Hostname: page-component-7bb8b95d7b-pwrkn Total loading time: 0 Render date: 2024-09-20T17:23:06.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Programming of the lung by early-life infection

Published online by Cambridge University Press:  14 February 2012

P. M. Hansbro ,
M. R. Starkey ,
R. Y. Kim ,
R. L. Stevens ,
P. S. Foster  and
J. C. Horvat
P. M. Hansbro*
Affiliation:
Centre for Asthma and Respiratory Disease and Hunter Medical Research Institute, The University of Newcastle, Newcastle, Australia
M. R. Starkey
Affiliation:
Centre for Asthma and Respiratory Disease and Hunter Medical Research Institute, The University of Newcastle, Newcastle, Australia
R. Y. Kim
Affiliation:
Centre for Asthma and Respiratory Disease and Hunter Medical Research Institute, The University of Newcastle, Newcastle, Australia
R. L. Stevens
Affiliation:
Department of Medicine, Harvard Medical School and Brigham and Women's Hospital, Boston, Massachusetts, USA
P. S. Foster
Affiliation:
Centre for Asthma and Respiratory Disease and Hunter Medical Research Institute, The University of Newcastle, Newcastle, Australia
J. C. Horvat
Affiliation:
Centre for Asthma and Respiratory Disease and Hunter Medical Research Institute, The University of Newcastle, Newcastle, Australia
*
*Address for correspondence: Professor P. M. Hansbro, Infection and Immunity, The David Maddison Clinical Sciences Building, The University of Newcastle, Cnr King and Watt Sts, Newcastle, NSW 2300, Australia. (Email Philip.Hansbro@newcastle.edu.au)
Get access Rights & Permissions [Opens in a new window]

Abstract

Many important human diseases, such as asthma, have their developmental origins in early life. Respiratory infections in particular may alter the course of asthma and may either protect against or promote the development of this disease. It is likely that the nature of the effects depends on the type and age of infection and is determined by the impact of infection on the immune and respiratory systems. Immunity in early life is plastic and can be moulded by antigen encounter, which may enhance or reinforce the asthmatic phenotype of early life, or induce protective responses. Chlamydial respiratory infections have specific effects and may increase asthma severity in early life by promoting systemic interleukin 13 responses and causing permanent changes in lung structure. Respiratory viral infections, such as those of respiratory syncytial virus and rhinovirus, promote pro-asthmatic responses in early life that contribute to the induction of asthma. By contrast, probiotics or infection or exposure to certain bacteria, such as Streptococcus pneumoniae, may have protective effects in asthma by increasing the numbers and activity of regulatory T cells. Here, we review the impact of infections on the developmental origins of asthma. Understanding these effects may lead to new therapeutic approaches for asthma that either target deleterious infections or utilize beneficial ones.

Keywords

developmental origins of diseaseimmunityinfectionlung structurerespiratory
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 3 , June 2012 , pp. 153 - 158
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Bush, A. Asthma research: the real action is in children. Paediatr Respir Rev. 2005; 6, 101–110.CrossRefGoogle ScholarPubMed
2. Prescott, S. The development of respiratory inflammation in children. Paediatr Respir Rev. 2006; 7, 89–96.CrossRefGoogle ScholarPubMed
3. Hansbro, PM, Beagley, KW, Horvat, JC, Gibson, PG. Role of atypical bacterial infection of the lung in predisposition/protection of asthma. Pharmacol Ther. 2004; 101, 193–210.CrossRefGoogle ScholarPubMed
4. Hansbro, NG, Horvat, JC, Wark, PA, Hansbro, PM. Understanding the mechanisms of viral induced asthma: new therapeutic directions. Pharmacol Ther. 2008; 117, 313–353.CrossRefGoogle ScholarPubMed
5. Maslowski, K, Mackay, C. Diet, gut microbiota and immune responses. Nat Immunol. 2011; 12, 5–9.CrossRefGoogle ScholarPubMed
6. Nagel, G, Weinmayr, G, Kleiner, A, et al. Effect of diet on asthma and allergic sensitisation in the International Study on Allergies and Asthma in Childhood (ISAAC) Phase Two. Thorax. 2010; 65, 516–522.CrossRefGoogle Scholar
7. Ly, N, Litonjua, A, Gold, D, Celedón, J. Gut microbiota, probiotics, and vitamin D: interrelated exposures influencing allergy, asthma, and obesity? J Allergy Clin Immunol. 2011; 127, 1087–1094.CrossRefGoogle ScholarPubMed
8. Jensen, M, Collins, C, Gibson, P, Wood, L. The obesity phenotype in children with asthma. Paediatr Respir Rev. 2011; 12, 152–159.CrossRefGoogle ScholarPubMed
9. Culley, FJ, Pollott, J, Openshaw, PJM. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J Exp Med. 2002; 196, 1381–1386.CrossRefGoogle ScholarPubMed
10. Horvat, J, Beagley, K, Wade, M, et al. Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease. Am J Respir Crit Care Med. 2007; 176, 556–564.CrossRefGoogle ScholarPubMed
11. Horvat, J, Starkey, M, Kim, R, et al. Early-life chlamydial lung infection enhances allergic airways disease through age-dependent differences in immunopathology. J Allergy Clin Immunol. 2010; 125, 617–625.CrossRefGoogle ScholarPubMed
12. Thorburn, A, Hansbro, P. Harnessing regulatory T cells to suppress asthma: from potential to therapy. Am J Respir Cell Mol Biol. 2010; 43, 511–519.CrossRefGoogle ScholarPubMed
13. Webley, WC, Tilahun, Y, Lay, K, et al. Occurrence of Chlamydia trachomatis and Chlamydia pneumoniae in paediatric respiratory infections. Eur Respir J. 2009; 33, 360–367.CrossRefGoogle ScholarPubMed
14. Barreto, M, Bonafoni, S, Barberi, S, et al. Does a parent-reported history of pneumonia increase the likelihood of respiratory symptoms needing therapy in asthmatic children and adolescents? J Asthma. 2011; 48, 714–720.CrossRefGoogle ScholarPubMed
15. Karimi, K, Inman, M, Bienenstock, J, Forsythe, P. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med. 2009; 179, 186–193.CrossRefGoogle ScholarPubMed
16. Arnold, I, 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, 3088–3093.CrossRefGoogle ScholarPubMed
17. Dharmage, S, Erbas, B, Jarvis, D, et al. Do childhood respiratory infections continue to influence adult respiratory morbidity? Eur Respir J. 2009; 33, 237–244.CrossRefGoogle ScholarPubMed
18. Hansbro, P, Kaiko, G, Foster, P. Cytokine/anti-cytokine therapy – novel treatments for asthma? Br J Pharmacol. 2011; 163, 81–95.CrossRefGoogle ScholarPubMed
19. Kaiko, G, Phipps, S, Hickey, D, et al. Chlamydia muridarum infection subverts dendritic cell function to promote Th2 immunity and airways hyperreactivity. J Immunol. 2008; 180, 2225–2232.CrossRefGoogle ScholarPubMed
20. Kaiko, G, Horvat, J, Beagley, K, Hansbro, P. Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology. 2008; 123, 326–338.CrossRefGoogle Scholar
21. Yang, X, Gao, X. Role of dendritic cells: a step forward for the hygiene hypothesis. Cell Mol Immunol. 2011; 8, 12–18.CrossRefGoogle ScholarPubMed
22. Wynne, O, Horvat, J, Kim, R, et al. Neonatal respiratory infection and adult re-infection: effect on GR and MR in the hippocampus in BALB/c mice. Brain Behav Immun. 2011; 25, 1214–1222.CrossRefGoogle Scholar
23. Wynne, O, Horvat, J, Osei-Kumar, A, et al. Early life infection permanently alters hippocampal gene expression in a sex specific manner. Stress. 2011; 14, 247–261.CrossRefGoogle Scholar
24. Wynne, O, Horvat, J, Osei-Kumar, A, et al. Effect of neonatal Chlamydia muridarum infection on adult hippocampal glucocorticoid and mineralcorticoid receptors. Dev Psychobiol. 2012; doi:10.1002/dev.20615.CrossRefGoogle Scholar
25. Singh, M, Ranjan Das, R. Probiotics for allergic respiratory diseases – putting it into perspective. Pediatr Allergy Immunol. 2009; 2, 3368–3376.Google Scholar
26. Preston, J, Thorburn, A, Starkey, M, et al. Respiratory Streptococcus pneumoniae infection suppresses allergic airways disease through the induction of regulatory T cells. Eur Respir J. 2011; 37, 53–64.CrossRefGoogle Scholar
27. Preston, J, Essilfie, A, Horvat, J, et al. Inhibition of allergic airways disease by immunomodulatory therapy with whole killed Streptococcus pneumoniae . Vaccine. 2007; 25, 8154–8162.CrossRefGoogle ScholarPubMed
28. Thorburn, A, O'Sullivan, B, Thomas, R, et al. Pneumococcal conjugate vaccine-induced T regulatory cells suppress the development of allergic airways disease. Thorax. 2010; 65, 1053–1060.CrossRefGoogle ScholarPubMed
29. Thorburn, A, Foster, P, Gibson, P, Hansbro, P. Components of Streptococcus pneumoniae suppress allergic airways disease and natural killer T cells by inducing regulatory T cells. J Immunol. 2012; in press.CrossRefGoogle ScholarPubMed
30. Hilty, M, Burke, C, Pedro, H, et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010; 5, e 8578.CrossRefGoogle ScholarPubMed
31. 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. 2011; 184, 198–205.CrossRefGoogle ScholarPubMed
32. Huang, Y, Nelson, C, Brodie, E, et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol. 2011; 127, 372–381.CrossRefGoogle ScholarPubMed
33. Gnarpe, J, Gnarpe, H, Sundelöf, B. Endemic prevalence of Chlamydia pneumoniae in subjectively healthy persons. Scand J Infect Dis. 1991; 23, 387–388.CrossRefGoogle ScholarPubMed
34. Schmidt, S, Muller, C, Mahner, B, Wiersbitzky, S. Prevalence, rate of persistence and respiratory tract symptoms of Chlamydia pneumoniae infection in 1211 kindergarten and school age children. Pediatr Infect Dis J. 2002; 21, 758–762.CrossRefGoogle ScholarPubMed
35. Kuo, C, Jackson, L, Campbell, L, Grayston, J. Chlamydia pneumoniae (TWAR). Clin Microbiol Rev. 1995; 8, 451–461.CrossRefGoogle ScholarPubMed
36. Wark, P, Johnston, S, Simpson, J, Hensley, M, Gibson, P. Chlamydia pneumoniae immunoglobulin A reactivation and airway inflammation in acute asthma. Eur Respir J. 2002; 20, 834–840.CrossRefGoogle ScholarPubMed
37. Sutherland, E, Martin, R. Asthma and atypical bacterial infection. Chest. 2007; 132, 1962–1966.CrossRefGoogle ScholarPubMed
38. Webley, W, Salva, P, Andrzejewski, C, et al. The bronchial lavage of pediatric patients with asthma contains infectious Chlamydia . Am J Respir Crit Care Med. 2005; 171, 1083–1088.CrossRefGoogle ScholarPubMed
39. Normann, E, Gnarpe, J, Wettergren, B, et al. Association between Chlamydia pneumoniae antibodies and wheezing in young children and the influence of sex. Thorax. 2006; 61, 1054–1058.CrossRefGoogle ScholarPubMed
40. von Hertzen, LC. Role of persistent infection in the control and severity of asthma: focus on Chlamydia pneumoniae . Eur Respir J. 2002; 19, 546–556.CrossRefGoogle ScholarPubMed
41. Cunningham, A, Johnston, S, Julious, S, Lampe, F, Ward, M. Chronic Chlamydia pneumoniae infection and asthma exacerbations in children. Eur Respir J. 1998; 11, 345–349.CrossRefGoogle ScholarPubMed
42. Emre, U, Roblin, P, Gelling, M, et al. The association of Chlamydia pneumoniae infection and reactive airway disease in children. Arch Pediatr Adolesc Med. 1994; 148, 727–732.CrossRefGoogle ScholarPubMed
43. Esposito, S, Blasi, F, Arosio, C, et al. Importance of acute Mycoplasma pneumoniae and Chlamydia pneumoniae infections in children with wheezing. Eur Respir J. 2000; 16, 1142–1146.CrossRefGoogle ScholarPubMed
44. Freymuth, F, Vabret, A, Brouard, J, et al. Detection of viral, Chlamydia pneumoniae and Mycoplasma pneumoniae infections in exacerbations of asthma in children. J Clin Virol. 1999; 13, 131–139.CrossRefGoogle ScholarPubMed
45. Zaitsu, M. The development of asthma in wheezing infants with Chlamydia pneumoniae infection. J Asthma. 2007; 44, 565–568.CrossRefGoogle ScholarPubMed
46. Wang, F, He, X, Baines, K, et al. Different inflammatory phenotypes in adults and children with acute asthma. Eur Respir J. 2011; 38, 567–574.CrossRefGoogle ScholarPubMed
47. Webley, W, Hahn, D. Respiratory Chlamydophyla pneumoniae resides primarily in the lower airway. Eur Respir J. 2011; 38, 994–995.CrossRefGoogle ScholarPubMed
48. Holt, P, Sly, P. Prevention of allergic respiratory disease in infants: current aspects and future perspectives. Curr Opin Allergy Clin Immunol. 2007; 7, 547–555.CrossRefGoogle ScholarPubMed
49. Brunetti, L, Colazzo, D, Francavilla, R, et al. The role of pulmonary infection in pediatric asthma. Allergy Asthma Proc. 2007; 28, 190–193.CrossRefGoogle ScholarPubMed
50. Krüll, M, Bockstaller, P, Wuppermann, F, et al. Mechanisms of Chlamydophila pneumoniae-mediated GM-CSF release in human bronchial epithelial cells. Am J Respir Cell Mol Biol. 2006; 34, 375–382.CrossRefGoogle ScholarPubMed
51. Asquith, K, Horvat, J, Kaiko, G, et al. Interleukin-13 promotes susceptibility to chlamydial infection of the respiratory and genital tracts. PLoS Pathog. 2011; 7, e1001339.CrossRefGoogle ScholarPubMed
52. Jahn, H, Krüll, M, Wuppermann, F, et al. Infection and activation of airway epithelial cells by Chlamydia pneumoniae . J Infect Dis. 2000; 182, 1678–1687.CrossRefGoogle ScholarPubMed
53. Prochnau, D, Rödel, J, Hartmann, M, Straube, E, Figulla, H. Growth factor production in human endothelial cells after Chlamydia pneumoniae infection. Int J Med Microbiol. 2004; 294, 53–57.CrossRefGoogle ScholarPubMed
54. Molestina, RE, Miller, RD, Ramirez, JA, Summersgill, JT. Infection of human endothelial cells with Chlamydia pneumoniae stimulates transendothelial migration of neutrophils and monocytes. Infect Immun. 1999; 67, 1323–1330.CrossRefGoogle ScholarPubMed
55. Coombes, B, Mahony, J. Chlamydia pneumoniae infection of human endothelial cells induces proliferation of smooth muscle cells via an endothelial cell-derived soluble factor(s). Infect Immun. 1999; 67, 2909–2915.CrossRefGoogle ScholarPubMed
56. Rodel, J, Woytas, M, Groh, A, et al. Production of basic fibroblast growth factor and interleukin 6 by human smooth muscle cells following infection with Chlamydia pneumoniae . Infect Immun. 2000; 68, 3635–3641.CrossRefGoogle ScholarPubMed
57. Doganci, A, Sauer, K, Karwot, R, Finotto, S. Pathological role of IL-6 in the experimental allergic bronchial asthma in mice. Clin Rev Allergy Immunol. 2005; 28, 257–270.CrossRefGoogle ScholarPubMed
58. Wills-Karp, M, Santeliz, J, Karp, CL. The gremless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol. 2001; 1, 69–75.CrossRefGoogle ScholarPubMed
59. Jupelli, M, Murthy, A, Chaganty, B, et al. Neonatal chlamydial pneumonia induces altered respiratory structure and function lasting into adult life. Lab Invest. 2011; 91, 1530–1539.CrossRefGoogle ScholarPubMed
60. Beagley, K, Huston, W, Hansbro, P, Timms, P. Chlamydial infection of immune cells: altered function and implications for disease. Crit Rev Immunol. 2009; 29, 275–305.CrossRefGoogle ScholarPubMed
61. Jupelli, M, Guentzel, M, Meier, P, et al. Endogenous IFN-{gamma} production is induced and required for protective immunity against pulmonary chlamydial infection in neonatal mice. J Immunol. 2008; 180, 4148–4155.CrossRefGoogle ScholarPubMed
62. Jupelli, M, Selby, D, Guentzel, M, et al. The contribution of interleukin-12/interferon-gamma axis in protection against neonatal pulmonary Chlamydia muridarum challenge. J Interferon Cytokine Res. 2010; 30, 407–415.CrossRefGoogle ScholarPubMed
63. Horvat, J, Starkey, M, Kim, R, et al. Chlamydial respiratory infection during allergen sensitization drives neutrophilic allergic airways disease. J Immunol. 2010; 184, 4159–4169.CrossRefGoogle ScholarPubMed
64. Essilfie, A, Simpson, J, Horvat, J, et al. Haemophilus influenzae infection drives IL-17-mediated neutrophilic allergic airways disease. PLoS Pathog. 2011; 7, e1002244.CrossRefGoogle ScholarPubMed
65. Essilfie, A, Simpson, J, Dunkley, M, et al. Combined Haemophilus influenzae respiratory infection and allergic airways disease drives chronic infection and features of steroid-resistant neutrophilic asthma. Thorax. 2012; in press.CrossRefGoogle ScholarPubMed
66. Siegle, J, Hansbro, N, Herbert, C, et al. Early-life viral infection and allergen exposure interact to induce an asthmatic phenotype in mice. Respir Res. 2010; 11, 14–29.CrossRefGoogle ScholarPubMed
67. Forsythe, P. Probiotics and lung diseases. Chest. 2011; 139, 901–908.CrossRefGoogle ScholarPubMed
68. Yao, T, Chang, C, Hsu, Y, Huang, J. Probiotics for allergic diseases: realities and myths. Pediatr Allergy Immunol. 2010; 21, 900–919.CrossRefGoogle ScholarPubMed
69. Bass, D. Behaviour of eosinophil leukocytes in acute inflammation. Lack of dependence on adrenal function. J Clin Invest. 1975; 55, 1229–1236.CrossRefGoogle ScholarPubMed
70. Schuller, D. Prophylaxis of otitis media in asthmatic children. Pediatr Infect Dis. 1983; 2, 280–283.CrossRefGoogle ScholarPubMed
71. Ansaldi, F, Turello, V, Lai, P, et al. Effectiveness of a 23-valent polysaccharide vaccine in preventing pneumonia and non-invasive pneumococcal infection in elderly people: a large-scale retrospective cohort study. J Int Med Res. 2005; 33, 490–500.CrossRefGoogle ScholarPubMed
72. Rose, M, Schubert, R, Kujumdshiev, S, Kitz, R, Zielen, S. Immunoglobulins and immunogenicity of pneumococcal vaccination in preschool asthma. Int J Clin Pract. 2006; 60, 1425–1431.CrossRefGoogle ScholarPubMed
73. Lee, H, Kang, J, Henrichsen, J, et al. Immunogenicity and safety of a 23-valent pneumococcal polysaccharide vaccine in healthy children and in children at increased risk of pneumococcal infection. Vaccine. 1995; 13, 1533–1538.CrossRefGoogle ScholarPubMed
74. Kadioglu, A, Coward, W, Colston, M, Hewitt, C, Andrew, P. CD4-T-lymphocyte interactions with pneumolysin and pneumococci suggest a crucial protective role in the host response to pneumococcal infection. Infect Immun. 2004; 72, 2689–2697.CrossRefGoogle ScholarPubMed
75. Szefler, S. Advances in pediatric asthma in 2010: addressing the major issues. J Allergy Clin Immunol. 2011; 127, 102–115.CrossRefGoogle ScholarPubMed