Interleukin-10 Inhibits Antigen-induced Cellular Recruitment into the Airways of Sensitized Mice

Overview

Journal J Clin Invest

Specialty General Medicine

Date 1995 Jun 1

PMID 7769104

Citations 47

Authors

S Haile

D Leduc

C Dumarey

M Huerre

B B Vargaftig

M Pretolani

Affiliations

Soon will be listed here.

Abstract

This report examines the effect of recombinant murine (rm) IL-10 on antigen-induced cellular recruitment into the airways of sensitized Balb/c mice. The intranasal instillation of 10 micrograms ovalbumin induced an early (6-24 h) increase in the number of neutrophils, and a late rise (24-96 h) in that of eosinophils in the bronchoalveolar lavage (BAL) fluid and bronchial tissue. A single intranasal instillation of 0.01-0.1 microgram of rmIL-10, administered concurrently with ovalbumin, but not 1 or 3 h thereafter, dose-dependently inhibited both airway neutrophilia and eosinophilia. This phenomenon was suppressed by treating the sensitized mice with 1 mg/mouse of a neutralizing anti-IL-10 mAb, which increased significantly ovalbumin-induced neutrophil and eosinophil accumulation in the BAL fluid. These results suggest that antigen stimulation may trigger the in vivo generation of IL-10, which, in turn, participates in the leukocyte infiltration into the airways. rmIL-10 also reduced TNF-alpha release in the BAL fluid observed 1 and 3 h after antigen challenge. Furthermore, the intranasal instillation of an anti-TNF-alpha antiserum to sensitized mice markedly reduced ovalbumin-induced neutrophil and eosinophil accumulation in the BAL fluid. These findings indicate that leukocyte infiltration into the airways of antigen-challenged mice is regulated by IL-10. Furthermore, inhibition of TNF-alpha production by rmIL-10 suggests that allergic airway inflammation and TNF-alpha formation are parallel events in this model.

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References

Fiorentino D, Bond M, Mosmann T . Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med. 1989; 170(6):2081-95. PMC: 2189521. DOI: 10.1084/jem.170.6.2081. View

Kasama T, Strieter R, Lukacs N, Burdick M, Kunkel S . Regulation of neutrophil-derived chemokine expression by IL-10. J Immunol. 1994; 152(7):3559-69. View

Thornhill M, Haskard D . IL-4 regulates endothelial cell activation by IL-1, tumor necrosis factor, or IFN-gamma. J Immunol. 1990; 145(3):865-72. View

Gordon J, Galli S . Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature. 1990; 346(6281):274-6. DOI: 10.1038/346274a0. View

Ohno I, Ohkawara Y, Yamauchi K, Tanno Y, Takishima T . Production of tumor necrosis factor with IgE receptor triggering from sensitized lung tissue. Am J Respir Cell Mol Biol. 1990; 3(4):285-9. DOI: 10.1165/ajrcmb/3.4.285. View

Wershil B, Wang Z, Gordon J, Galli S . Recruitment of neutrophils during IgE-dependent cutaneous late phase reactions in the mouse is mast cell-dependent. Partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. J Clin Invest. 1991; 87(2):446-53. PMC: 295096. DOI: 10.1172/JCI115016. View

Kay A, Ying S, Varney V, Gaga M, Durham S, Moqbel R . Messenger RNA expression of the cytokine gene cluster, interleukin 3 (IL-3), IL-4, IL-5, and granulocyte/macrophage colony-stimulating factor, in allergen-induced late-phase cutaneous reactions in atopic subjects. J Exp Med. 1991; 173(3):775-8. PMC: 2118805. DOI: 10.1084/jem.173.3.775. View

Mattoli S, Mattoso V, Soloperto M, Allegra L, FASOLI A . Cellular and biochemical characteristics of bronchoalveolar lavage fluid in symptomatic nonallergic asthma. J Allergy Clin Immunol. 1991; 87(4):794-802. DOI: 10.1016/0091-6749(91)90125-8. View

Hamid Q, Azzawi M, Ying S, Moqbel R, Wardlaw A, Corrigan C . Expression of mRNA for interleukin-5 in mucosal bronchial biopsies from asthma. J Clin Invest. 1991; 87(5):1541-6. PMC: 295235. DOI: 10.1172/JCI115166. View

10.

Gosset P, Tsicopoulos A, Wallaert B, Vannimenus C, Joseph M, Tonnel A . Increased secretion of tumor necrosis factor alpha and interleukin-6 by alveolar macrophages consecutive to the development of the late asthmatic reaction. J Allergy Clin Immunol. 1991; 88(4):561-71. DOI: 10.1016/0091-6749(91)90149-i. View

11.

Svetic A, Finkelman F, Jian Y, Dieffenbach C, Scott D, McCarthy K . Cytokine gene expression after in vivo primary immunization with goat antibody to mouse IgD antibody. J Immunol. 1991; 147(7):2391-7. View

12.

Fiorentino D, Zlotnik A, Mosmann T, Howard M, OGarra A . IL-10 inhibits cytokine production by activated macrophages. J Immunol. 1991; 147(11):3815-22. View

13.

Bogdan C, Vodovotz Y, Nathan C . Macrophage deactivation by interleukin 10. J Exp Med. 1991; 174(6):1549-55. PMC: 2119047. DOI: 10.1084/jem.174.6.1549. View

14.

Robinson D, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley A . Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992; 326(5):298-304. DOI: 10.1056/NEJM199201303260504. View

15.

Sanderson C . Interleukin-5, eosinophils, and disease. Blood. 1992; 79(12):3101-9. View

16.

Hsu D, Moore K, Spits H . Differential effects of IL-4 and IL-10 on IL-2-induced IFN-gamma synthesis and lymphokine-activated killer activity. Int Immunol. 1992; 4(5):563-9. DOI: 10.1093/intimm/4.5.563. View

17.

Nakajima H, Sano H, Nishimura T, Yoshida S, Iwamoto I . Role of vascular cell adhesion molecule 1/very late activation antigen 4 and intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 interactions in antigen-induced eosinophil and T cell recruitment into the tissue. J Exp Med. 1994; 179(4):1145-54. PMC: 2191449. DOI: 10.1084/jem.179.4.1145. View

18.

Lukacs N, Strieter R, Chensue S, Kunkel S . Interleukin-4-dependent pulmonary eosinophil infiltration in a murine model of asthma. Am J Respir Cell Mol Biol. 1994; 10(5):526-32. DOI: 10.1165/ajrcmb.10.5.8179915. View

19.

Takanaski S, Nonaka R, Xing Z, OByrne P, Dolovich J, Jordana M . Interleukin 10 inhibits lipopolysaccharide-induced survival and cytokine production by human peripheral blood eosinophils. J Exp Med. 1994; 180(2):711-5. PMC: 2191606. DOI: 10.1084/jem.180.2.711. View

20.

Vargaftig B, Maclouf J, Pretolani M . Strain-dependency of leukotriene C4 generation from isolated lungs of immunized mice. Br J Pharmacol. 1994; 112(4):1230-6. PMC: 1910240. DOI: 10.1111/j.1476-5381.1994.tb13215.x. View