240
Views
25
CrossRef citations to date
0
Altmetric
Review

The role of Helicobacter pylori infection in the development of allergic asthma

&
Pages 441-449 | Published online: 09 Jan 2014

References

  • No authors listed. The ENFUMOSA cross-sectional European multicentre study of the clinical phenotype of chronic severe asthma. European Network for Understanding Mechanisms of Severe Asthma. Eur. Respir. J. 22, 470–477 (2003).
  • Rogers AJ, Raby BA, Lasky-Su JA et al. Assessing the reproducibility of asthma candidate gene associations, using genomewide data. Am. J. Respir. Crit. Care Med. 179(12), 1084–1090 (2009).
  • Renz H, von Mutius E, Brandtzaeg P, Cookson WO, Autenrieth IB, Haller D. Gene–environment interactions in chronic inflammatory disease. Nat. Immunol. 12(4), 273–277 (2011).
  • Braun-Fahrländer C, Riedler J, Herz U et al.; Allergy and Endotoxin Study Team. Environmental exposure to endotoxin and its relation to asthma in school-age children. N. Engl. J. Med. 347(12), 869–877 (2002).
  • Ege MJ, Mayer M, Normand AC et al.; GABRIELA Transregio 22 Study Group. Exposure to environmental microorganisms and childhood asthma. N. Engl. J. Med. 364(8), 701–709 (2011).
  • Anderson GP. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 372(9643), 1107–1119 (2008).
  • Wenzel SE. Asthma: defining of the persistent adult phenotypes. Lancet 368(9537), 804–813 (2006).
  • Haldar P, Pavord ID. Noneosinophilic asthma: a distinct clinical and pathologic phenotype. J. Allergy Clin. Immunol. 119(5), 1043–1052; quiz 1053 (2007).
  • Woodruff PG, Modrek B, Choy DF et al. T-helper type 2-driven inflammation defines major subphenotypes of asthma. Am. J. Respir. Crit. Care Med. 180(5), 388–395 (2009).
  • Corren J, Lemanske RF, Hanania NA et al. Lebrikizumab treatment in adults with asthma. N. Engl. J. Med. 365(12), 1088–1098 (2011).
  • Dehzad N, Bopp T, Reuter S et al. Regulatory T cells more effectively suppress Th1-induced airway inflammation compared with Th2. J. Immunol. 186(4), 2238–2244 (2011).
  • McKinley L, Alcorn JF, Peterson A et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181(6), 4089–4097 (2008).
  • Kudo M, Melton AC, Chen C et al. IL-17A produced by αβ T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat. Med. 18(4), 547–554 (2012).
  • Locksley RM. Asthma and allergic inflammation. Cell 140(6), 777–783 (2010).
  • Moro K, Yamada T, Tanabe M et al. Innate production of T(h)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463(7280), 540–544 (2010).
  • Saenz SA, Siracusa MC, Perrigoue JG et al. IL-25 elicits a multipotent progenitor cell population that promotes T(h)2 cytokine responses. Nature 464(7293), 1362–1366 (2010).
  • Neill DR, Wong SH, Bellosi A et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464(7293), 1367–1370 (2010).
  • Price AE, Liang HE, Sullivan BM et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl Acad. Sci. USA 107(25), 11489–11494 (2010).
  • Wilhelm C, Hirota K, Stieglitz B et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat. Immunol. 12(11), 1071–1077 (2011).
  • Mjösberg JM, Trifari S, Crellin NK et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat. Immunol. 12(11), 1055–1062 (2011).
  • Monticelli LA, Sonnenberg GF, Abt MC et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12(11), 1045–1054 (2011).
  • Lambrecht BN, Hammad H. The role of dendritic and epithelial cells as master regulators of allergic airway inflammation. Lancet 376(9743), 835–843 (2010).
  • Reinhardt RL, Liang HE, Locksley RM. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10(4), 385–393 (2009).
  • Taube C, Duez C, Cui ZH et al. The role of IL-13 in established allergic airway disease. J. Immunol. 169(11), 6482–6489 (2002).
  • Grünig G, Warnock M, Wakil AE et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282(5397), 2261–2263 (1998).
  • Wills-Karp M, Luyimbazi J, Xu X et al. Interleukin-13: central mediator of allergic asthma. Science 282(5397), 2258–2261 (1998).
  • Blaser MJ, Falkow S. What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7(12), 887–894 (2009).
  • Strachan DP. Hay fever, hygiene, and household size. BMJ 299(6710), 1259–1260 (1989).
  • Matricardi PM, Rosmini F, Panetta V, Ferrigno L, Bonini S. Hay fever and asthma in relation to markers of infection in the United States. J. Allergy Clin. Immunol. 110(3), 381–387 (2002).
  • McLoughlin RM, Mills KH. Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma. J. Allergy Clin. Immunol. 127(5), 1097–1107; quiz 1108 (2011).
  • Gill SR, Pop M, Deboy RT et al. Metagenomic analysis of the human distal gut microbiome. Science 312(5778), 1355–1359 (2006).
  • Guarner F, Malagelada JR. Gut flora in health and disease. Lancet 361(9356), 512–519 (2003).
  • Ly NP, Litonjua A, Gold DR, Celedón JC. Gut microbiota, probiotics, and vitamin D: interrelated exposures influencing allergy, asthma, and obesity? J. Allergy Clin. Immunol. 127(5), 1087–1094; quiz 1095 (2011).
  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 5(7), e177 (2007).
  • Herbst T, Sichelstiel A, Schär C et al. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am. J. Respir. Crit. Care Med. 184(2), 198–205 (2011).
  • Reis BS, Mucida D. The role of the intestinal context in the generation of tolerance and inflammation. Clin. Dev. Immunol. 2012, 157948 (2012).
  • Prescott SL, Macaubas C, Holt BJ et al. Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J. Immunol. 160(10), 4730–4737 (1998).
  • Monteleone I, Platt AM, Jaensson E, Agace WW, Mowat AM. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur. J. Immunol. 38(6), 1533–1547 (2008).
  • Niess JH, Adler G. Enteric flora expands gut lamina propria CX3CR1+ dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J. Immunol. 184(4), 2026–2037 (2010).
  • Cong Y, Wang L, Konrad A, Schoeb T, Elson CO. Curcumin induces the tolerogenic dendritic cell that promotes differentiation of intestine-protective regulatory T cells. Eur. J. Immunol. 39(11), 3134–3146 (2009).
  • Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8(10), 1086–1094 (2007).
  • Coombes JL, Siddiqui KR, Arancibia-Cárcamo CV et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204(8), 1757–1764 (2007).
  • Shirai Y, Hashimoto M, Kato R et al. Lipopolysaccharide induces CD25-positive, IL-10-producing lymphocytes without secretion of proinflammatory cytokines in the human colon: low MD-2 mRNA expression in colonic macrophages. J. Clin. Immunol. 24(1), 42–52 (2004).
  • Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl Acad. Sci. USA 107(27), 12204–12209 (2010).
  • Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453(7195), 620–625 (2008).
  • Ochoa-Repáraz J, Mielcarz DW, Ditrio LE et al. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J. Immunol. 185(7), 4101–4108 (2010).
  • Olszak T, An D, Zeissig S et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336(6080), 489–493 (2012).
  • Hill DA, Siracusa MC, Abt MC et al. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat. Med. 18(4), 538–546 (2012).
  • Bik EM, Eckburg PB, Gill SR et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl Acad. Sci. USA 103(3), 732–737 (2006).
  • Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3(7), e2836 (2008).
  • Linz B, Balloux F, Moodley Y et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445(7130), 915–918 (2007).
  • Taylor DN, Blaser MJ. The epidemiology of Helicobacter pylori infection. Epidemiol. Rev. 13, 42–59 (1991).
  • Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA. The cohort effect and Helicobacter pylori. J. Infect. Dis. 168(1), 219–221 (1993).
  • Malaty HM, El-Kasabany A, Graham DY et al. Age at acquisition of Helicobacter pylori infection: a follow-up study from infancy to adulthood. Lancet 359(9310), 931–935 (2002).
  • Cullen DJ, Collins BJ, Christiansen KJ et al. When is Helicobacter pylori infection acquired? Gut 34(12), 1681–1682 (1993).
  • Kuipers EJ, Peña AS, van Kamp G et al. Seroconversion for Helicobacter pylori. Lancet 342(8867), 328–331 (1993).
  • Chen Y, Blaser MJ. Helicobacter pylori colonization is inversely associated with childhood asthma. J. Infect. Dis. 198(4), 553–560 (2008).
  • Rothenbacher D, Bode G, Brenner H. History of breastfeeding and Helicobacter pylori infection in pre-school children: results of a population-based study from Germany. Int. J. Epidemiol. 31(3), 632–637 (2002).
  • Nahar S, Kibria KM, Hossain ME et al. Evidence of intra-familial transmission of Helicobacter pylori by PCR-based RAPD fingerprinting in Bangladesh. Eur. J. Clin. Microbiol. Infect. Dis. 28(7), 767–773 (2009).
  • den Hoed CM, Vila AJ, Holster IL et al. Helicobacter pylori and the birth cohort effect: evidence for stabilized colonization rates in childhood. Helicobacter 16(5), 405–409 (2011).
  • Dooley CP, Cohen H, Fitzgibbons PL et al. Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons. N. Engl. J. Med. 321(23), 1562–1566 (1989).
  • Kosunen TU, Aromaa A, Knekt P et al. Helicobacter antibodies in 1973 and 1994 in the adult population of Vammala, Finland. Epidemiol. Infect. 119(1), 29–34 (1997).
  • Perez-Perez GI, Salomaa A, Kosunen TU et al. Evidence that CagA(+) Helicobacter pylori strains are disappearing more rapidly than CagA(−) strains. Gut 50(3), 295–298 (2002).
  • Kosunen TU, Höök-Nikanne J, Salomaa A, Sarna S, Aromaa A, Haahtela T. Increase of allergen-specific immunoglobulin E antibodies from 1973 to 1994 in a Finnish population and a possible relationship to Helicobacter pylori infections. Clin. Exp. Allergy 32(3), 373–378 (2002).
  • Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 4(9), 688–694 (2004).
  • Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH. Meta-analysis of the relationship between CagA seropositivity and gastric cancer. Gastroenterology 125(6), 1636–1644 (2003).
  • Chen Y, Blaser MJ. Inverse associations of Helicobacter pylori with asthma and allergy. Arch. Intern. Med. 167(8), 821–827 (2007).
  • Thjodleifsson B, Asbjornsdottir H, Sigurjonsdottir RB et al. Seroprevalence of Helicobacter pylori and CagA antibodies in Iceland, Estonia and Sweden. Scand. J. Infect. Dis. 39(8), 683–689 (2007).
  • von Hertzen LC, Laatikainen T, Mäkelä MJ et al. Infectious burden as a determinant of atopy – a comparison between adults in Finnish and Russian Karelia. Int. Arch. Allergy Immunol. 140(2), 89–95 (2006).
  • Reibman J, Marmor M, Filner J et al. Asthma is inversely associated with Helicobacter pylori status in an urban population. PLoS ONE 3(12), e4060 (2008).
  • Matricardi PM, Rosmini F, Riondino S et al. Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. BMJ 320(7232), 412–417 (2000).
  • McCune A, Lane A, Murray L et al. Reduced risk of atopic disorders in adults with Helicobacter pylori infection. Eur. J. Gastroenterol. Hepatol. 15(6), 637–640 (2003).
  • Tsang KW, Lam WK, Chan KN et al. Helicobacter pylori sero-prevalence in asthma. Respir. Med. 94(8), 756–759 (2000).
  • Pessi T, Virta M, Adjers K et al. Genetic and environmental factors in the immunopathogenesis of atopy: interaction of Helicobacter pylori infection and IL-4 genetics. Int. Arch. Allergy Immunol. 137(4), 282–288 (2005).
  • Jarvis D, Luczynska C, Chinn S, Burney P. The association of hepatitis A and Helicobacter pylori with sensitization to common allergens, asthma and hay fever in a population of young British adults. Allergy 59(10), 1063–1067 (2004).
  • Arnold IC, Lee JY, Amieva MR et al. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 140(1), 199–209 (2011).
  • Harris PR, Wright SW, Serrano C et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 134(2), 491–499 (2008).
  • 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. 121(8), 3088–3093 (2011).
  • Amedei A, Cappon A, Codolo G et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J. Clin. Invest. 116(4), 1092–1101 (2006).
  • 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. 10(11), 2355–2363 (2008).
  • Onishi Y, Fehervari Z, Yamaguchi T, Sakaguchi S. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl Acad. Sci. USA 105(29), 10113–10118 (2008).
  • Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv. Immunol. 108, 111–165 (2010).
  • Kretschmer K, Apostolou I, Hawiger D, Khazaie K, Nussenzweig MC, von Boehmer H. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6(12), 1219–1227 (2005).
  • 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. 122(3), 1082–1096 (2012).
  • Bergman MP, Engering A, Smits HH et al. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200(8), 979–990 (2004).
  • Kao JY, Zhang M, Miller MJ et al. Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138(3), 1046–1054 (2010).
  • Hitzler I, Oertli M, Becher B, Agger EM, Müller A. Dendritic cells prevent rather than promote immunity conferred by a Helicobacter vaccine using a mycobacterial adjuvant. Gastroenterology 141(1), 186–196, 196.e1 (2011).

Website

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.