Improved efficacy of allergen-specific immunotherapy by JAK inhibition in a murine model of allergic asthma

PLoS ONE

Volumn 12, Issue 6, 2017, Pages

  Aguilar Pimentel, Antonio ^a   Graessel, Anke ^b   Alessandrini, Francesca ^b   Fuchs, Helmut ^a   Gailus Durner, Valerie ^a   Hrabě De Angelis, Martin ^a,b   Russkamp, Dennis ^b   Chaker, Adam ^b,c   Ollert, Markus ^d,e   Blank, Simon ^b   Gutermuth, Jan ^f   Schmidt Weber, Carsten B ^b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^f UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CXCL1 CHEMOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; JANUS KINASE; TOFACITINIB; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; CYTOKINE; OVALBUMIN; PIPERIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE;

ALLERGIC AIRWAY INFLAMMATION; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG MECHANISM; ENZYME INHIBITION; EOSINOPHIL; FEMALE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; IN VITRO STUDY; LUNG ALVEOLUS CELL; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; ANIMAL; ANTAGONISTS AND INHIBITORS; ASTHMA; C57BL MOUSE; CELL DIFFERENTIATION; DESENSITIZATION; DISEASE MODEL; DRUG EFFECTS; HUMAN; SECRETION (PROCESS);

ALLERGENS; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CELL DIFFERENTIATION; CYTOKINES; DESENSITIZATION, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; HUMANS; JANUS KINASES; MICE; MICE, INBRED C57BL; OVALBUMIN; PIPERIDINES; PYRIMIDINES; PYRROLES;

EID: 85020044391     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0178563     Document Type: Article

References (42)

1. Abramson MJ, Puy RM, Weiner JM. Injection allergen immunotherapy for asthma. The Cochrane database of systematic reviews. 2010;(8):CD001186. https://doi.org/10.1002/14651858.CD001186.pub2 PMID: 20687065.
2. Calderon MA, Alves B, Jacobson M, Hurwitz B, Sheikh A, Durham S. Allergen injection immunotherapy for seasonal allergic rhinitis. The Cochrane database of systematic reviews. 2007;(1):CD001936. https://doi.org/10.1002/14651858.CD001936.pub2 PMID: 17253469.
3. Frati F, Dell'Albani I, Incorvaia C. Long-term efficacy of allergen immunotherapy: what do we expect? Immunotherapy. 2013; 5(2):131-3. https://doi.org/10.2217/imt.12.154 PMID: 23413904.
4. Moote W, Kim H. Allergen-specific immunotherapy. Allergy, asthma, and clinical immunology: official journal of the Canadian Society of Allergy and Clinical Immunology. 2011; 7 Suppl 1:S5. https://doi.org/10.1186/1710-1492-7-S1-S5 PMID: 22166078.
5. Ring J, Alomar A, Bieber T, Deleuran M, Fink-Wagner A, Gelmetti C, et al. Guidelines for treatment of atopic eczema (atopic dermatitis) Part II. Journal of the European Academy of Dermatology and Venereology: JEADV. 2012; 26(9):1176-93. https://doi.org/10.1111/j.1468-3083.2012.04636.x PMID: 22813359.
6. Golden DB. Insect sting anaphylaxis. Immunology and allergy clinics of North America. 2007; 27 (2):261-72, vii. https://doi.org/10.1016/j.iac.2007.03.008 PMID: 17493502.
7. Akdis CA, Akdis M. Mechanisms of allergen-specific immunotherapy and immune tolerance to allergens. The World Allergy Organization journal. 2015; 8(1):17. https://doi.org/10.1186/s40413-015-0063-2 PMID: 26023323.
8. Chesne J, Schmidt-Weber CB, Esser von-Bieren J. The Use of Adjuvants for Enhancing Allergen Immunotherapy Efficacy. Immunology and allergy clinics of North America. 2016; 36(1):125-45. https://doi.org/10.1016/j.iac.2015.08.009 PMID: 26617231.
9. Schmidt-Weber CB, Blaser K. Immunological mechanisms of specific allergen immunotherapy. Inflammation & allergy drug targets. 2006; 5(1):15-21. PMID: 16613560.
10. Wu Z. Antigen specific immunotherapy generates CD27(+) CD35(+) tolerogenic dendritic cells. Cellular immunology. 2013; 283(1-2):75-80. https://doi.org/10.1016/j.cellimm.2013.06.014 PMID: 23887049.
11. Radulovic S, Jacobson MR, Durham SR, Nouri-Aria KT. Grass pollen immunotherapy induces Foxp3-expressing CD4+ CD25+ cells in the nasal mucosa. The Journal of allergy and clinical immunology. 2008; 121(6):1467-72, 72 e1. https://doi.org/10.1016/j.jaci.2008.03.013 PMID: 18423565.
12. Akdis M, Akdis CA. Mechanisms of allergen-specific immunotherapy: multiple suppressor factors at work in immune tolerance to allergens. The Journal of allergy and clinical immunology. 2014; 133 (3):621-31. https://doi.org/10.1016/j.jaci.2013.12.1088 PMID: 24581429.
13. Mantel PY, Kuipers H, Boyman O, Rhyner C, Ouaked N, Ruckert B, et al. GATA3-driven Th2 responses inhibit TGF-beta1-induced FOXP3 expression and the formation of regulatory T cells. PLoS biology. 2007; 5(12):e329. https://doi.org/10.1371/journal.pbio.0050329 PMID: 18162042.
14. van Amelsfort JM, van Roon JA, Noordegraaf M, Jacobs KM, Bijlsma JW, Lafeber FP, et al. Proinflammatory mediator-induced reversal of CD4+, CD25+ regulatory T cell-mediated suppression in rheumatoid arthritis. Arthritis and rheumatism. 2007; 56(3):732-42. https://doi.org/10.1002/art.22414 PMID: 17328044.
15. Miroux C, Morales O, Carpentier A, Dharancy S, Conti F, Boleslowski E, et al. Inhibitory effects of cyclosporine on human regulatory T cells in vitro. Transplantation proceedings. 2009; 41(8):3371-4. https://doi.org/10.1016/j.transproceed.2009.08.043 PMID: 19857752.
16. Dao Nguyen X, Robinson DS. Fluticasone propionate increases CD4CD25 T regulatory cell suppression of allergen-stimulated CD4CD25 T cells by an IL-10-dependent mechanism. The Journal of allergy and clinical immunology. 2004; 114(2):296-301. https://doi.org/10.1016/j.jaci.2004.04.048 PMID: 15316506.
17. Karagiannidis C, Akdis M, Holopainen P, Woolley NJ, Hense G, Ruckert B, et al. Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma. The Journal of allergy and clinical immunology. 2004; 114(6):1425-33. https://doi.org/10.1016/j.jaci.2004.07.014 PMID: 15577848.
18. Sewgobind VD, Quaedackers ME, van der Laan LJ, Kraaijeveld R, Korevaar SS, Chan G, et al. The Jak inhibitor CP-690,550 preserves the function of CD4CD25FoxP3 regulatory T cells and inhibits effector T cells. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2010; 10(8):1785-95. https://doi.org/10.1111/j.1600-6143.2010.03200.x PMID: 20626385.
19. O'Shea JJ, Schwartz DM, Villarino AV, Gadina M, McInnes IB, Laurence A. The JAK-STAT pathway: impact on human disease and therapeutic intervention. Annual review of medicine. 2015; 66:311-28. https://doi.org/10.1146/annurev-med-051113-024537 PMID: 25587654.
20. Roskoski R Jr. Janus kinase (JAK) inhibitors in the treatment of inflammatory and neoplastic diseases. Pharmacological research. 2016; 111:784-803. https://doi.org/10.1016/j.phrs.2016.07.038 PMID: 27473820.
21. He Y, Wong AY, Chan EW, Lau WC, Man KK, Chui CS, et al. Efficacy and safety of tofacitinib in the treatment of rheumatoid arthritis: a systematic review and meta-analysis. BMC musculoskeletal disorders. 2013; 14:298. https://doi.org/10.1186/1471-2474-14-298 PMID: 24139404.
22. Aguilar-Pimentel JA, Alessandrini F, Huster KM, Jakob T, Schulz H, Behrendt H, et al. Specific CD8 T cells in IgE-mediated allergy correlate with allergen dose and allergic phenotype. American journal of respiratory and critical care medicine. 2010; 181(1):7-16. https://doi.org/10.1164/rccm.200902-0190OC PMID: 19815810.
23. Fuchs H, Gailus-Durner V, Adler T, Aguilar-Pimentel JA, Becker L, Calzada-Wack J, et al. Mouse phenotyping. Methods. 2011; 53(2):120-35. https://doi.org/10.1016/j.ymeth.2010.08.006 PMID: 20708688.
24. Gailus-Durner V, Fuchs H, Becker L, Bolle I, Brielmeier M, Calzada-Wack J, et al. Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nature methods. 2005; 2 (6):403-4. https://doi.org/10.1038/nmeth0605-403 PMID: 15908916.
25. Alessandrini F, Schulz H, Takenaka S, Lentner B, Karg E, Behrendt H, et al. Effects of ultrafine carbon particle inhalation on allergic inflammation of the lung. The Journal of allergy and clinical immunology. 2006; 117(4):824-30. https://doi.org/10.1016/j.jaci.2005.11.046 PMID: 16630940.
26. Andre S, Tough DF, Lacroix-Desmazes S, Kaveri SV, Bayry J. Surveillance of antigen-presenting cells by CD4+ CD25+ regulatory T cells in autoimmunity: immunopathogenesis and therapeutic implications. The American journal of pathology. 2009; 174(5):1575-87. https://doi.org/10.2353/ajpath.2009.080987 PMID: 19349365.
27. Vissers JL, van Esch BC, Hofman GA, Kapsenberg ML, Weller FR, van Oosterhout AJ. Allergen immunotherapy induces a suppressive memory response mediated by IL-10 in a mouse asthma model. The Journal of allergy and clinical immunology. 2004; 113(6):1204-10. https://doi.org/10.1016/j.jaci.2004. 02.041 PMID: 15208606.
28. Meyer DM, Jesson MI, Li X, Elrick MM, Funckes-Shippy CL, Warner JD, et al. Anti-inflammatory activity and neutrophil reductions mediated by the JAK1/JAK3 inhibitor, CP-690,550, in rat adjuvant-induced arthritis. Journal of inflammation. 2010; 7:41. https://doi.org/10.1186/1476-9255-7-41 PMID: 20701804.
29. Ashino S, Takeda K, Li H, Taylor V, Joetham A, Pine PR, et al. Janus kinase 1/3 signaling pathways are key initiators of TH2 differentiation and lung allergic responses. The Journal of allergy and clinical immunology. 2014; 133(4):1162-74. https://doi.org/10.1016/j.jaci.2013.10.036 PMID: 24365136.
30. Lee JS, Campbell HD, Kozak CA, Young IG. The IL-4 and IL-5 genes are closely linked and are part of a cytokine gene cluster on mouse chromosome 11. Somatic cell and molecular genetics. 1989; 15 (2):143-52. PMID: 2784591.
31. Ikutani M, Yanagibashi T, Ogasawara M, Tsuneyama K, Yamamoto S, Hattori Y, et al. Identification of innate IL-5-producing cells and their role in lung eosinophil regulation and antitumor immunity. J Immunol. 2012; 188(2):703-13. https://doi.org/10.4049/jimmunol.1101270 PMID: 22174445.
32. Schmidt-Weber CB, Alexander SI, Henault LE, James L, Lichtman AH. IL-4 enhances IL-10 gene expression in murine Th2 cells in the absence of TCR engagement. Journal of immunology. 1999; 162 (1):238-44. PMID: 9886391.
33. Shirinbak S, Taher YA, Maazi H, Gras R, van Esch BC, Henricks PA, et al. Suppression of Th2-driven airway inflammation by allergen immunotherapy is independent of B cell and Ig responses in mice. Journal of immunology. 2010; 185(7):3857-65. https://doi.org/10.4049/jimmunol.0903909 PMID: 20802147.
34. Rizzi M, Lorenzetti R, Fischer K, Staniek J, Janowska I, Troilo A, et al. Impact of tofacitinib treatment on human B-cells in vitro and in vivo. Journal of autoimmunity. 2017; 77:55-66. https://doi.org/10.1016/j. jaut.2016.10.005 PMID: 27793425.
35. Anderson CF, Gerber JS, Mosser DM. Modulating macrophage function with IgG immune complexes. J Endotoxin Res. 2002; 8(6):477-81. https://doi.org/10.1179/096805102125001118 PMID: 12697094.
36. Gallo P, Goncalves R, Mosser DM. The influence of IgG density and macrophage Fc (gamma) receptor cross-linking on phagocytosis and IL-10 production. Immunology letters. 2010; 133(2):70-7. https://doi.org/10.1016/j.imlet.2010.07.004 PMID: 20670655.
37. Dowty ME, Lin J, Ryder TF, Wang W, Walker GS, Vaz A, et al. The pharmacokinetics, metabolism, and clearance mechanisms of tofacitinib, a janus kinase inhibitor, in humans. Drug Metab Dispos. 2014; 42 (4):759-73. https://doi.org/10.1124/dmd.113.054940 PMID: 24464803.
38. Piscianz E, Valencic E, Cuzzoni E, De Iudicibus S, De Lorenzo E, Decorti G, et al. Fate of lymphocytes after withdrawal of tofacitinib treatment. PLoS One. 2014; 9(1):e85463. https://doi.org/10.1371/journal. pone.0085463 PMID: 24416411.
39. Migita K, Izumi Y, Jiuchi Y, Kozuru H, Kawahara C, Izumi M, et al. Effects of Janus kinase inhibitor tofacitinib on circulating serum amyloid A and interleukin-6 during treatment for rheumatoid arthritis. Clin Exp Immunol. 2014; 175(2):208-14. https://doi.org/10.1111/cei.12234 PMID: 24665995.
40. Okiyama N, Furumoto Y, Villarroel VA, Linton JT, Tsai WL, Gutermuth J, et al. Reversal of CD8 T-cellmediated mucocutaneous graft-versus-host-like disease by the JAK inhibitor tofacitinib. J Invest Dermatol. 2014; 134(4):992-1000. https://doi.org/10.1038/jid.2013.476 PMID: 24213371.
41. Mantel PY, Ouaked N, Ruckert B, Karagiannidis C, Welz R, Blaser K, et al. Molecular mechanisms underlying FOXP3 induction in human T cells. Journal of immunology. 2006; 176(6):3593-602. PMID: 16517728.
42. Zhou Y, Leng X, Luo S, Su Z, Luo X, Guo H, et al. Tolerogenic Dendritic Cells Generated with Tofacitinib Ameliorate Experimental Autoimmune Encephalomyelitis through Modulation of Th17/Treg Balance. Journal of immunology research. 2016; 2016:5021537. https://doi.org/10.1155/2016/5021537 PMID: 28070525.