355
Views
7
CrossRef citations to date
0
Altmetric
Reviews

Microorganism-induced suppression of allergic airway disease: novel therapies on the horizon?

, , , &

References

  • To T, Stanojevic S, Moores G, et al. Global asthma prevalence in adults: findings from the cross-sectional world health survey. BMC Public Health 2012;12:204
  • Fuchs O, von Mutius. Prenatal and childhood infections: implications for the development and treatment of childhood asthma. Lancet Respir Med 2013;1(9):743-54
  • Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012;18(5):673-83
  • Li BW, Hendriks RW. Group 2 innate lymphoid cells in lung inflammation. Immunology 2013;140(3):281-7
  • Anderson HR, Gupta R, Strachan DP, Limb ES. 50 years of asthma: UK trends from 1955 to 2004. Thorax 2007;62(1):85-90
  • Pearce N, Ait-Khaled N, Beasley R, et al. Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 2007;62(9):758-66
  • Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299(6710):1259-60
  • Yazdanbakhsh M, Kremsner PG, van RR. Allergy, parasites, and the hygiene hypothesis. Science 2002;296(5567):490-4
  • Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science 2012;335(6071):936-41
  • Blaser MJ, Falkow S. What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 2009;7(12):887-94
  • Umetsu DT, McIntire JJ, Akbari O, et al. Asthma: an epidemic of dysregulated immunity. Nat Immunol 2002;3(8):715-20
  • Rook GA, Martinelli R, Brunet LR. Innate immune responses to mycobacteria and the downregulation of atopic responses. Curr Opin Allergy Clin Immunol 2003;3(5):337-42
  • Cooper PJ. Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol 2009;9(1):29-37
  • Feary J, Britton J, Leonardi-Bee J. Atopy and current intestinal parasite infection: a systematic review and meta-analysis. Allergy 2011;66(4):569-78
  • Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am J Respir Crit Care Med 2006;174(5):514-23
  • Medeiros M Jr, Figueiredo JP, Almeida MC, et al. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 2003;111(5):947-51
  • Araujo MI, Lopes AA, Medeiros M, et al. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 2000;123(2):145-8
  • van den Biggelaar AH, van RR, Rodrigues LC, et al. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000;356(9243):1723-7
  • Flohr C, Quinnell RJ, Britton J. Do helminth parasites protect against atopy and allergic disease? Clin Exp Allergy 2009;39(1):20-32
  • Zaccone P, Cooke A. Vaccine against autoimmune disease: can helminths or their products provide a therapy? Curr Opin Immunol 2013;25(3):418-23
  • Braun-Fahrlander C, Riedler J, Herz U, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002;347(12):869-77
  • Riedler J, Braun-Fahrlander C, Eder W, et al. Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 2001;358(9288):1129-33
  • von Mutius E, Radon K. Living on a farm: impact on asthma induction and clinical course. Immunol Allergy Clin North Am 2008;28(3):631-47
  • Ege MJ, Mayer M, Normand AC, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011;364(8):701-9
  • Hilty M, Burke C, Pedro H, et al. Disordered microbial communities in asthmatic airways. PLoS One 2010;5(1):e8578
  • Marri PR, Stern DA, Wright AL, et al. Asthma-associated differences in microbial composition of induced sputum. J Allergy Clin Immunol 2013;131(2):346-52
  • Goleva E, Jackson LP, Harris JK, et al. The effects of airway microbiome on corticosteroid responsiveness in asthma. Am J Respir Crit Care Med 2013;188(10):1193-201
  • Bisgaard H, Hermansen MN, Buchvald F, et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 2007;357(15):1487-95
  • Folsgaard NV, Schjorring S, Chawes BL, et al. Pathogenic bacteria colonizing the airways in asymptomatic neonates stimulates topical inflammatory mediator release. Am J Respir Crit Care Med 2013;187(6):589-95
  • Matricardi PM, Rosmini F, Panetta V, et al. Hay fever and asthma in relation to markers of infection in the United States. J Allergy Clin Immunol 2002;110(3):381-7
  • Abrahamsson TR, Jakobsson HE, Andersson AF, et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy 2014;44(6):842-50
  • Hoskin-Parr L, Teyhan A, Blocker A, Henderson AJ. Antibiotic exposure in the first two years of life and development of asthma and other allergic diseases by 7.5 yr: a dose-dependent relationship. Pediatr Allergy Immunol 2013;24(8):762-71
  • Marra F, Lynd L, Coombes M, et al. Does antibiotic exposure during infancy lead to development of asthma?: a systematic review and metaanalysis. Chest 2006;129(3):610-18
  • Penders J, Kummeling I, Thijs C. Infant antibiotic use and wheeze and asthma risk: a systematic review and meta-analysis. Eur Respir J 2011;38(2):295-302
  • Chen Y, Blaser MJ. Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med 2007;167(8):821-7
  • Reibman J, Marmor M, Filner J, et al. Asthma is inversely associated with Helicobacter pylori status in an urban population. PLoS One 2008;3(12):e4060
  • Taube C, Muller A. The role of Helicobacter pylori infection in the development of allergic asthma. Expert Rev Respir Med 2012;6(4):441-9
  • Zevit N, Balicer RD, Cohen HA, et al. Inverse association between Helicobacter pylori and pediatric asthma in a high-prevalence population. Helicobacter 2012;17(1):30-5
  • Arnold IC, Hitzler I, Muller A. The immunomodulatory properties of Helicobacter pylori confer protection against allergic and chronic inflammatory disorders. Front Cell Infect Microbiol 2012;2:10
  • Chen Y, Blaser MJ. Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis 2008;198(4):553-60
  • Arnold IC, Dehzad N, Reuter S, et al. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest 2011;121(8):3088-93
  • Oertli M, Sundquist M, Hitzler I, et al. DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylori-specific immune tolerance, and asthma protection. J Clin Invest 2012;122(3):1082-96
  • Oertli M, Noben M, Engler DB, et al. Helicobacter pylori gamma-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc Natl Acad Sci USA 2013;110(8):3047-52
  • Muller A, Oertli M, Arnold IC. H. pylori exploits and manipulates innate and adaptive immune cell signaling pathways to establish persistent infection. Cell Commun Signal 2011;9(1):25
  • Araujo CA, Perini A, Martins MA, et al. PAS-1, a protein from Ascaris suum, modulates allergic inflammation via IL-10 and IFN-gamma, but not IL-12. Cytokine 2008;44(3):335-41
  • Kim SE, Kim JH, Min BH, et al. Crude extracts of Caenorhabditis elegans suppress airway inflammation in a murine model of allergic asthma. PLoS One 2012;7(4):e35447
  • Lin WH, Wu CR, Lee HZ, et al. Induced apoptosis of Th2 lymphocytes and inhibition of airway hyperresponsiveness and inflammation by combined lactic acid bacteria treatment. Int Immunopharmacol 2013;15(4):703-11
  • Rzepecka J, Siebeke I, Coltherd JC, et al. The helminth product, ES-62, protects against airway inflammation by resetting the Th cell phenotype. Int J Parasitol 2013;43(3-4):211-23
  • Wu CJ, Chen LC, Kuo ML. Attenuated Salmonella typhimurium reduces ovalbumin-induced airway inflammation and T-helper type 2 responses in mice. Clin Exp Immunol 2006;145(1):116-22
  • Danilowicz-Luebert E, Steinfelder S, Kuhl AA, et al. A nematode immunomodulator suppresses grass pollen-specific allergic responses by controlling excessive Th2 inflammation. Int J Parasitol 2013;43(3-4):201-10
  • Trujillo-Vargas CM, Werner-Klein M, Wohlleben G, et al. Helminth-derived products inhibit the development of allergic responses in mice. Am J Respir Crit Care Med 2007;175(4):336-44
  • Hirose I, Tanaka H, Takahashi G, et al. Immunomodulatory effects of CpG oligodeoxynucleotides on house dust mite-induced airway inflammation in mice. Int Arch Allergy Immunol 2008;147(1):6-16
  • Codolo G, Mazzi P, Amedei A, et al. The neutrophil-activating protein of Helicobacter pylori down-modulates Th2 inflammation in ovalbumin-induced allergic asthma. Cell Microbiol 2008;10(11):2355-63
  • Amedei A, Cappon A, Codolo G, et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest 2006;116(4):1092-101
  • Parronchi P, Brugnolo F, Annunziato F, et al. Phosphorothioate oligodeoxynucleotides promote the in vitro development of human allergen-specific CD4+ T cells into Th1 effectors. J Immunol 1999;163(11):5946-53
  • Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 2012;30:531-64
  • Shevach EM, Thornton AM. tTregs, pTregs, and iTregs: similarities and differences. Immunol Rev 2014;259(1):88-102
  • Aranzamendi C, Fransen F, Langelaar M, et al. Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro. Parasite Immunol 2012;34(4):210-23
  • Dittrich AM, Erbacher A, Specht S, et al. Helminth infection with Litomosoides sigmodontis induces regulatory T cells and inhibits allergic sensitization, airway inflammation, and hyperreactivity in a murine asthma model. J Immunol 2008;180(3):1792-9
  • Hartmann S, Schnoeller C, Dahten A, et al. Gastrointestinal nematode infection interferes with experimental allergic airway inflammation but not atopic dermatitis. Clin Exp Allergy 2009;39(10):1585-96
  • Kitagaki K, Businga TR, Racila D, et al. Intestinal helminths protect in a murine model of asthma. J Immunol 2006;177(3):1628-35
  • Layland LE, Straubinger K, Ritter M, et al. Schistosoma mansoni-mediated suppression of allergic airway inflammation requires patency and Foxp3+ Treg cells. PLoS Negl Trop Dis 2013;7(8):e2379
  • Park HK, Cho MK, Choi SH, et al. Trichinella spiralis: infection reduces airway allergic inflammation in mice. Exp Parasitol 2011;127(2):539-44
  • Wilson MS, Taylor MD, Balic A, et al. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 2005;202(9):1199-212
  • Wohlleben G, Trujillo C, Muller J, et al. Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 2004;16(4):585-96
  • McSorley HJ, Maizels RM. Helminth infections and host immune regulation. Clin Microbiol Rev 2012;25(4):585-608
  • Feleszko W, Jaworska J, Rha RD, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 2007;37(4):498-505
  • Li YN, Huang F, Liu L, et al. Effect of oral feeding with Clostridium leptum on regulatory T-cell responses and allergic airway inflammation in mice. Ann Allergy Asthma Immunol 2012;109(3):201-7
  • Cardoso LS, Oliveira SC, Goes AM, et al. Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation. Clin Exp Immunol 2010;160(2):266-74
  • de Araujo CA, Perini A, Martins MA, et al. PAS-1, an Ascaris suum protein, modulates allergic airway inflammation via CD8+gammadeltaTCR+ and CD4+CD25+FoxP3+ T cells. Scand J Immunol 2010;72(6):491-503
  • Park SK, Cho MK, Park HK, et al. Macrophage migration inhibitory factor homologs of anisakis simplex suppress Th2 response in allergic airway inflammation model via CD4+CD25+Foxp3+ T cell recruitment. J Immunol 2009;182(11):6907-14
  • Kawashima S, Hirose K, Iwata A, et al. β-glucan curdlan induces IL-10-producing CD4+ T cells and inhibits allergic airway inflammation. J Immunol 2012;189(12):5713-21
  • Lagranderie M, Abolhassani M, Vanoirbeek J, et al. Mycobacterium bovis BCG killed by extended freeze-drying reduces airway hyperresponsiveness in 2 animal models. J Allergy Clin Immunol 2008;121(2):471-8
  • Lagranderie M, Abolhassani M, Vanoirbeek JA, et al. Mycobacterium bovis bacillus Calmette-Guerin killed by extended freeze-drying targets plasmacytoid dendritic cells to regulate lung inflammation. J Immunol 2010;184(2):1062-70
  • Navarro S, Cossalter G, Chiavaroli C, et al. The oral administration of bacterial extracts prevents asthma via the recruitment of regulatory T cells to the airways. Mucosal Immunol 2011;4(1):53-65
  • Thorburn AN, Foster PS, Gibson PG, Hansbro PM. Components of Streptococcus pneumoniae suppress allergic airways disease and NKT cells by inducing regulatory T cells. J Immunol 2012;188(9):4611-20
  • Schabussova I, Hufnagl K, Tang ML, et al. Perinatal maternal administration of Lactobacillus paracasei NCC 2461 prevents allergic inflammation in a mouse model of birch pollen allergy. PLoS One 2012;7(7):e40271
  • Pacifico LG, Marinho FA, Fonseca CT, et al. Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3+ T cells independent of interleukin-10. Infect Immun 2009;77(1):98-107
  • Mangan NE, van RN, McKenzie AN, Fallon PG. Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 2006;176(1):138-47
  • van der Vlugt LE, Labuda LA, Ozir-Fazalalikhan A, et al. Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS One 2012;7(2):e30883
  • Wilson MS, Taylor MD, O’Gorman MT, et al. Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 2010;40(6):1682-96
  • Rosser EC, Blair PA, Mauri C. Cellular targets of regulatory B cell-mediated suppression. Mol Immunol 2014. [Epub ahead of print]
  • Amu S, Saunders SP, Kronenberg M, et al. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 2010;125(5):1114-24
  • Neves P, Lampropoulou V, Calderon-Gomez E, et al. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity 2010;33(5):777-90
  • Sayi A, Kohler E, Toller IM, et al. TLR-2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J Immunol 2011;186(2):878-90
  • Wei L, Wang J, Liu Y. Prior to Foxp3 regulatory T-cell induction, interleukin-10-producing B cells expand after Helicobacter pylori infection. Pathog Dis 2014. [Epub ahead of print]
  • Zhang M, Zheng X, Zhang J, et al. CD19(+)CD1d(+)CD5(+) B cell frequencies are increased in patients with tuberculosis and suppress Th17 responses. Cell Immunol 2012;274(1-2):89-97
  • Atarashi K, Tanoue T, Oshima K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013;500(7461):232-6
  • Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504(7480):446-50
  • Trompette A, Gollwitzer ES, Yadava K, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014;20(2):159-66
  • Hussaarts L, van der Vlugt LE, Yazdanbakhsh M, Smits HH. Regulatory B-cell induction by helminths: implications for allergic disease. J Allergy Clin Immunol 2011;128(4):733-9
  • Everts B, Smits HH, Hokke CH, Yazdanbakhsh M. Helminths and dendritic cells: sensing and regulating via pattern recognition receptors, Th2 and Treg responses. Eur J Immunol 2010;40(6):1525-37
  • Ludwig-Portugall I, Layland LE. TLRs, Treg, and B Cells, an Interplay of Regulation during Helminth Infection. Front Immunol 2012;3:8
  • van der Kleij D, Latz E, Brouwers JF, et al. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem 2002;277(50):48122-9
  • Jeong YI, Kim SH, Ju JW, et al. Clonorchis sinensis-derived total protein attenuates airway inflammation in murine asthma model by inducing regulatory T cells and modulating dendritic cell functions. Biochem Biophys Res Commun 2011;407(4):793-800
  • Anthony RM, Urban JF Jr, Alem F, et al. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat Med 2006;12(8):955-60
  • Maizels RM, Balic A, Gomez-Escobar N, et al. Helminth parasites – masters of regulation. Immunol Rev 2004;201:89-116
  • Pesce JT, Ramalingam TR, Wilson MS, et al. Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog 2009;5(4):e1000393
  • Reece JJ, Siracusa MC, Scott AL. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect Immun 2006;74(9):4970-81
  • Schnoeller C, Rausch S, Pillai S, et al. A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J Immunol 2008;180(6):4265-72
  • Stiehm M, Peters K, Wiesmuller KH, et al. A novel synthetic lipopeptide is allergy-protective by the induction of LPS-tolerance. Clin Exp Allergy 2013;43(7):785-97
  • Wang CC, Nolan TJ, Schad GA, Abraham D. Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin. Clin Exp Allergy 2001;31(3):495-503
  • Rzepecka J, Donskow-Schmelter K, Doligalska M. Heligmosomoides polygyrus infection down-regulates eotaxin concentration and CCR3 expression on lung eosinophils in murine allergic pulmonary inflammation. Parasite Immunol 2007;29(8):405-13
  • Datti F, Datti M, Antunes E. Prenatal exposure to endotoxin in rats attenuates the allergic airways eosinophil infiltration in the adult offspring: role of inducible nitric oxide synthase activation. Pulm Pharmacol Ther 2008;21(2):349-55
  • Herbst T, Sichelstiel A, Schar C, et al. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am J Respir Crit Care Med 2011;184(2):198-205
  • Olszak T, An D, Zeissig S, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012;336(6080):489-93
  • Hill DA, Siracusa MC, Abt MC, et al. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med 2012;18(4):538-46
  • McSorley HJ, Blair NF, Smith KA, et al. Blockade of IL-33 release and suppression of type 2 innate lymphoid cell responses by helminth secreted products in airway allergy. Mucosal Immunol 2014. [Epub ahead of print]
  • Melendez AJ, Harnett MM, Pushparaj PN, et al. Inhibition of Fc epsilon RI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nat Med 2007;13(11):1375-81
  • Amoah AS, Obeng BB, Larbi IA, et al. Peanut-specific IgE antibodies in asymptomatic Ghanaian children possibly caused by carbohydrate determinant cross-reactivity. J Allergy Clin Immunol 2013;132(3):639-47
  • Nembrini C, Sichelstiel A, Kisielow J, et al. Bacterial-induced protection against allergic inflammation through a multicomponent immunoregulatory mechanism. Thorax 2011;66(9):755-63
  • Tan Y, Liu H, Yang H, et al. An inactivated Pseudomonas aeruginosa medicament inhibits airway allergic inflammation and improves epithelial functions. J Physiol Sci 2013;63(1):63-9
  • Garg SK, Croft AM, Bager P. Helminth therapy (worms) for induction of remission in inflammatory bowel disease. Cochrane Database Syst Rev 2014;1:CD009400
  • Sandborn WJ, Elliott DE, Weinstock J, et al. Randomised clinical trial: the safety and tolerability of Trichuris suis ova in patients with Crohn’s disease. Aliment Pharmacol Ther 2013;38(3):255-63
  • Summers RW, Elliott DE, Urban JF Jr, et al. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 2005;128(4):825-32
  • Rosche B, Wernecke KD, Ohlraun S, et al. Trichuris suis ova in relapsing-remitting multiple sclerosis and clinically isolated syndrome (TRIOMS): study protocol for a randomized controlled trial. Trials 2013;14:112
  • Bager P, Arnved J, Ronborg S, et al. Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol 2010;125(1):123-30
  • Bourke CD, Mutapi F, Nausch N, et al. Trichuris suis ova therapy for allergic rhinitis does not affect allergen-specific cytokine responses despite a parasite-specific cytokine response. Clin Exp Allergy 2012;42(11):1582-95
  • Mortaz E, Adcock IM, Folkerts G, et al. Probiotics in the management of lung diseases. Mediators Inflamm 2013;2013:751068
  • Forsythe P. Probiotics and lung immune responses. Ann Am Thorac Soc 2014;11(Suppl 1)):S33-7
  • Azad MB, Coneys JG, Kozyrskyj AL, et al. Probiotic supplementation during pregnancy or infancy for the prevention of asthma and wheeze: systematic review and meta-analysis. BMJ 2013;347:f6471
  • Pelucchi C, Chatenoud L, Turati F, et al. Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis. Epidemiology 2012;23(3):402-14
  • Lau S, Gerhold K, Zimmermann K, et al. Oral application of bacterial lysate in infancy decreases the risk of atopic dermatitis in children with 1 atopic parent in a randomized, placebo-controlled trial. J Allergy Clin Immunol 2012;129(4):1040-7
  • Zhang J, Guo S, Li C, Jiang X. Therapeutic effects of inhaled inactivated Mycobacterium phlei in adult patients with moderate persistent asthma. Immunotherapy 2012;4(4):383-7
  • Lima C, Perini A, Garcia ML, et al. Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clin Exp Allergy 2002;32(11):1659-66
  • Yang J, Zhao J, Yang Y, et al. Schistosoma japonicum egg antigens stimulate CD4 CD25 T cells and modulate airway inflammation in a murine model of asthma. Immunology 2007;120(1):8-18
  • Lee KH, Park HK, Jeong HJ, et al. Immunization of proteins from Toxascaris leonina adult worm inhibits allergic specific Th2 response. Vet Parasitol 2008;156(3-4):216-25
  • McSorley HJ, O’Gorman MT, Blair N, et al. Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminth Heligmosomoides polygyrus. Eur J Immunol 2012;42(10):2667-82
  • Itami DM, Oshiro TM, Araujo CA, et al. Modulation of murine experimental asthma by Ascaris suum components. Clin Exp Allergy 2005;35(7):873-9
  • de Boer DJ, Roelofs JJ, de Vos AF, et al. Lipopolysaccharide inhibits Th2 lung inflammation induced by house dust mite allergens in mice. Am J Respir Cell Mol Biol 2013;48(3):382-9
  • Zhu Z, Oh SY, Zheng T, Kim YK. Immunomodulating effects of endotoxin in mouse models of allergic asthma. Clin Exp Allergy 2010;40(4):536-46
  • Li R, Cheng C, Chong SZ, et al. Attenuated Bordetella pertussis BPZE1 protects against allergic airway inflammation and contact dermatitis in mouse models. Allergy 2012;67(10):1250-8
  • Schabussova I, Ul-Haq O, Hoflehner E, et al. Oesophagostomum dentatum extract modulates T cell-dependent immune responses to bystander antigens and prevents the development of allergy in mice. PLoS One 2013;8(7):e67544
  • Allard JB, Rinaldi L, Wargo MJ, et al. Th2 allergic immune response to inhaled fungal antigens is modulated by TLR-4-independent bacterial products. Eur J Immunol 2009;39(3):776-88
  • Brand S, Teich R, Dicke T, et al. Epigenetic regulation in murine offspring as a novel mechanism for transmaternal asthma protection induced by microbes. J Allergy Clin Immunol 2011;128(3):618-25
  • Moingeon P, Mascarell L. Novel routes for allergen immunotherapy: safety, efficacy and mode of action. Immunotherapy 2012;4(2):201-12
  • Erb KJ. Can helminths or helminth-derived products be used in humans to prevent or treat allergic diseases? Trends Immunol 2009;30(2):75-82
  • Tilp C, Kapur V, Loging W, Erb KJ. Prerequisites for the pharmaceutical industry to develop and commercialise helminths and helminth-derived product therapy. Int J Parasitol 2013;43(3-4):319-25
  • Bethony JM, Simon G, Diemert DJ, et al. Randomized, placebo-controlled, double-blind trial of the Na-ASP-2 hookworm vaccine in unexposed adults. Vaccine 2008;26(19):2408-17
  • Diemert DJ, Pinto AG, Freire J, et al. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J Allergy Clin Immunol 2012;130(1):169-76
  • Barnes PJ. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J Allergy Clin Immunol 2013;131(3):636-45

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.