B lymphocytes regulate airway granulocytic inflammation and cytokine production in a murine model of fungal allergic asthma

Cellular and Molecular Immunology

Volumn 12, Issue 2, 2015, Pages 202-212

  Ghosh, Sumit ^a   Hoselton, Scott A ^a   Asbach, Scott V ^a   Steffan, Breanne N ^a   Wanjara, Steve B ^a   Dorsam, Glenn P ^a   Schuh, Jane M ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Aspergillus fumigatus; B lymphocytes; inflammation

Indexed keywords

COLLAGEN; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; CYTOKINE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN STRUCTURE; MESSENGER RNA;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; EOSINOPHILIA; EXPOSURE; GRANULOCYTE; IMMUNOREGULATION; MOUSE; NEUTROPHILIA; NONHUMAN; PNEUMONIA; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; TH2 CELL; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHUS HYPERREACTIVITY; CELL CULTURE; DISEASE MODEL; FUNGUS SPORE; GENETICS; HUMAN; IMMUNOGLOBULIN STRUCTURE; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALIA; ASPERGILLUS FUMIGATUS; FUNGI; MURINAE; MUS;

ANIMALS; ASTHMA; B-LYMPHOCYTES; BLOTTING, WESTERN; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; GRANULOCYTES; HUMANS; IMMUNOGLOBULIN E; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN JOINING REGION; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PNEUMONIA; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPORES, FUNGAL;

EID: 84938586144     PISSN: 16727681     EISSN: 20420226     Source Type: Journal    
DOI: 10.1038/cmi.2014.103     Document Type: Article

References (61)

1. Cabana MD, Kunselman SJ, Nyenhuis SM, Wechsler ME. Researching asthma across the ages: insights from the National Heart, Lung, and Blood Institutes Asthma Network. J Allergy Clin Immunol 2014; 133: 27-33.
2. Knutsen AP, Bush RK, Demain JG, Denning DW, Dixit A, Fairs A et al. Fungi and allergic lower respiratory tract diseases. J Allergy Clin Immunol 2012; 129: 280-291; quiz 292-293.
3. Lewkowich IP, Herman NS, Schleifer KW, Dance MP, Chen BL, Dienger KM et al. CD41CD251 T cells protect against experimentally induced asthma and alter pulmonary dendritic cell phenotype and function. J Exp Med 2005; 202: 1549-1561.
4. Lindell DM, Berlin AA, Schaller MA, Lukacs NW. B cell antigen presentation promotes Th2 responses and immunopathology during chronic allergic lung disease. PLoS One 2008; 3: e3129.
5. Kita H. Eosinophils: multifunctional and distinctive properties. Int Arch Allergy Immunol 2013; 161(Suppl 2): 3-9.
6. Hong CM, Galvagno SM Jr. Patients with chronic pulmonary disease. Med Clin N Am 2013; 97: 1095-1107.
7. Denning DW, ODriscoll BR, Hogaboam CM, Bowyer P, Niven RM. The link between fungi and severe asthma: a summary of the evidence. Eur Respir J 2006; 27: 615-26.
8. Agarwal R, Chakrabarti A, Shah A, Gupta D, Meis JF, Guleria R et al. Allergic bronchopulmonary aspergillosis: review of literature and proposal of new diagnostic and classification criteria. Clin Exp Allergy 2013; 43: 850-873.
9. Rosenberg HF, Dyer KD, Foster PS. Eosinophils: changing perspectives in health and disease. Nat Rev Immunol 2013; 13: 9-22.
10. Ghosh S, Hoselton SA, Dorsam GP, Schuh JM. Eosinophils in fungusassociated allergic pulmonary disease. Front Pharmacol 2013; 4: 8.
11. Kita H. Eosinophils: multifaceted biological properties and roles in health and disease. Immunol Rev 2011; 242: 161-177.
12. Murdock BJ, Shreiner AB, McDonald RA, Osterholzer JJ, White ES, Toews GB et al. Coevolution of TH1, TH2, and TH17 responses during repeated pulmonary exposure to Aspergillus fumigatus conidia. Infect Immun 2011; 79: 125-135.
13. Macdowell AL, Peters SP. Neutrophils in asthma. Curr Allergy Asthma Rep 2007; 7: 464-468.
14. Ghosh S, Hoselton SA, Schuh JM. Characterization of CD191CD231 B2 lymphocytes in the allergic airways of BALB/c mice in response to the inhalation of Aspergillus fumigatus conidia. Open Immunol J 2012; 5: 46-54.
15. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2011; 91: 221-264.
16. Ghosh S, Samarasinghe AE, Hoselton SA, Dorsam GP, Schuh JM. Hyaluronan deposition and co-localization with inflammatory cells and collagen in a murine model of fungal allergic asthma. Inflamm Res 2014; 63: 475-484.
17. Hoselton SA, Samarasinghe AE, Seydel JM, Schuh JM. An inhalation model of airway allergic response to inhalation of environmental Aspergillus fumigatus conidia in sensitized BALB/c mice. Med Mycol 2010; 48: 1056-1065.
18. Samarasinghe AE, Hoselton SA, Schuh JM. A comparison between intratracheal and inhalation delivery of Aspergillus fumigatus conidia in the development of fungal allergic asthma in C57BL/6 mice. Fungal Biol 2011; 115: 21-29.
19. Bice DE, Gray RH, Evans MJ, Muggenburg BA. Identification of plasma cells in lung alveoli and interstitial tissues after localized lung immunization. J Leuk Biol 1987; 41: 1-7.
20. Takhar P, Corrigan CJ, Smurthwaite L, OConnor BJ, Durham SR, Lee TH et al. Class switch recombination to IgE in the bronchial mucosa of atopic and nonatopic patients with asthma. J Allergy Clin Immunol 2007; 119: 213-218.
21. Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol 2008; 8: 205-217.
22. Zhang M, Murphy RF, Agrawal DK. Decoding IgE Fc receptors. Immunol Res 2007; 37: 1-16.
23. Rolinck-Werninghaus C, Wahn U, Hamelmann E. Anti-IgE therapy in allergic asthma. Curr Drug Targets Inflamm Allergy 2005; 4: 551-564.
24. Buhl R. Anti-IgE antibodies for the treatment of asthma. Curr Opin Pulmon Med 2005; 11: 27-34.
25. Nowak D. Management of asthma with anti-immunoglobulin E: a review of clinical trials of omalizumab. Respir Med 2006; 100: 1907-1917.
26. Knutsen AP. Immunopathology and immunogenetics of allergic bronchopulmonary aspergillosis. J Allergy (Cairo) 2011; 2011: 785983.
27. Rapaka RR, Ricks DM, Alcorn JF, Chen K, Khader SA, Zheng M et al. Conserved natural IgM antibodies mediate innate and adaptive immunity against the opportunistic fungus Pneumocystis murina. J Exp Med 2010; 207: 2907-2919.
28. Flicker S, Gadermaier E, Madritsch C, Valenta R. Passive immunization with allergen-specific antibodies. Curr Top Microbiol Immunol 2011; 820: 141-159.
29. Chen J, Trounstine M, Alt FW, Young F, Kurahara C, Loring JF et al. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int Immunol 1993; 5: 647-656.
30. Hogaboam CM, Blease K, Mehrad B, Steinhauser ML, Standiford TJ, Kunkel SL et al. Chronic airway hyperreactivity, goblet cell hyperplasia, and peribronchial fibrosis during allergic airway disease induced by Aspergillus fumigatus. Am J Pathol 2000; 156: 723-732.
31. Ghosh S, Samarasinghe AE, Hoselton SA, Dorsam GP, Schuh JM. Hyaluronan deposition and co-localization with inflammatory cells and collagen in a murine model of fungal allergic asthma. Inflamm Res 2014; 63: 475-484.
32. Ghosh S, Hoselton SA, Schuh JM. mu-chain-deficient mice possess B-1 cells and produce IgG and IgE, but not IgA, following systemic sensitization and inhalational challenge in a fungal asthma model. J Immunol 2012; 189: 1322-1329.
33. Chung KF. Inflammatory biomarkers in severe asthma. Curr Opin Pulmon Med 2012; 18: 35-41.
34. de Filippo K, Henderson RB, Laschinger M, Hogg N. Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J Immunol 2008; 180: 4308-4315.
35. Conroy DM, Williams TJ. Eotaxin and the attraction of eosinophils to the asthmatic lung. Respir Res 2001; 2: 150-156.
36. Pease JE, Williams TJ. Eotaxin and asthma. Curr Opin Pharmacol 2001; 1: 248-253.
37. Chien JW, Lin CY, Yang KD, Lin CH, Kao JK, Tsai YG. Increased IL-17A secreting CD41 T cells, serum IL-17 levels and exhaled nitric oxide are correlated with childhood asthma severity. Clin Exp Allergy 2013; 43: 1018-1026.
38. Gladiator A, Wangler N, Trautwein-Weidner K, Leibund Gut- Landmann S. Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol 2013; 190: 521-525.
39. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010; 104: 1131-1137.
40. Smith KA, Maizels RM. IL-6 controls susceptibility to helminth infection by impeding Th2 responsiveness and altering the Treg phenotype in vivo. Eur J Immunol 2014; 44: 150-161.
41. Pedroza M, Schneider DJ, Karmouty-Quintana H, Coote J, Shaw S, Corrigan R et al. Interleukin-6 contributes to inflammation and remodeling in a model of adenosine mediated lung injury. PLoS One 2011; 6: e22667.
42. Hamelmann E, Vella AT, Oshiba A, Kappler JW, Marrack P, Gelfand EW. Allergic airway sensitization induces T cell activation but not airway hyperresponsiveness in B cell-deficient mice. Proc Natl Acad Sci USA 1997; 94: 1350-1355.
43. Jungsuwadee P, Benkovszky M, Dekan G, Stingl G, Epstein MM. Repeated aerosol allergen exposure suppresses inflammation in Bcell- deficient mice with established allergic asthma. Int Arch Allergy Immunol 2004; 133: 40-48.
44. de Bruijn ML, Nieland JD, Schumacher TN, Ploegh HL, Kast WM, Melief CJ. Mechanisms of induction of primary virus-specific cytotoxic T lymphocyte responses. Eur J Immunol 1992; 22: 3013-3020.
45. Guery JC, Adorini L. Dendritic cells are the most efficient in presenting endogenous naturally processed self-epitopes to class IIrestricted T cells. J Immunol 1995; 154: 536-544.
46. Zhong G, Reis e Sousa C, Germain RN. Antigen-unspecific B cells and lymphoid dendritic cells both show extensive surface expression of processed antigen-major histocompatibility complex class II complexes after soluble protein exposure in vivo or in vitro. J Exp Med 1997; 186: 673-682.
47. Qi H, Egen JG, Huang AY, Germain RN. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 2006; 312: 1672-1676.
48. Angeli V, Ginhoux F, Llodra J, Quemeneur L, Frenette PS, Skobe M et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 2006; 24: 203-215.
49. Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med 2000; 192: 475-482.
50. Lundy SK, Berlin AA, Martens TF, Lukacs NW. Deficiency of regulatory B cells increases allergic airway inflammation. Inflamm Res 2005; 54: 514-521.
51. Mizoguchi A, Bhan AK. A case for regulatory B cells. JImmunol 2006; 176: 705-710.
52. Yu P, Wang Y, Chin RK, Martinez-Pomares L, Gordon S, Kosco-Vibois MH et al. B cells control the migration of a subset of dendritic cells into B cell follicles via CXC chemokine ligand 13 in a lymphotoxindependent fashion. J Immunol 2002; 168: 5117-5123.
53. Wang P, Zheng SG. Regulatory T cells and B cells: implication on autoimmune diseases. Int J Clin Exp Pathol 2013; 6: 2668-2674.
54. Ray A, Basu S, Williams CB, Salzman NH, Dittel BN. A novel IL-10- independent regulatory role for B cells in suppressing autoimmunity by maintenance of regulatory T cells via GITR ligand. J Immunol 2012; 188: 3188-3198.
55. Mann MK, Maresz K, Shriver LP, Tan Y, Dittel BN. B cell regulation of CD41CD251 T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol 2007; 178: 3447-3456.
56. Doganci A, Sauer K, Karwot R, Finotto S. Pathological role of IL-6 in the experimental allergic bronchial asthma in mice. Clin Rev Allergy Immunol 2005; 28: 257-270.
57. Nembrini C, Marsland BJ, Kopf M. IL-17-producing T cells in lung immunity and inflammation. J Allergy Clin Immunol 2009; 23: 986-994; quiz 995-996.
58. Murdock BJ, Falkowski NR, Shreiner AB, Sadighi Akha AA, McDonald RA, White ES et al. Interleukin-17 drives pulmonary eosinophilia following repeated exposure to Aspergillus fumigatus conidia. Infect Immun 2012; 80: 1424-1436.
59. Song C, Luo L, Lei Z, Li B, Liang Z, Liu G et al. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J Immunol 2008; 181: 6117-6124.
60. Hellings PW, Kasran A, Liu Z, Vandekerckhove P, Wuyts A, Overbergh L et al. Interleukin-17 orchestrates the granulocyte influx into airways after allergen inhalation in a mouse model of allergic asthma. Am J Respir Cell Mol Biol 2003; 28: 42-50.
61. Bartemes KR, Iijima K, Kobayashi T, Kephart GM, McKenzie AN, Kita H. IL-33-responsive lineage-CD251 CD44hi lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 2012; 188: 1503-1513.