hunzelmann, S. Arce, M. Herber, R.A. Manz, A. Radbrucht, and et al. Detection and characterization of plasma cells in peripheral blood: correlation of IgE(+) plasma cell frequency with IgE serum titre Clin Exp Immunol 130 2002 370 378
29. M.A. Berkowska, J.J. Heeringa, E. Hajdarbegovic, M. van der Burg, H.B. Thio, P.M. van Hagen, and et al. Human IgE(+) B cells are derived from T cell-dependent and T cell-independent pathways J Allergy Clin Immunol 134 2014 688 697
30. S.D. Boyd, B.A. Gaeta, K.J. Jackson, A.Z. Fire, E.L. Marshall, J.D. Merker, and et al. Individual variation in the germline Ig gene repertoire inferred from variable region gene rearrangements J Immunol 184 2010 6986 6992
31. S.D. Boyd, E.L. Marshall, J.D. Merker, J.M. Maniar, L.N. Zhang, B. Sahaf, and et al. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel V-D-J pyrosequencing Sci Transl Med 1 2009 12ra23
32. K.J. Jackson, Y. Liu, K.M. Roskin, J. Glanville, R.A. Hoh, K. Seo, and et al. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements Cell Host Microbe 16 2014 105 114
33. N. Jiang, J. He, J.A. Weinstein, L. Penland, S. Sasaki, X.S. He, and et al. Lineage structure of the human antibody repertoire in response to influenza vaccination Sci Transl Med 5 2013 193er8
34. C. Wang, Y. Liu, L.T. Xu, K.J. Jackson, K.M. Roskin, T.D. Pham, and et al. Effects of aging, cytomegalovirus infection, and EBV infection on human B cell repertoires J Immunol 192 2014 603 611
35. X.L. Wu, T.Q. Zhou, J. Zhu, B.S. Zhang, I. Georgiev, C. Wang, and et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing Science 333 2011 1593 1602
36. J. McCafferty, A.D. Griffiths, G. Winter, and D.J. Chiswell Phage antibodies-filamentous phage displaying antibody variable domains Nature 348 1990 552 554
37. V. Niederberger, J. Ring, J. Rakoski, S. Jager, S. Spitzauer, P. Valent, and et al. Antigens drive memory IgE responses in human allergy via the nasal mucosa Int Arch Allergy Immunol 142 2007 133 144
38. K. Marth, M. Novatchkova, M. Focke-Tejkl, S. Jenisch, S. Jager, D. Kabelitz, and et al. Tracing antigen signatures in the human IgE repertoire Mol Immunol 47 2010 2323 2329
39. H.A. Coker, H.E. Harries, G.K. Banfield, V.A. Carr, S.R. Durham, E. Chevretton, and et al. Biased use of V(H)5 IgE-positive B cells in the nasal mucosa in allergic rhinitis J Allergy Clin Immunol 116 2005 445 452
40. I. Dahlke, D.J. Nott, J. Ruhno, W.A. Sewell, and A.M. Collins Antigen selection in the IgE response of allergic and nonallergic individuals J Allergy Clin Immunol 117 2006 1477 1483
41. M. Levin, and M. Ohlin Inconclusive evidence for or against positive antigen selection in the shaping of human immunoglobulin E repertoires: A call for new approaches Int Arch Allergy Immunol 161 2013 122 126
42. E. Pratt, A.M. Collins, W.A. Sewell, and R.J. Harvey Antigen selection in IgE antibodies from individuals with chronic rhinosinusitis with nasal polyps Am J Rhinol Allergy 24 2010 416 421
43. L. Cameron, A.S. Gounni, S. Frenkiel, F. Lavigne, D. Vercelli, and Q. Hamid S epsilon S mu and S epsilon S gamma switch circles in human nasal mucosa following ex vivo allergen challenge: evidence for direct as well as sequential class switch recombination J Immunol 171 2003 3816 3822
44. H.A. Coker, S.R. Durham, and H.J. Gould Local somatic hypermutation and class switch recombination in the nasal mucosa of allergic rhinitis patients J Immunol 171 2003 5602 5610
45. P. Gevaert, K.T. Nouri-Aria, H. Wu, C.E. Harper, P. Takhar, D.J. Fear, and et al. Local receptor revision and class switching to IgE in chronic rhinosinusitis with nasal polyps Allergy 68 2013 55 63
46. P. Takhar, C.J. Corrigan, L. Smurthwaite, B.J. O'Connor, S.R. Durham, T.H. Lee, and et al. Class switch recombination to IgE in the bronchial mucosa of atopic and nonatopic patients with asthma J Allergy Clin Immunol 119 2007 213 218
47. P. Takhar, L. Smurthwaite, H.A. Coker, D.J. Fear, G.K. Banfield, V.A. Carr, and et al. Allergen drives class switching to IgE in the nasal mucosa in allergic rhinitis J Immunol 174 2005 5024 5032
48. A. Pomes Relevant B cell epitopes in allergic disease Int Arch Allergy Immunol 152 2010 1 11
49. L.K. James, H. Bowen, R.A. Calvert, T.S. Dodev, M.H. Shamji, A.J. Beavil, and et al. Allergen specificity of IgG(4)-expressing B cells in patients with grass pollen allergy undergoing immunotherapy J Allergy Clin Immunol 130 2012 663 670
50. P.J. Meijer, P.S. Andersen, M.H. Hansen, L. Steinaa, A. Jensen, J. Lantto, and et al. Isolation of human antibody repertoires with preservation of the natural heavy and light chain pairing J Mol Biol 358 2006 764 772
51. R.A. Hoh, S.A. Joshi, Y. Liu, C. Wang, K.M. Roskin, J.Y. Lee, and et al. Single B-cell deconvolution of peanut-specific antibody responses in allergic patients J Allergy Clin Immunol 137 2016 157 167