Top

Inflammation Research

Published in:

01-05-2010 | Original Research Paper

Asthma during pregnancy alters immune cell profile and airway epithelial chemokine release

Authors: Annette Osei-Kumah, Peter A. B. Wark, Roger Smith, Vicki L. Clifton

Published in: Inflammation Research | Issue 5/2010

Abstract

Objective

Pregnancy can influence the course of maternal asthma, but the mechanisms are presently unknown. The aim of the present study was to access maternal immune cell profiles in the presence and absence of asthma and to determine the effect of pregnancy-derived factors on epithelial cell function.

Methods

Cells from the human bronchial epithelial cell line BEAS-2B were treated with plasma from pregnant or nonpregnant asthmatic and nonasthmatic subjects. Cell culture supernatants were collected after 24 h and assayed for IL-6, IL-8, eotaxin, RANTES and sICAM-1 protein using ELISA. Maternal immune cell count and peripheral blood chemotactic response to plasma from pregnant and non-pregnant asthmatic subjects were also assessed.

Results

The presence of maternal asthma during pregnancy was associated with increased monocyte and neutrophil numbers, increased BEAS-2B cell production of IL-8 and sICAM-1 (P < 0.05) and increased chemotactic capacity relative to pregnant women without asthma.

Conclusion

The results of this study suggest that circulating pregnancy-related factors enhance chemotactic mediators in epithelial cells in the presence of asthma. This may be one mechanism that contributes to pregnancy-induced changes in asthma.

Schatz M, Harden K, Forsythe A, Chilingar L, Hoffman C, Sperling W, et al. The course of asthma during pregnancy, post partum, and with successive pregnancies: a prospective analysis. J Allergy Clin Immunol. 1988;81:509–17.CrossRefPubMed

Jana N, Vasishta K, Saha SC, Khunnu B. Effect of bronchial asthma on the course of pregnancy, labour and perinatal outcome. J Obstet Gynaecol. 1995;21:227–32.

Murphy VE, Gibson P, Talbot PI, Clifton VL. Severe asthma exacerbations during pregnancy. Obstet Gynecol. 2005;106:1046–54.PubMed

Murphy VE, Johnson RF, Wang YC, Akinsanya K, Gibson PG, Smith R, et al. Proteomic study of plasma proteins in pregnant women with asthma. Respirology. 2006;11:41–8.CrossRefPubMed

Osei-Kumah A, Ammit AJ, Smith R, Ge Q, Clifton VL. Inflammatory mediator release in normal bronchial smooth muscle cells is altered by pregnant maternal and fetal plasma independent of asthma. Placenta. 2006;27:847–52.CrossRefPubMed

Rothenberg ME, Ownbey R, Mehlhop PD, Loiselle PM, van de Rijn M, Bonventre JV, et al. Eotaxin triggers eosinophil-selective chemotaxis and calcium flux via a distinct receptor and induces pulmonary eosinophilia in the presence of interleukin 5 in mice. Mol Med. 1996;2:334–48.PubMed

Garcia-Zepeda EA, Rothenberg ME, Ownbey RT, Celestin J, Leder P, Luster AD. Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat Med. 1996;2:449–56.CrossRefPubMed

Larche M, Robinson DS, Kay AB. The role of T lymphocytes in the pathogenesis of asthma. J Allergy Clin Immunol. 2003;111:450–63. quiz 464.CrossRefPubMed

Lazaar AL, Albelda SM, Pilewski JM, Brennan B, Pure E, Panettieri RA Jr. T lymphocytes adhere to airway smooth muscle cells via integrins and CD44 and induce smooth muscle cell DNA synthesis. J Exp Med. 1994;180:807–16.CrossRefPubMed

10.

Campbell AM, Chanez P, Vignola AM, Bousquet J, Couret I, Michel FB, et al. Functional characteristics of bronchial epithelium obtained by brushing from asthmatic and normal subjects. Am Rev Respir Dis. 1993;147:529–34.PubMed

11.

Cromwell O, Hamid Q, Corrigan CJ, Barkans J, Meng Q, Collins PD, et al. Expression and generation of interleukin-8, IL-6 and granulocyte–macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1 beta and tumour necrosis factor-alpha. Immunology. 1992;77:330–7.PubMed

12.

Kumlin M, Hamberg M, Granstrom E, Bjorck T, Dahlen B, Matsuda H, et al. 15(S)-hydroxyeicosatetraenoic acid is the major arachidonic acid metabolite in human bronchi: association with airway epithelium. Arch Biochem Biophys. 1990;282:254–62.CrossRefPubMed

13.

Nadel JA. Neurogenic inflammation in airways and its modulation by peptidases. Ann N Y Acad Sci. 1992;664:408–14.CrossRefPubMed

14.

Sousa AR, Poston RN, Lane SJ, Nakhosteen JA, Lee TH. Detection of GM-CSF in asthmatic bronchial epithelium and decrease by inhaled corticosteroids. Am Rev Respir Dis. 1993;147:1557–61.PubMed

15.

Rossi GA, Sacco O, Balbi B, Oddera S, Mattioni T, Corte G, et al. Human ciliated bronchial epithelial cells: expression of the HLA-DR antigens and of the HLA-DR alpha gene, modulation of the HLA-DR antigens by gamma-interferon and antigen-presenting function in the mixed leukocyte reaction. Am J Respir Cell Mol Biol. 1990;3:431–9.PubMed

16.

Yoon JS, Kim HH, Lee Y, Lee JS. Cytokine induction by respiratory syncytial virus and adenovirus in bronchial epithelial cells. Pediatr Pulmonol. 2007;42:277–82.CrossRefPubMed

17.

Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol. 1998;179:80–6.CrossRefPubMed

18.

Siegel I, Gleicher N. Peripheral white blood cell alterations in early labor. Diagn Gynecol Obstet. 1981;3:123–6.PubMed

19.

Valdimarsson H, Mulholland C, Fridriksdottir V, Coleman DV. A longitudinal study of leucocyte blood counts and lymphocyte responses in pregnancy: a marked early increase of monocyte-lymphocyte ratio. Clin Exp Immunol. 1983;53:437–43.PubMed

20.

Borzychowski AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol. 2005;35:3054–63.CrossRefPubMed

21.

Sacks G, Sargent I, Redman C. Innate immunity in pregnancy. Immunol Today. 2000;21:200–1.CrossRefPubMed

22.

Sacks G, Sargent I, Redman C. An innate view of human pregnancy. Immunol Today. 1999;20:114–8.CrossRefPubMed

23.

Sacks GP, Redman CW, Sargent IL. Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells. Clin Exp Immunol. 2003;131:490–7.CrossRefPubMed

24.

Mann BS, Chung KF. Blood neutrophil activation markers in severe asthma: lack of inhibition by prednisolone therapy. Respir Res. 2006;7:59.CrossRefPubMed

25.

Silvestri M, Bontempelli M, Giacomelli M, Malerba M, Rossi GA, Di Stefano A, et al. High serum levels of tumour necrosis factor-alpha and interleukin-8 in severe asthma: markers of systemic inflammation? Clin Exp Allergy. 2006;36:1373–81.CrossRefPubMed

26.

Murphy VE, Gibson PG, Giles WB, Zakar T, Smith R, Bisits AM, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003;168:1317–23.CrossRefPubMed

27.

National Institute of Health. Guidelines for the diagnosis and management of asthma. NIH publication no. 97-4051. Bethesda, MD: National Heart, Lung and Blood Institute; 1997.

28.

Murphy VE, Gibson PG, Talbot PI, Kessell CG, Clifton VL. Asthma self-management skills and the use of asthma education during pregnancy. Eur Respir J. 2005;26:435–41.CrossRefPubMed

29.

Hung CH, Li CY, Hua YM, Chen CJ, Yang KD, Jong YJ. Effects of leukotriene receptor antagonists on monocyte chemotaxis, p38 and cytoplasmic calcium. Pediatr Allergy Immunol. 2006;17:250–8.CrossRefPubMed

30.

Bayram H, Devalia JL, Khair OA, Abdelaziz MM, Sapsford RJ, Sagai M, et al. Comparison of ciliary activity and inflammatory mediator release from bronchial epithelial cells of nonatopic nonasthmatic subjects and atopic asthmatic patients and the effect of diesel exhaust particles in vitro. J Allergy Clin Immunol. 1998;102:771–82.CrossRefPubMed

31.

Bayram H, Devalia JL, Sapsford RJ, Ohtoshi T, Miyabara Y, Sagai M, et al. The effect of diesel exhaust particles on cell function and release of inflammatory mediators from human bronchial epithelial cells in vitro. Am J Respir Cell Mol Biol. 1998;18:441–8.PubMed

32.

Bayram H, Sapsford RJ, Abdelaziz MM, Khair OA. Effect of ozone and nitrogen dioxide on the release of proinflammatory mediators from bronchial epithelial cells of nonatopic nonasthmatic subjects and atopic asthmatic patients in vitro. J Allergy Clin Immunol. 2001;107:287–94.CrossRefPubMed

33.

Erzurum SC. Inhibition of tumor necrosis factor alpha for refractory asthma. N Engl J Med. 2006;354:754–8.CrossRefPubMed

34.

Kwon OJ, Au BT, Collins PD, Adcock IM, Mak JC, Robbins RR, et al. Tumor necrosis factor-induced interleukin-8 expression in cultured human airway epithelial cells. Am J Physiol. 1994;267:L398–405.PubMed

35.

Standiford TJ, Kunkel SL, Basha MA, Chensue SW, Lynch JP 3rd, Toews GB, et al. Interleukin-8 gene expression by a pulmonary epithelial cell line. A model for cytokine networks in the lung. J Clin Invest. 1990;86:1945–53.CrossRefPubMed

36.

Nakamura H, Yoshimura K, McElvaney NG, Crystal RG. Neutrophil elastase in respiratory epithelial lining fluid of individuals with cystic fibrosis induces interleukin-8 gene expression in a human bronchial epithelial cell line. J Clin Invest. 1992;89:1478–84.CrossRefPubMed

37.

Brown JR, Kleimberg J, Marini M, Sun G, Bellini A, Mattoli S. Kinetics of eotaxin expression and its relationship to eosinophil accumulation and activation in bronchial biopsies and bronchoalveolar lavage (BAL) of asthmatic patients after allergen inhalation. Clin Exp Immunol. 1998;114:137–46.CrossRefPubMed

38.

Holgate ST. Epithelial damage and response. Clin Exp Allergy. 2000;30(Suppl 1):37–41.CrossRefPubMed

39.

Holgate ST. Inflammatory and structural changes in the airways of patients with asthma. Respir Med. 2000;94(Suppl D):S3–6.PubMed

40.

Pueringer RJ, Hunninghake GW. Inflammation and airway reactivity in asthma. Am J Med. 1992;92:32S–8S.CrossRefPubMed

41.

Shiels IA, Bowler SD, Taylor SM. Airway smooth muscle proliferation in asthma: the potential of vascular leakage to contribute to pathogenesis. Med Hypotheses. 1995;45:37–40.CrossRefPubMed

42.

Sukkar MB, Hughes JM, Johnson PR, Armour CL. GM-CSF production from human airway smooth muscle cells is potentiated by human serum. Mediat Inflamm. 2000;9:161–8.CrossRef

43.

Holgate ST, Lackie PM, Davies DE, Roche WR, Walls AF. The bronchial epithelium as a key regulator of airway inflammation and remodelling in asthma. Clin Exp Allergy. 1999;29(Suppl 2):90–5.CrossRefPubMed

44.

Leonard EJ, Yoshimura T. Neutrophil attractant/activation protein-1 (NAP-1 [interleukin-8]). Am J Respir Cell Mol Biol. 1990;2:479–86.PubMed

45.

Smith WB, Gamble JR, Clark-Lewis I, Vadas MA. Interleukin-8 induces neutrophil transendothelial migration. Immunology. 1991;72:65–72.PubMed

46.

Larsen CG, Anderson AO, Appella E, Oppenheim JJ, Matsushima K. The neutrophil-activating protein (NAP-1) is also chemotactic for T lymphocytes. Science. 1989;243:1464–6.CrossRefPubMed

47.

Alam R, York J, Boyars M, Stafford S, Grant JA, Lee J, et al. Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am J Respir Crit Care Med. 1996;153:1398–404.PubMed

48.

Venge J, Lampinen M, Hakansson L, Rak S, Venge P. Identification of IL-5 and RANTES as the major eosinophil chemoattractants in the asthmatic lung. J Allergy Clin Immunol. 1996;97:1110–5.CrossRefPubMed

49.

Palframan RT, Collins PD, Severs NJ, Rothery S, Williams TJ, Rankin SM. Mechanisms of acute eosinophil mobilization from the bone marrow stimulated by interleukin 5: the role of specific adhesion molecules and phosphatidylinositol 3-kinase. J Exp Med. 1998;188:1621–32.CrossRefPubMed

50.

Lilly CM, Nakamura H, Kesselman H, Nagler-Anderson C, Asano K, Garcia-Zepeda EA, et al. Expression of eotaxin by human lung epithelial cells: induction by cytokines and inhibition by glucocorticoids. J Clin Invest. 1997;99:1767–73.CrossRefPubMed

51.

Sampson AP. The role of eosinophils and neutrophils in inflammation. Clin Exp Allergy. 2000;30(Suppl 1):22–7.CrossRefPubMed

52.

Arnold R, Konig W. ICAM-1 expression and low-molecular-weight G-protein activation of human bronchial epithelial cells (A549) infected with RSV. J Leukoc Biol. 1996;60:766–71.PubMed

Title: Asthma during pregnancy alters immune cell profile and airway epithelial chemokine release
Authors: Annette Osei-Kumah
Peter A. B. Wark
Roger Smith
Vicki L. Clifton
Publication date: 01-05-2010
Publisher: SP Birkhäuser Verlag Basel
Published in: Inflammation Research / Issue 5/2010
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI: https://doi.org/10.1007/s00011-009-0102-y

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

2024 ASCO Annual Meeting

Springer Medicine

Abstract

Objective

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 5/2010

Chicken type II collagen induced immune balance of main subtype of helper T cells in mesenteric lymph node lymphocytes in rats with collagen-induced arthritis

The effects of bilastine compared with cetirizine, fexofenadine, and placebo on allergen-induced nasal and ocular symptoms in patients exposed to aeroallergen in the Vienna Challenge Chamber

A 12-week regimen of caloric restriction improves levels of adipokines and pro-inflammatory cytokines in Korean women with BMIs greater than 23 kg/m2

Procalcitonin as an early marker of bacterial infection in neutropenic febrile children with acute lymphoblastic leukemia

Paul-Peter Tak, Academic Medical Center, University of Amsterdam, The Netherlands (ed): New Therapeutic Targets in Rheumatoid Arthritis. (PIR: Progress in Inflammation Research Series)

Association between serum amyloid A and obesity: a meta-analysis and systematic review

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials