Low-dose intestinal Trichuris muris infection alters the lung immune microenvironment and can suppress allergic airway inflammation

Infection and Immunity

Volumn 84, Issue 2, 2016, Pages 491-501

  Chenery, Alistair L ^a   Antignano, Frann ^a   Burrows, Kyle ^a   Scheer, Sebastian ^a   Perona Wright, Georgia ^a   Zaph, Colby ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; PAPAIN; HOUSE DUST ALLERGEN;

ADAPTIVE IMMUNITY; ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; INNATE IMMUNITY; INTERFERON PRODUCTION; MICROENVIRONMENT; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TRICHURIASIS; TRICHURIS MURIS; ANIMAL; ASTHMA; BIOSYNTHESIS; C57BL MOUSE; CELL COMMUNICATION; DOSE RESPONSE; HOST PARASITE INTERACTION; IMMUNOLOGY; INFLAMMATION; INTESTINE; INTESTINE INFECTION; LUNG; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; RESPIRATORY TRACT ALLERGY; TRICHURIS;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTESTINAL DISEASES, PARASITIC; INTESTINES; LUNG; MICE; MICE, INBRED C57BL; PAPAIN; RESPIRATORY HYPERSENSITIVITY; TRICHURIASIS; TRICHURIS;

EID: 84957612502     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01240-15     Document Type: Article

References (51)

1. Holgate ST. 2007. Epithelium dysfunction in asthma. J Allergy Clin Immunol 120:1233-1244. http://dx.doi.org/10.1016/j.jaci.2007.10.025.
2. Turner JR. 2009. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9:799-809. http://dx.doi.org/10.1038/nri2653.
3. Maloy KJ, Powrie F. 2011. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474:298-306. http://dx.doi.org/10.1038/nature10208.
4. Mestecky J. 1987. The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 7:265-276. http://dx.doi.org/10.1007/BF00915547.
5. Holmgren J, Czerkinsky C. 2005. Mucosal immunity and vaccines. Nat Med 11:S45-S53. http://dx.doi.org/10.1038/nm1213.
6. Czerkinsky C, Holmgren J. 2009. Enteric vaccines for the developing world: a challenge for mucosal immunology. Mucosal Immunol 2:284-287 http://dx.doi.org/10.1038/mi.2009.22.
7. Keely S, Talley NJ, Hansbro PM. 2012. Pulmonary-intestinal cross-talk in mucosal inflammatory disease. Mucosal Immunol 5:7-18. http://dx.doi.org/10.1038/mi.2011.55.
8. Penders J, Stobberingh EE, van den Brandt PA, Thijs C. 2007. The role of the intestinal microbiota in the development of atopic disorders. Allergy 62:1223-1236. http://dx.doi.org/10.1111/j.1398-9995.2007.01462.x.
9. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet M-R, Mohn WW, McNagny KM, Finlay BB. 2012. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13:440-447. http://dx.doi.org/10.1038/embor.2012.32.
10. Ruane D, Brane L, Reis BS, Cheong C, Poles J, Do Y, Zhu H, Velinzon K, Choi J-H, Studt N, Mayer L, Lavelle EC, Steinman RM, Mucida D, Mehandru S. 2013. Lung dendritic cells induce migration of protective T cells to the gastrointestinal tract. J Exp Med 210:1871-1888. http://dx.doi.org/10.1084/jem.20122762.
11. Nemoto Y, Kanai T, Takahara M, Oshima S, Okamoto R, Tsuchiya K, Matsumoto S, Watanabe M, Alerts E. 2013. Th1/Th17-mediated interstitial pneumonia in chronic colitis mice independent of intestinal microbiota. J Immunol 190:6616-6625. http://dx.doi.org/10.4049/jimmunol.1202930.
12. Wang H, Liu J-S, Peng S-H, Deng X-Y, Zhu D-M, Javidiparsijani S, Wang G-R, Li D-Q, Li L-X, Wang Y-C, Luo J-M. 2013. Gut-lung crosstalk in pulmonary involvement with inflammatory bowel diseases. World J Gastroenterol 19:6794-6804. http://dx.doi.org/10.3748/wjg.v19.i40.6794.
13. Brand S. 2009. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58:1152-1167. http://dx.doi.org/10.1136/gut.2008.163667.
14. Cohn L, Elias JA, Chupp GL. 2004. Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol 22:789-815. http://dx.doi.org/10.1146/annurev.immunol.22.012703.104716.
15. Hammad H, Lambrecht BN. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol 8:193-204. http://dx.doi.org/10.1038/nri2275.
16. Zhu J, Yamane H, Paul WE. 2010. Differentiation of effector CD4 T cell populations. Annu Rev Immunol 28:445-489. http://dx.doi.org/10.1146/annurev-immunol-030409-101212.
17. Baumgart DC, Thomas S, Przesdzing I, Metzke D, Bielecki C, Lehmann SM, Lehnardt S, Dörffel Y, Sturm A, Scheffold A, Schmitz J, Radbruch A. 2009. Exaggerated inflammatory response of primary human myeloid dendritic cells to lipopolysaccharide in patients with inflammatory bowel disease. Clin Exp Immunol 157:423-436. http://dx.doi.org/10.1111/j.1365-2249.2009.03981.x.
18. Klein Wolterink RGJ, Kleinjan A, van Nimwegen M, Bergen I, de Bruijn M, Levani Y, Hendriks RW. 2012. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 42:1106-1116. http://dx.doi.org/10.1002/eji.201142018.
19. Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, Hreggvidsdottir HS, Heinsbroek SE, Legrand N, Buskens CJ, Bemelman WA, Mjösberg JM, Spits H. 2013. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 14:221-229. http://dx.doi.org/10.1038/ni.2534.
20. Reinhardt RL, Liang H-E, Locksley RM. 2009. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat Immunol 10:385-393. http://dx.doi.org/10.1038/ni.1715.
21. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, Yogev N, Gu Y, Khodoun M, Hildeman D, Boespflug N, Fogolin MB, Gröbe L, Greweling M, Finkelman FD, Cardin R, Mohrs M, Müller W, Waisman A, Roers A, Karp CL. 2009. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183: 2312-2320. http://dx.doi.org/10.4049/jimmunol.0900185.
22. Antignano F, Mullaly SC, Burrows K, Zaph C. 2011. Trichuris muris infection: a model of type 2 immunity and inflammation in the gut. J Vis Exp 51:2774. http://dx.doi.org/10.3791/2774.
23. Gold MJ, Antignano F, Halim TYF, Hirota JA, Blanchet M-R, Zaph C, Takei F, McNagny KM. 2014. Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J Allergy Clin Immunol 133:1142-1148. http://dx.doi.org/10.1016/j.jaci.2014.02.033.
24. Arora S, McDonald RA, Toews GB, Huffnagle GB. 2006. Effect of a CD4-depleting antibody on the development of Cryptococcus neoformansinduced allergic bronchopulmonary mycosis in mice. Infect Immun 74: 4339-4348. http://dx.doi.org/10.1128/IAI.01989-05.
25. Cliffe LJ, Grencis RK. 2004. The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv Parasitol 57:255-307. http://dx.doi.org/10.1016/S0065-308X(04)57004-5.
26. Cope A, Le Friec G, Cardone J, Kemper C. 2011. The Th1 life cycle: molecular control of IFN-γ to IL-10 switching. Trends Immunol 32:278-286 http://dx.doi.org/10.1016/j.it.2011.03.010.
27. + T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol 188: 1178-1190. http://dx.doi.org/10.4049/jimmunol.1102755.
28. + cell populations during visceral leishmaniasis. PLoS Pathog 8:e1002827. http://dx.doi.org/10.1371/journal.ppat.1002827.
29. Halim TYF, Krauss RH, Sun AC, Takei F. 2012. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36:451-463. http://dx.doi.org/10.1016/j.immuni.2011.12.020.
30. Boehm U, Klamp T, Groot M, Howard JC. 1997. Cellular responses to interferon-gamma. Annu Rev Immunol 15:749-795.
31. Bancroft AJ, Else KJ, Grencis RK. 1994. Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur J Immunol 24:3113-3118.
32. Foth BJ, Tsai IJ, Reid AJ, Bancroft AJ, Nichol S, Tracey A, Holroyd N, Cotton JA, Stanley EJ, Zarowiecki M, Liu JZ, Huckvale T, Cooper PJ, Grencis RK, Berriman M. 2014. Whipworm genome and dual-species transcriptome analyses provide molecular insights into an intimate hostparasite interaction. Nat Genet 46:693-700. http://dx.doi.org/10.1038/ng.3010.
33. Wild JS, Sigounas A, Sur N, Siddiqui MS, Alam R, Kurimoto M, Sur S. 2000 IFN-gamma-inducing factor (IL-18) increases allergic sensitization, serum IgE, Th2 cytokines, and airway eosinophilia in a mouse model of allergic asthma. J Immunol 164:2701-2710. http://dx.doi.org/10.4049/jimmunol.164.5.2701.
34. Wong CK, Ho CY, Ko FWS, Chan CHS, Ho ASS, Hui DSC, Lam CWK. 2001 Proinflammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFN-γ, IL-4, IL-10 and IL-13) in patients with allergic asthma. Clin Exp Immunol 125:177-183. http://dx.doi.org/10.1046/j.1365-2249.2001.01602.x.
35. Mitchell C, Provost K, Niu N, Homer R, Cohn L. 2011. IFN-γ acts on the airway epithelium to inhibit local and systemic pathology in allergic airway disease. J Immunol 187:3815-3820. http://dx.doi.org/10.4049/jimmunol.1100436.
36. Ford JG, Rennick D, Donaldson DD, Venkayya R, McArthur C, Hansell E, Kurup VP, Warnock M, Grünig G. 2001. Il-13 and IFN-gamma: interactions in lung inflammation. J Immunol 167:1769-1777. http://dx.doi.org/10.4049/jimmunol.167.3.1769.
37. Contreras-Ruiz L, Ghosh-Mitra A, Shatos MA, Dartt DA, Masli S. 2013. Modulation of conjunctival goblet cell function by inflammatory cytokines. Mediators Inflamm 2013:636812. http://dx.doi.org/10.1155/2013/636812.
38. Akdis CA, Akdis M. 2014. Mechanisms of immune tolerance to allergens: role of IL-10 and Tregs. J Clin Invest 124:4678-4680. http://dx.doi.org/10.1172/JCI78891.
39. Böhm L, Maxeiner J, Meyer-Martin H, Reuter S, Finotto S, Klein M, Schild H, Schmitt E, Bopp T, Taube C. 2015. IL-10 and regulatory T cells cooperate in allergen-specific immunotherapy to ameliorate allergic asthma. J Immunol 194:887-897. http://dx.doi.org/10.4049/jimmunol.1401612.
40. Takanaski S. 1994. Interleukin 10 inhibits lipopolysaccharide-induced survival and cytokine production by human peripheral blood eosinophils. J Exp Med 180:711-715. http://dx.doi.org/10.1084/jem.180.2.711.
41. Chung F. 2001. Anti-inflammatory cytokines in asthma and allergy: interleukin-10, interleukin-12, interferon-gamma. Mediators Inflamm 10: 51-59. http://dx.doi.org/10.1080/09629350120054518.
42. Ogawa Y, Duru E, Ameredes B. 2008. Role of IL-10 in the resolution of airway inflammation. Curr Mol Med 8:437-445. http://dx.doi.org/10.2174/156652408785160907.
43. Mohrs K, Harris DP, Lund FE, Mohrs M. 2005. Systemic dissemination and persistence of Th2 and type 2 cells in response to infection with a strictly enteric nematode parasite. J Immunol 175:5306-5313. http://dx.doi.org/10.4049/jimmunol.175.8.5306.
44. Ito T, Yang M, Wang Y-H, Lande R, Gregorio J, Perng OA, Qin X-F, Liu Y-J, Gilliet M. 2007. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 204:105-115. http://dx.doi.org/10.1084/jem.20061660.
45. de Bruin AM, Voermans C, Nolte MA. 2014. Impact of interferon-γ on hematopoiesis. Blood 124:2479-2486. http://dx.doi.org/10.1182/blood-2014-04-568451.
46. Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y, Filbey KJ, Finney CAM, Greenwood EJD, Knox DP, Wilson MS, Belkaid Y, Rudensky AY, Maizels RM. 2010. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-beta pathway. J Exp Med 207:2331-2341. http://dx.doi.org/10.1084/jem.20101074.
47. McSorley HJ, Blair NF, Smith KA, McKenzie AN, Maizels RM. 2014. Blockade of IL-33 release and suppression of type 2 innate lymphoid cell responses by helminth secreted products in airway allergy. Mucosal Immunol 7:1068-1078. http://dx.doi.org/10.1038/mi.2013.123.
48. Kitagaki K, Businga TR, Racila D, Elliott DE, Weinstock JV, Kline JN. 2006 Intestinal helminths protect in a murine model of asthma. J Immunol 177:1628-1635. http://dx.doi.org/10.4049/jimmunol.177.3.1628.
49. Houlden A, Hayes KS, Bancroft AJ, Worthington JJ, Wang P, Grencis RK, Roberts IS. 2015. Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome: effects reversed by pathogen clearance. PLoS One 10:e0125945. http://dx.doi.org/10.1371/journal.pone.0125945.
50. Zaiss MM, Rapin A, Lebon L, Dubey LK, Mosconi I, Sarter K, Piersigilli A, Menin L, Walker AW, Rougemont J, Paerewijck O, Geldhof P, McCoy KD, Macpherson AJ, Croese J, Giacomin PR, Loukas A, Junt T, Marsland BJ, Harris NL. 2015. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43:998-1010. http://dx.doi.org/10.1016/j.immuni.2015.09.012.
51. Bourke CD, Mutapi F, Nausch N, Photiou DMF, Poulsen LK, Kristensen B, Arnved J, Rønborg S, RoepstorffA, Thamsborg S, Kapel C, Melbye M, Bager P. 2012. Trichuris suis ova therapy for allergic rhinitis does not affect allergen-specific cytokine responses despite a parasitespecific cytokine response. Clin Exp Allergy 42:1582-1595. http://dx.doi.org/10.1111/j.1365-2222.2012.04063.x.