The Escherichia coli heat-labile enterotoxin B subunit protects from allergic airway disease development by inducing CD4+ regulatory T cells

Mucosal Immunology

Volumn 6, Issue 3, 2013, Pages 535-546

  Donaldson, D S ^a   Apostolaki, M ^a   Bone, H K ^a   Richards, C M ^a   Williams, N A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI ENTEROTOXIN; ESCHERICHIA COLI ENTEROTOXIN B; IMMUNOGLOBULIN E; INTERLEUKIN 4; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DRUG EFFECT; EOSINOPHILIA; FEMALE; IMMUNOGLOBULIN PRODUCTION; LUNG LAVAGE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT ALLERGY;

EID: 84876352416     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.93     Document Type: Article

References (44)

1. Eder, W., Ege, M.J. & von Mutius, E. The asthma epidemic. N. Engl. J. Med. 355, 2226-2235 (2006).
2. Hamid, Q. & Tulic, M. Immunobiology of asthma. Annu. Rev. Physiol. 71, 489-507 (2009).
3. Fanta, C.H. Asthma. N. Engl. J. Med. 360, 1002-1014 (2009).
4. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M. & Toda, M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164 (1995).
5. Xystrakis, E. et al. Reversing the defective induction of IL-10-secreting regulatory Tcells in glucocorticoid-resistant asthma patients. J. Clin. Invest. 116, 146-155 (2006).
6. Bauer, L. et al. Modulation of the allergic immune response inBALB/c mice by subcutaneous injectionofhigh doses ofthe dominant Tcell epitope from the major birch pollen allergen Bet v 1. Clin. Exp. Immunol. 107, 536-541 (1997).
7. von Garnier, C. et al. Allergen-derived long peptide immunotherapy down-regulates specific IgE response and protects from anaphylaxis. Eur. J. Immunol. 30, 1638-1645 (2000).
8. Alexander, C., Ying, S., B Kay, A. & Larche, M. Feld 1-derived Tcell peptide therapy induces recruitment of CD4 + CD25 +; CD4 + interferon-gamma + T helper type 1 cells to sites of allergen-induced late-phase skin reactions in cat-allergic subjects. Clin. Exp. Allergy 35, 52-58 (2005).
9. Verhoef, A., Alexander, C., Kay, A.B. & Larche, M. T cell epitope immunotherapy induces a CD4 + Tcell population with regulatory activity. PLoS Med. 2, e78 (2005).
10. Campbell, J.D. et al. Peptide immunotherapy in allergic asthma generates IL-10-dependent immunological tolerance associated with linked epitope suppression. J. Exp. Med. 206, 1535-1547 (2009).
11. Larche, M. Update on the current status of peptide immunotherapy. J. Allergy Clin. Immunol. 119, 906-909 (2007).
12. Ober, C. & Thompson, E.E. Rethinking genetic models of asthma: the role of environmental modifiers. Curr. Opin. Immunol. 17, 670-678 (2005).
13. Luross, J.A., Heaton, T., Hirst, T.R., Day, M.J. & Williams, N.A. Escherichia coli heat-labile enterotoxin B subunit prevents autoimmune arthritis through induction of regulatory CD4+ T cells. Arthritis Rheum. 46, 1671-1682 (2002).
14. Ola, T.O. & Williams, N.A. Protection of non-obese diabetic mice from autoimmune diabetes by Escherichia coli heat-labile enterotoxinBsubunit. Immunology 117, 262-270 (2006).
15. Spangler, B.D. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56, 622-647(1992).
16. Sixma, T.K. et al. Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J. Mol. Biol. 230, 890-918 (1993).
17. Cassel, D. & Pfeuffer, T. Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl. Acad. Sci. USA 75, 2669-2673 (1978).
18. Donaldson, D.S., Tong, K.K. & Williams, N.A. Mucosal administrationofthe B subunit of E. coli heat-labile enterotoxin promotes the development of Foxp3-expressing regulatoryTcells. Mucosal Immunol. 4, 227-238 (2011).
19. Brusselle, G.G. et al. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin. Exp. Allergy 24, 73-80 (1994).
20. Korsgren, M., Erjefalt, J.S., Korsgren, O., Sundler, F. & Persson, C.G. Allergic eosinophil-rich inflammation develops in lungs and airways of B cell-deficient mice. J. Exp. Med. 185, 885-892 (1997).
21. Ling, E.M. et al. Relation of CD4 + CD25 + regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 363, 608-615 (2004).
22. Thunberg, S. et al. Immune regulation by CD4 +CD25 + T cells and interleukin-10 in birch pollen-allergic patients and non-allergic controls. Clin. Exp. Allergy 37, 1127-1136 (2007).
23. Brusko, T.M., Putnam, A.L. & Bluestone, J.A. Human regulatoryTcells: role in autoimmune disease and therapeutic opportunities. Immunol. Rev. 223, 371-390 (2008).
24. Hartl, D. et al. Quantitative and functional impairment of pulmonary CD4 +CD25hi regulatory T cells in pediatric asthma. J. Allergy Clin. Immunol. 119, 1258-1266 (2007).
25. Francis, J.N., Till, S.J. & Durham, S.R. Induction of IL-10+ CD4 +CD25 + T cells by grass pollen immunotherapy. J. Allergy Clin. Immunol. 111, 1255-1261 (2003).
26. Gardner, L.M., Thien, F.C., Douglass, J.A., Rolland, J.M. & O'Hehir, R.E. Induction of T 'regulatory' cells by standardized house dust mite immunotherapy: an increase in CD4 + CD25 + interleukin-10+ T cells expressing peripheral tissue trafficking markers. Clin. Exp. Allergy 34, 1209-1219 (2004).
27. Lewkowich, I.P. et al. CD4 +CD25 + Tcells protect against experimentally induced asthmaand alter pulmonary dendritic cellphenotype and function. J. Exp. Med. 202, 1549-1561 (2005).
28. Leech, M.D., Benson, R.A., De Vries, A., Fitch, P.M. & Howie, S.E. Resolution of Der p1-induced allergic airway inflammation is dependent on CD4 +CD25 +Foxp3 + regulatory cells. J. Immunol. 179, 7050-7058 (2007).
29. Kearley, J., Barker, J.E., Robinson, D.S. & Lloyd, C.M. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4 +CD25 + regulatoryTcellsisinterleukin10dependent. J. Exp. Med. 202, 1539-1547 (2005).
30. Kearley, J., Robinson, D.S. & Lloyd, C.M. CD4+CD25 + regulatoryTcells reverse established allergic airway inflammation and prevent airway remodeling. J. Allergy Clin. Immunol. 122, 617-624 e616 (2008).
31. Nashar, T.O., Webb, H.M., Eaglestone, S., Williams, N.A. & Hirst, T.R. Potent immunogenicity of the B subunits of Escherichia coli heat-labile enterotoxin: receptor binding is essential and induces differential modulation of lymphocyte subsets. Proc. Natl. Acad. Sci. USA 93, 226-230 (1996).
32. Tritto, E. et al. The acquired immune response to the mucosal adjuvant LTK63 imprints the mouse lung with a protective signature. J. Immunol. 179, 5346-5357 (2007).
33. Williams, A.E. et al. Innate imprinting by the modified heat-labile toxin of Escherichiacoli (LTK63) provides generic protection against lung infectious disease. J. Immunol. 173, 7435-7443 (2004).
34. Fu, C.L., Chuang, Y.H., Chau, L.Y. & Chiang, B.L. Effects of adenovirus-expressing IL-10inalleviating airway inflammationinasthma. J. Gene Med. 8, 1393-1399 (2006).
35. Hansen, G. et al. CD4(+) T helper cells engineeredtoproduce latent TGF-beta1 reverse allergen-induced airway hyperreactivity and inflammation. J. Clin. Invest. 105, 61-70 (2000).
36. Fantini, M.C., Becker, C., Monteleone, G., Pallone, F., Galle, P.R. & Neurath, M.F. Cutting edge: TGF-beta induces a regulatory phenotype in CD4 +CD25-T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172, 5149-5153 (2004).
37. Dardalhon, V. et al. IL-4 inhibits TGF-beta-induced Foxp3+ T cells and, together with TGF-beta, generates IL-9+ IL-10 + Foxp3(-) effectorTcells. Nat. Immunol. 9, 1347-1355 (2008).
38. Veldhoen, M. et al. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 9, 1341-1346 (2008).
39. McLane, M.P. et al. Interleukin-9 promotes allergen-induced eosinophilic inflammation and airway hyperresponsiveness in transgenic mice. Am. J. Respir. Cell Mol. Biol. 19, 713-720 (1998).
40. Makinde, T., Murphy, R.F. & Agrawal, D.K. The regulatory role of TGF-beta in airway remodeling in asthma. Immunol. Cell Biol. 85, 348-356 (2007).
41. Turcanu, V., Hirst, T.R. & Williams, N.A. Modulation of human monocytes by Escherichia coli heat-labile enterotoxin B-subunit; altered cytokine production and its functional consequences. Immunology 106, 316-325 (2002).
42. Hamelmann, E. et al. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156 (3 Part 1), 766-775 (1997).
43. Apostolaki, M. & Williams, N.A. Nasal delivery of antigen with the B subunit of Escherichia coli heat-labile enterotoxin augments antigen-specific T-cell clonal expansion and differentiation. Infect. Immun. 72, 4072-4080 (2004).
44. Tager, A.M. et al. Leukotriene B4 receptor BLT1 mediates early effector T cell recruitment. Nat. Immunol. 4, 982-990 (2003).