Bacillus Calmette-Guérin suppresses asthmatic responses via CD4+CD25+ regulatory T cells and dendritic cells

Allergy, Asthma and Immunology Research

Volumn 6, Issue 3, 2014, Pages 201-207

  Kim, Young Joon ^a   Kim, Ha Jung ^a   Kang, Mi Jin ^a   Yu, Ho Sung ^a   Seo, Ju Hee ^a   Kim, Hyung Young ^a   Park, Seoung Ju ^b   Lee, Yong Chul ^b   Hong, Soo Jong ^a  

^a University of Ulsan College of Medicine   (South Korea)

^b Chonbuk National University Medical School   (South Korea)

Author keywords

Allergic inflammation; Asthma; BCG; Dendritic cells; Mouse; T lymphocytes, regulatory

Indexed keywords

BASILIXIMAB; BCG VACCINE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; OVALBUMIN;

ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; BCG VACCINATION; BRONCHUS HYPERREACTIVITY; CD4+ CD25+ T LYMPHOCYTE; CELL TRANSFER; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; INFLAMMATION; INFLAMMATORY CELL; LUNG LAVAGE; MOUSE; NONHUMAN; PULMONARY EOSINOPHILIC INFLAMMATION; REGULATORY T LYMPHOCYTE; SENSITIZATION;

EID: 84899624010     PISSN: 20927355     EISSN: 20927363     Source Type: Journal    
DOI: 10.4168/aair.2014.6.3.201     Document Type: Article

References (44)

1. Walker C, Bode E, Boer L, Hansel TT, Blaser K, Virchow JC Jr. Allergic and nonallergic asthmatics have distinct patterns of T-cell activation and cytokine production in peripheral blood and bronchoalveolar lavage. Am Rev Respir Dis 1992;146:109-15.
2. Lee SH, Park JS, Park CS. The search for genetic variants and epigenetics related to asthma. Allergy Asthma Immunol Res 2011;3: 236-44.
3. Wang JM, Rambaldi A, Biondi A, Chen ZG, Sanderson CJ, Mantovani A. Recombinant human interleukin 5 is a selective eosinophil chemoattractant. Eur J Immunol 1989;19:701-5.
4. Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299: 1259-60.
5. Riedler J, Braun-Fahrländer C, Eder W, Schreuer M, Waser M, Maisch S, Carr D, Schierl R, Nowak D, von Mutius E; ALEX Study Team. Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 2001;358:1129-33.
6. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrländer C, Heederik D, Piarroux R, von Mutius E; GABRIELA Transregio 22 Study Group. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011;364:701-9.
7. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med 2006;355:2226-35.
8. Hong SJ, Ahn KM, Lee SY, Kim KE. The prevalences of asthma and allergic diseases in Korean children. Korean J Pediatr 2008;51:343-50.
9. Lee SI. Prevalence of childhood asthma in Korea: international study of asthma and allergies in childhood. Allergy Asthma Immunol Res 2010;2:61-4.
10. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002;347:911-20.
11. Seroogy CM, Gern JE. The role of T regulatory cells in asthma. J Allergy Clin Immunol 2005;116:996-9.
12. Curotto de Lafaille MA, Kutchukhidze N, Shen S, Ding Y, Yee H, Lafaille JJ. Adaptive Foxp3+ regulatory T cell-dependent and -independent control of allergic inflammation. Immunity 2008;29:114-26.
13. Robinson DS, Larché M, Durham SR. Tregs and allergic disease. J Clin Invest 2004;114:1389-97.
14. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, Sahoo A, Nam JH, Rhee JH, Hwang KC, Im SH. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 2010;107:2159-64.
15. Read S, Malmström V, Powrie F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 2000;192:295-302.
16. Hopfenspirger MT, Agrawal DK. Airway hyperresponsiveness, late allergic response, and eosinophilia are reversed with mycobacterial antigens in ovalbumin-presensitized mice. J Immunol 2002;168: 2516-22.
17. Erb KJ, Holloway JW, Sobeck A, Moll H, Le Gros G. Infection of mice with Mycobacterium bovis-Bacillus Calmette-Guérin (BCG) suppresses allergen-induced airway eosinophilia. J Exp Med 1998;187: 561-9.
18. Jason J, Archibald LK, Nwanyanwu OC, Kazembe PN, Chatt JA, Norton E, Dobbie H, Jarvis WR. Clinical and immune impact of Mycobacterium bovis BCG vaccination scarring. Infect Immun 2002; 70:6188-95.
19. Li Q, Shen HH. Neonatal bacillus Calmette-Guérin vaccination inhibits de novo allergic inflammatory response in mice via alteration of CD4+CD25+ T-regulatory cells. Acta Pharmacol Sin 2009;30:125-33.
20. Hammad H, Lambrecht BN. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol 2008;8:193-204.
21. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y, Figdor CG. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000;100:575-85.
22. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003;21:685-711.
23. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-52.
24. Brinster C, Shevach EM. Bone marrow-derived dendritic cells reverse the anergic state of CD4+CD25+ T cells without reversing their suppressive function. J Immunol 2005;175:7332-40.
25. Watanabe N, Wang YH, Lee HK, Ito T, Wang YH, Cao W, Liu YJ. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 2005;436:1181-5.
26. Chung DJ, Rossi M, Romano E, Ghith J, Yuan J, Munn DH, Young JW. Indoleamine 2,3-dioxygenase-expressing mature human monocyte-derived dendritic cells expand potent autologous regulatory T cells. Blood 2009;114:555-63.
27. Kim YJ, Kim HJ, Kang MJ, Kwon JW, Seo JH, Kim BJ, Yu J, Hong SJ. Effects of Bacillus Calmette-Guérin (BCG) vaccination according to time point of administration on asthma in a murine model. Korean J Asthma Allergy Clin Immunol 2010;30:307-13.
28. Choi MS, Park S, Choi T, Lee G, Haam KK, Hong MC, Min BI, Bae H. Bee venom ameliorates ovalbumin induced allergic asthma via modulating CD4+CD25+ regulatory T cells in mice. Cytokine 2013; 61:256-65.
29. Yu J, Jang SO, Kim BJ, Song YH, Kwon JW, Kang MJ, Choi WA, Jung HD, Hong SJ. The effects of Lactobacillus rhamnosus on the prevention of asthma in a murine model. Allergy Asthma Immunol Res 2010;2:199-205.
30. Tournoy KG, Kips JC, Schou C, Pauwels RA. Airway eosinophilia is not a requirement for allergen-induced airway hyperresponsiveness. Clin Exp Allergy 2000;30:79-85.
31. Soualhine H, Deghmane AE, Sun J, Mak K, Talal A, Av-Gay Y, Hmama Z. Mycobacterium bovis bacillus Calmette-Guérin secreting active cathepsin S stimulates expression of mature MHC class II molecules and antigen presentation in human macrophages. J Immunol 2007;179:5137-45.
32. Liu E, Law HK, Lau YL. BCG promotes cord blood monocyte-derived dendritic cell maturation with nuclear Rel-B up-regulation and cytosolic I kappa B alpha and beta degradation. Pediatr Res 2003;54:105-12.
33. Demangel C, Bean AG, Martin E, Feng CG, Kamath AT, Britton WJ. Protection against aerosol Mycobacterium tuberculosis infection using Mycobacterium bovis Bacillus Calmette Guérin-infected dendritic cells. Eur J Immunol 1999;29:1972-9.
34. Han Y, Guo Q, Zhang M, Chen Z, Cao X. CD69+ CD4+ CD25-T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-beta 1. J Immunol 2009;182: 111-20.
35. Ahrens B, Gruber C, Rha RD, Freund T, Quarcoo D, Awagyan A, Hutloff A, Dittrich AM, Wahn U, Hamelmann E. BCG priming of dendritic cells enhances T regulatory and Th1 function and suppresses allergen-induced Th2 function in vitro and in vivo. Int Arch Allergy Immunol 2009;150:210-20.
36. Lagranderie M, Abolhassani M, Vanoirbeek JA, Lima C, Balazuc AM, Vargaftig BB, Marchal G. Mycobacterium bovis bacillus Calmette-Guérin killed by extended freeze-drying targets plasmacytoid dendritic cells to regulate lung inflammation. J Immunol 2010;184: 1062-70.
37. Lewkowich IP, Herman NS, Schleifer KW, Dance MP, Chen BL, Dienger KM, Sproles AA, Shah JS, Köhl J, Belkaid Y, Wills-Karp M. CD4+CD25+ T cells protect against experimentally induced asthma and alter pulmonary dendritic cell phenotype and function. J Exp Med 2005;202:1549-61.
38. Lagranderie MR, Balazuc AM, Deriaud E, Leclerc CD, Gheorghiu M. Comparison of immune responses of mice immunized with five different Mycobacterium bovis BCG vaccine strains. Infect Immun 1996;64:1-9.
39. Fehérvari Z, Sakaguchi S. Development and function of CD25+ CD4+ regulatory T cells. Curr Opin Immunol 2004;16:203-8.
40. Gao X, Bai H, Cheng J, Fan Y, Wang S, Jiao L, Xiu N, Yang X. CD8a+ and CD8a-DC subsets from BCG-infected mice inhibit allergic Th2-cell responses by enhancing Th1-cell and Treg-cell activity respectively. Eur J Immunol 2012;42:165-75.
41. Orme IM, Andersen P, Boom WH. T cell response to Mycobacterium tuberculosis. J Infect Dis 1993;167:1481-97.
42. Christ AP, Rodriguez D, Bortolatto J, Borducchi E, Keller A, Mucida D, Silva JS, Leite LC, Russo M. Enhancement of Th1 lung immunity induced by recombinant Mycobacterium bovis Bacillus Calmette-Guérin attenuates airway allergic disease. Am J Respir Cell Mol Biol 2010;43:243-52.
43. Barlan I, Bahceciler NN, Akdis M, Akdis CA. Bacillus Calmette-Guérin, Mycobacterium bovis, as an immunomodulator in atopic diseases. Immunol Allergy Clin North Am 2006;26:365-77.
44. Fonseca DM, Paula MO, Wowk PF, Campos LW, Gembre AF, Turato WM, Ramos SG, Dias-Baruffi M, Barboza R, Gomes E, Horn C, Marchal G, Arruda LK, Russo M, Bonato VL. IFN-γ-mediated efficacy of allergen-free immunotherapy using mycobacterial antigens and CpG-ODN. Immunol Cell Biol 2011;89:777-85.