Prenatal initiation of endotoxin airway exposure prevents subsequent allergen-induced sensitization and airway inflammation in mice

Journal of Allergy and Clinical Immunology

Volumn 118, Issue 3, 2006, Pages 666-673

  Gerhold, Kerstin ^a   Avagyan, Angela ^a   Seib, Christine ^a   Frei, Remo ^b   Steinle, Johanna ^b   Ahrens, Birgit ^a   Dittrich, Anna Maria ^a   Blumchen, Katharina ^a   Lauener, Roger ^b   Hamelmann, Eckard ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

Asthma; cytokines; lipopolysaccharides; mice; ovalbumin

Indexed keywords

ALLERGEN; BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; IMMUNOGLOBULIN E; OVALBUMIN; PLACEBO; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHITIS; BRONCHUS REACTIVITY; CELLULAR IMMUNITY; CONTROLLED STUDY; EOSINOPHIL; FEMALE; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; IMMUNOMODULATION; INFLAMMATION; LUNG LAVAGE; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIZATION; SPLEEN CELL; TH1 CELL;

AEROSOLS; ALLERGENS; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOTOXINS; FEMALE; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RESPIRATORY HYPERSENSITIVITY; TH1 CELLS; TH2 CELLS;

EID: 33748070482     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2006.05.022     Document Type: Article

References (40)

1. Isolauri E., Huurre A., Salminen S., and Impivaara O. The allergy epidemic extends beyond the past few decades. Clin Exp Allergy 34 (2004) 1007-1010
2. Lau S., Nickel R., Niggemann B., Gruber C., Sommerfeld C., Illi S., et al. The development of childhood asthma: lessons from the German Multicentre Allergy Study (MAS). Paediatr Respir Rev 3 (2002) 265-272
3. von Mutius E. The environmental predictors of allergic disease. J Allergy Clin Immunol 105 (2000) 9-19
4. Braun-Fahrlander C., Gassner M., Grize L., Neu U., Sennhauser F.H., Varonier H.S., et al. Prevalence of hay fever and allergic sensitization in farmer's children and their peers living in the same rural community. SCARPOL team. Swiss Study on Childhood Allergy and Respiratory Symptoms with Respect to Air Pollution. Clin Exp Allergy 29 (1999) 28-34
5. Rodriguez D., Keller A.C., Faquim-Mauro E.L., de Macedo M.S., Cunha F.Q., Lefort J., et al. Bacterial lipopolysaccharide signaling through Toll-like receptor 4 suppresses asthma-like responses via nitric oxide synthase 2 activity. J Immunol 171 (2003) 1001-1008
6. von Mutius E., Braun-Fahrlander C., Schierl R., Riedler J., Ehlermann S., Maisch S., et al. Exposure to endotoxin or other bacterial components might protect against the development of atopy. Clin Exp Allergy 30 (2000) 1230-1234
7. Braun-Fahrlander C., Riedler J., Herz U., Eder W., Waser M., Grize L., et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 347 (2002) 869-877
8. Palsson-McDermott E.M., and O'Neill L.A.J. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113 (2004) 153-162
9. Tulic M.K., Knight D.A., Holt P.G., and Sly P.D. Lipopolysaccharide inhibits the late-phase response to allergen by altering nitric oxide synthase activity and interleukin-10. Am J Respir Cell Mol Biol 24 (2001) 640-646
10. Gerhold K., Blumchen K., Bock A., Seib C., Stock P., Kallinich T., et al. Endotoxins prevent murine IgE production, T(H)2 immune responses, and development of airway eosinophilia but not airway hyperreactivity. J Allergy Clin Immunol 110 (2002) 110-116
11. Gerhold K., Bluemchen K., Franke A., Stock P., and Hamelmann E. Exposure to endotoxin and allergen in early life and its effect on allergen sensitization in mice. J Allergy Clin Immunol 112 (2003) 389-396
12. Hamelmann E., Oshiba A., Loader J., Larsen G.L., Gleich G., Lee J., et al. Antiinterleukin-5 antibody prevents airway hyperresponsiveness in a murine model of airway sensitization. Am J Respir Crit Care Med 155 (1997) 819-825
13. Hamelmann E., Schwarze J., Takeda K., Oshiba A., Larsen G.L., Irvin C.G., et al. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am J Respir Crit Care Med 156 (1997) 766-775
14. Gerberick G.F., Curse L.W., Miller C.M., Sikorski E.E., and Ridder G.M. Selective modulation of T cell memory markers CD62L and CD44 on murine draining lymph node cells following allergen and irritant treatment. Toxicol Appl Pharmacol 146 (1997) 1-10
15. + regulatory T cells. Nat Immunol 4 (2003) 330-336
16. Agnello D., Lankford C.S., Bream J., Morinobu A., Gadina M., O'Shea J.J., et al. Cytokines and transcription factors that regulate T helper cell differentiation: new players and new insights. J Clin Immunol 23 (2003) 147-161
17. Tulic M., Wale J.L., Holt P.G., and Sly P.D. Modification of the inflammatory response to allergen challenge after exposure to bacterial lipopolysaccharide. Am J Respir Cell Mol Biol 22 (2000) 604-612
18. Lapa e Silva J.R., Possebon da Silva M.D., Lefort J., and Vargaftig B.B. Endotoxins, asthma, and allergic immune responses. Toxicology 152 (2000) 31-35
19. McGuirk P., McCann C., and Mills K.H.G. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J Exp Med 195 (2002) 221-231
20. Unger W.W.J., Jansen W., Wolvers D.A.W., van Halteren A.G.S., Kraal G., and Samsom J.N. Nasal tolerance induces antigen-specific CD4+CD25- regulatory T-cells that can transfer their regulatory capacity to naive CD4+ T-cells. Int Immunol 15 (2003) 731-739
21. Stock P., Akbari O., Berry G., Freeman G.J., DeKruyff R.H., and Umetsu D.T. Induction of T helper type 1 like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat Immunol 5 (2004) 1149-1156
22. Stassen M., Fondel S., Bopp T., Richter C., Muller C., Kubach J., et al. Human CD25+ regulatory T-cells: two subsets defined by the integrins alpha 4 beta 7 or alpha 4 beta 1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 34 (2004) 1303-1311
23. Gentile D.A., Schreiber R., Howe-Adams J., Trecki J., Patel A., Angelini B., et al. Diminished dendritic cell interleukin 10 production in atopic children. Ann Allergy Asthma Immunol 92 (2004) 538-544
24. Gao J.X., Madrenas J., Zeng W., Cameron M.J., Zhang Z., Wang J.J., et al. CD40-deficient dendritic cells producing interleukin-10, but not interleukin-12, induce T-cell hyporesponsiveness in vitro and prevent acute allograft rejection. Immunology 98 (1999) 159-170
25. Erb K.J., Holloway J.W., Sobeck A., Moll H., and Le Gros G. Infection of mice with Mycobacterium bovis-Bacillus Calmette-Guerin (BCG) suppresses allergen-induced airway eosinophilia. J Exp Med 187 (1998) 561-569
26. Serebrisky D., Teper A.A., Huang C.K., Lee S.Y., Zhang T.F., Schofield B.H., et al. CpG oligodeoxynucleotides can reverse Th2-associated allergic airway responses and alter the B7.1/B7.2 expression in a murine model of asthma. J Immunol 165 (2000) 5906-5912
27. Smeltz R.B., Chen J., Hu-Li J., and Shevach E.M. Regulation of interleukin (IL)-18 receptor α chain expression on CD4+ T-cells during T helper (Th)1/Th2 differentiation: critical downregulatory role of IL-4. J Exp Med 194 (2001) 143-154
28. Blumer N., Herz U., Wegmann M., and Renz H. Prenatal lipopolysaccharide-exposure prevents allergic sensitization and airway inflammation, but not airway responsiveness in a murine model of experimental asthma. Clin Exp Allergy 35 (2005) 397-402
29. Kennedy J.D., Hatfield C.A., Fidler S.F., Winterrowd G.F., Haas J.V., Chin J.E., et al. Phenotypic characterization of T lymphocytes emigrating into lung tissue and the airway lumen after antigen inhalation in sensitized mice. Am J Respir Cell Mol Biol 12 (1995) 613-623
30. Savage N.D., Harris S.H., Rossi A.G., De Silva B., Howie S.E., Layton G.T., et al. Inhibition of TCR-mediated shedding of L-selectin (CD62L) on human and mouse CD4+ T-cells by metalloproteinase inhibition: analysis of the regulation of Th1/Th2 function. Eur J Immunol 32 (2002) 2905-2914
31. Chaouat G., Ledee-Bataille N., Dubanchet S., Zourbas S., Sandra O., and Martal J. TH1/TH2 paradigm in pregnancy: paradigm lost? Cytokines in pregnancy/early abortion: reexamining the TH1/TH2 paradigm. Int Arch Allergy Immunol 134 (2004) 93-119
32. Adkins B., and Du R.Q. Newborn mice develop balanced Th1/Th2 primary effector responses in vivo but are biased to Th2 secondary responses. J Immunol 160 (1998) 4217-4224
33. Adkins B., Bu Y., and Guevara P. The generation of Th memory in neonates versus adults: prolonged primary Th2 effector function and impaired development of Th1 memory effector function in murine neonates. J Immunol 166 (2001) 918-925
34. Zuany-Amorim C., Sawicka E., Manlius C., Le Moine A., Brunet L.R., Kemeny D.M., et al. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat Med 8 (2002) 625-629
35. Takeuchi O., and Akira S. Toll-like receptors their physiological role and signal transduction system. Int Immunopharmacol 1 (2001) 625-635
36. Harju K., Glumoff V., and Hallman M. Ontogeny of Toll-like receptors Tlr2 and Tlr4 in mice. Pediatr Res 49 (2001) 81-83
37. Gayle D.A., Beloosesky R., Desai M., Amidi F., Nunez S.E., and Ross M.G. Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain. Am J Physiol Regul Integr Comp Physiol 286 (2004) R1024-R1029
38. Knapp S., Florquin S., Golenbock D.T., and van der Poll T. Pulmonary Lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation in vivo. J Immunol 176 (2006) 3189-3195
39. Lauener R.P., Birchler T., Adamski J., Braun-Fahrlander C., Bufe A., Herz U., et al. Expression of CD14 and Toll-like receptor 2 in farmers' and non-farmers' children. Lancet 360 (2002) 465-466
40. Alexis N.E., Lay J.C., Almond M., Bromberg P.A., Patel D.D., and Beden D.B. Acute LPS inhalation in healthy volunteers induces dendritic cell maturation in vivo. J Allergy Clin Immunol 115 (2005) 345-350