Intestinal helminths protect in a murine model of asthma

Journal of Immunology

Volumn 177, Issue 3, 2006, Pages 1628-1635

  Kitagaki, Kunihiko ^a   Businga, Thomas R ^a   Racila, Doina ^a   Elliott, David E ^a   Weinstock, Joel V ^a,b   Kline, Joel N ^a,c  

^a UNIVERSITY OF IOWA   (United States)

^b TUFTS MEDICAL CENTER   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CD4 ANTIGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 5; OVALBUMIN; TRANSCRIPTION FACTOR FOXP3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; EXPOSURE; FEMALE; FLOW CYTOMETRY; HELIGOSOMOIDES POLYGYRUS; HELMINTH; HELMINTHIASIS; HYGIENE; INTESTINE PARASITE; LYMPH NODE; MOUSE; NEMATODE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; TH1 CELL; TH2 CELL;

EID: 33746214821     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.3.1628     Document Type: Article

References (50)

1. Kay, A. B. 1996. TH2-type cytokines in asthma. Ann. NY Acad. Sci. 796: 1-8.
2. Beasley, R., J. Crane, C. K. Lai, and N. Pearce. 2000. Prevalence and etiology of asthma. J. Allergy Clin. Immunol. 105: S466-S472.
3. Yemaneberhan, H., Z. Bekele, A. Venn, S. Lewis, E. Parry, and J. Britton. 1997. Prevalence of wheeze and asthma and relation to atopy in urban and rural Ethiopia. Lancet 350: 85-90.
4. Von Ehrenstein, O. S., E. Von Mutius, S. Illi, L. Baumann, O. Bohm, and R. von Kries. 2000. Reduced risk of hay fever and asthma among children of farmers. Clin. Exp. Allergy 30: 187-193.
5. Wills-Karp, M., J. Santeliz, and C. L. Karp. 2001. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat. Rev. Immunol. 1: 69-75.
6. Strachan, D. P. 1989. Hay fever, hygiene, and household size. Br. Med. J. 299: 1259-1260.
7. Ball, T. M., J. A. Castro-Rodriguez, K. A. Griffith, C. J. Holberg, F. D. Martinez, and A. L. Wright. 2000. Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N. Engl. J. Med. 343: 538-543.
8. Pelosi, U., G. Porcedda, F. Tiddia, S. Tripodi, A. E. Tozzi, V. Panetta, C. Pintor, and P. M. Matricardi. 2005. The inverse association of salmonellosis in infancy with allergic rhinoconjunctivitis and asthma at school-age: a longitudinal study. Allergy 60: 626-630.
9. Mosmann, T. R., H. Cherwinski, M. W. Bond, M. A. Giedlin, and R. L. Coffman. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136: 2348-2357.
10. Stene, L. C., and P. Nafstad. 2001. Relation between occurrence of type 1 diabetes and asthma. Lancet 357: 607-608.
11. Elliott, D. E., J. J. Urban, C. K. Argo, and J. V. Weinstock. 2000. Does the failure to acquire helminthic parasites predispose to Crohn's disease? FASEB J. 14: 1848-1855.
12. Edwards, L. J., and C. S. Constantinescu. 2004. A prospective study of conditions associated with multiple sclerosis in a cohort of 658 consecutive outpatients attending a multiple sclerosis clinic. Mult. Scler. 10: 575-581.
13. Yazdanbakhsh, M., P. G. Kremsner, and R. van Ree. 2002. Allergy, parasites, and the hygiene hypothesis. Science 296: 490-494.
14. Araujo, M. I., A. A. Lopes, M. Medeiros, A. A. Cruz, L. Sousa-Atta, D. Sole, and E. M. Carvalho. 2000. Inverse association between skin response to aeroallergens and Schistonoma mansoni infection. Int. Arch. Allergy Immunol. 123: 145-148.
15. Van den Biggelaar, A. H., R. van Ree, L. C. Rodrigues, B. Lell, A. M. Deelder, P. G. Kremsner, and M. Yazdanbakhsh. 2000. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356: 1723-1727.
16. Nyan, O. A., G. E. Walraven, W. A. Banya, P. Milligan, M. Van Der Sande, S. M. Ceesay, G. Del Prete, and K. P. McAdam. 2001. Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities. Clin. Exp. Allergy 31: 1672-1678.
17. Masters, S., and E. Barrett-Connor. 1985. Parasites and asthma: predictive or protective? Epidemiol. Rev. 7: 49-58.
18. Yazdanbakhsh, M., A. van den Biggelaar, and R. M. Maizels. 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22: 372-377.
19. Fox, J. G., P. Beck, C. A. Dangler, M. T. Whary, T. C. Wang, H. N. Shi, and C. Nagler-Anderson. 2000. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat. Med. 6: 536-542.
20. Wohlleben, G., C. Trujillo, J. Muller, Y. Ritze, S. Grunewald, U. Tatsch, and K. J. Erb. 2004. Helminth infection modulates the development of allergen-induced airway inflammation. Int. Immunol. 16: 585-596.
21. Elliott, D. E., T. Setiawan, A. Metwali, A. Blum, J. F. Urban, Jr., and J. V. Weinstock. 2004. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur. J. Immunol. 34: 2690-2698.
22. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15: 505-533.
23. Robinson, M., F. Wahid, J. M. Behnke, and F. S. Gilbert. 1989. Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98: 115-124.
24. + TH1-like responses. J. Clin. Invest. 98: 1010-1020.
25. Schuessler, T. F., and J. H. Bates. 1995. A computer-controlled research ventilator for small animals: design and evaluation. IEEE Trans. Biomed. Eng. 42: 860-866.
26. Bates, J. H., B. Daroczy, and Z. Hantos. 1992. A comparison of interrupter and forced oscillation measurements of respiratory resistance in the dog. J. Appl. Physiol. 72: 46-52.
27. Tomioka, S., J. H. Bates, and C. G. Irvin. 2002. Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations. J. Appl. Physiol. 93: 263-270.
28. Erb, K. J., J. W. Holloway, A. Sobeck, H. Moll, and G. Le Gros. 1998. Infection of mice with Mycobacterium bovis-Bacillus Calmette-Guerin (BCG) suppresses allergen-induced airway eosinophilia. J. Exp. Med. 187: 561-569.
29. Herz, U., K. Gerhold, C. Gruber, A. Braun, U. Wahn, H. Renz, and K. Paul. 1998. BCG infection suppresses allergic sensitization and development of increased airway reactivity in an animal model. J. Allergy Clin. Immunol. 102: 867-874.
30. Wilson, M. S., M. D. Taylor, A. Balic, C. A. Finney, J. R. Lamb, and R. M. Maizels. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202: 1199-1212.
31. Makela, M. J., A. Kanehiro, L. Borish, A. Dakhama, J. Loader, A. Joetham, Z. Xing, M. Jordana, G. L. Larsen, and E. W. Gelfand. 2000. IL-10 is necessary for the expression of airway hyperresponsiveness but not pulmonary inflammation after allergic sensitization. Proc. Natl. Acad. Sci. USA 97: 6007-6012.
32. Yang, X., S. Wang, Y. Fan, and X. Han. 2000. IL-10 deficiency prevents IL-5 overproduction and eosinophilic inflammation in a murine model of asthma-like reaction. Eur. J. Immunol. 30: 382-391.
33. Tournoy, K. G., J. C. Kips, and R. A. Pauwels. 2000. Endogenous interleukin-10 suppresses allergen-induced airway inflammation and nonspecific airway responsiveness. Clin. Exp. Allergy 30: 775-783.
34. Grunig, G., D. B. Corry, M. W. Leach, B. W. Seymour, V. P. Kurup, and D. M. Rennick. 1997. Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J. Exp. Med. 185: 1089-1099.
35. Justice, J. P., Y. Shibata, S. Sur, J. Mustafa, M. Fan, and M. R. Van Scott. 2001. IL-10 gene knockout attenuates allergen-induced airway hyperresponsiveness in C57BL/6 mice. Am. J. Physiol. 280: L363-L368.
36. Fiorentino, D. F., A. Zlotnik, P. Vieira, T. R. Mosmann, M. Howard, K. W. Moore, and A. O'Garra. 1991. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146: 3444-3451.
37. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147: 3815-3822.
38. Kitagaki, K., V. V. Jain, T. R. Businga, I. Hussain, and J. N. Kline. 2002. Immunomodulatory effects of CpG oligodeoxynucleotides on established Th2 responses. Clin. Diagn. Lab. Immunol. 9: 1260-1269.
39. Makela, M. J., A. Kanehiro, A. Dakhama, L. Borish, A. Joetham, R. Tripp, L. Anderson, and E. W. Gelfand. 2002. The failure of interleukin-10-deficient mice to develop airway hyperresponsiveness is overcome by respiratory syncytial virus infection in allergen-sensitized/challenged mice. Am. J. Respir. Crit. Care Med. 165: 824-831.
40. Ameredes, B. T., R. Zamora, J. M. Sethi, H. L. Liu, L. K. Kohut, A. L. Gligonic, A. M. Choi, and W. J. Calhoun. 2005. Alterations in nitric oxide and cytokine production with airway inflammation in the absence of IL-10. J. Immunol. 175: 1206-1213.
41. Wilson, M. S., and R. M. Maizels. 2006. Regulatory T cells induced by parasites and the modulation of allergic responses. Chem. Immunol. Allergy 90: 176-195.
42. Shi, H. N., C. J. Ingui, I. Dodge, and C. Nagler-Anderson. 1998. A helminth-induced mucosal Th2 response alters nonresponsiveness to oral administration of a soluble antigen. J. Immunol. 160: 2449-2455.
43. Scrivener, S., H. Yemaneberhan, M. Zebenigus, D. Tilahun, S. Girma, S. Ali, P. McElroy, A. Custovic, A. Woodcock, D. Pritchard, et al. 2001. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet 358: 1493-1499.
44. Godfrey, R. C. 1975. Asthma and IgE levels in rural and urban communities of The Gambia. Clin. Allergy 5: 201-207.
45. Merrett, T. G., J. Merrett, and J. B. Cookson. 1976. Allergy and parasites: the measurement of total and specific IgE levels in urban and rural communities in Rhodesia. Clin. Allergy 6: 131-134.
46. Kline, J. N., A. M. Krieg, T. J. Waldschmidt, Z. K. Ballas, V. Jain, and T. R. Businga. 1999. CpG oligodeoxynucleotides do not require TH1 cytokines to prevent eosinophilic airway inflammation in a murine model of asthma. J. Allergy Clin. Immunol. 104: 1258-1264.
47. Zuany-Amorim, C., E. Sawicka, C. Manlius, A. Le Moine, L. R. Brunei, D. M. Kemeny, G. Bowen, G. Rook, and C. Walker. 2002. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat. Med. 8: 625-629.
48. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
49. McGuirk, P., and K. H. Mills. 2002. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 23: 450-455.
50. MacDonald, A. J., M. Duffy, M. T. Brady, S. McKiernan, W. Hall, J. Hegarty, M. Curry, and K. H. Mills. 2002. CD4 T helper type 1 and regulatory T cells induced against the same epitopes on the core protein in hepatitis C virus-infected persons. J. Infect. Dis. 185: 720-727.