Environmental Tobacco Smoke and Progesterone Alter Lung Inflammation and Mucous Metaplasia in a Mouse Model of Allergic Airway Disease

American Lung Association (2005) Trends in asthma morbidity and mortality. Epidemiology and Statistics Unit, Research and Program Services

Balzar S, Strand M, Rhodes D, Wenzel SE (2007) IgE expression pattern in lung: relation to systemic IgE and asthma phenotypes. J Allergy Clin Immunol 119(4):855–862

Camancho-Arroyo I, Ruiz A, Gamboa-Dominguez A, Perez-Palacios G, Cerbon M (1994) Immunohistochemical localization of intracellular progesterone and glucocorticoid receptors in the rabbit lung. J Endocrinol 142:311–316

Chen Y, Stewart P, Johansen H, McRae L, Taylor G (2003) Sex difference in hospitalization due to asthma in relation to age. J Clin Epidemiol 56:180–187

de Marco R, Locatelli F, Sunyer J, Burney P, The European Community Respiratory Health Survey Study Group (2000) Differences in incidence of reported asthma related to age in men and women. A retrospective analysis of the data of the European respiratory health survey. Am J Respir Crit Care Med 162:68–74

Deb R, Shakib F, Reid K, Clark H (2007) Major house dust mite allergens Dermatophagoides pteronyssinus 1 and Dermatophagoides farinae 1 degrade and inactivate lung surfactant proteins A and D. J Biol Chem 282(51):36808–36819

Diaz-Sanchez D, Rumold R, Gong H Jr (2006) Challenge with environmental tobacco smoke exacerbates allergic airway disease in human beings. J Allergy Clin Immunol 118(2):441–446

Elias JA, Zhu Z, Chupp G, Homer RJ (1999) Airway remodeling in asthma. J Clin Invest 104(8):1001–1006

Elliot JG, Jensen CM, Mutavdzic S, Lamb JP, Carroll NG, James AL (2004) Aggregations of lymphoid cells in the airways of nonsmokers, smokers, and subjects with asthma. Am J Respir Crit Care Med 169(6):712–718

Faas M, Bouman A, Moes H, Heineman MJ, Leij LD, Schuiling G (2000) The immune response during the luteal phase of the ovarian cycle: a Th2-type response? Fertil Steril 74(5):1008–1013

Flickinger G, Elsner C, Illingworth D, Muechler E, Mikhail G (1977) Estrogen and progesterone receptors in the female genital tract of humans and monkeys. Ann N Y Acad Sci 286:180–189

Fuchs B, Braun A (2008) Improved mouse models of allergy and allergic asthma—chances beyond ovalbumin. Curr Drug Targets 9(6):495–502

Gershwin LJ (2007) Effects of allergenic extracts on airway epithelium. Curr Allergy Asthma Rep 7(5):357–362

Girod S, Zahm J, Plotkowski C, Beck G, Puchelle E (1992) Role of physiochemical properties of mucus in the protection of the respiratory epithelium. Eur Respir J 5(4):477–487

Hellings PW, Vandekerckhove P, Claeys R, Billen J, Kasran A, Ceuppens JL (2003) Progesterone increases airway eosinophilia and hyper-responsiveness in a murine model of allergic asthma. Clin Exp Allergy 33:1457–1463

Lange P, Parner J, Prescott E, Ulrik CS, Vestbo J (2001) Exogenous female sex steroid hormones and risk of asthma and asthma-like symptoms: a cross sectional study of the general population. Thorax 56:613–616

Lemanske RF, Busse WW (2003) 6. Asthma. J Allergy Clin Immunol 111(2, Supplement 2):502–519

Maestrelli P, Saetta M, Mapp CE, Fabbri LM (2001) Remodeling in response to infection and injury. Airway inflammation and hypersecretion of mucus in smoking subjects with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164(10):76S–80S

Martinez-Moragon E, Plaza V, Serrano J, Picado C, Galdiz JB, Lopez-Vina A, Sanchis J, The Spanish High Risk Asthma Research Group (2004) Near-fatal asthma related to menstruation. J Allergy Clin Immunol 113(2):242–244

Meek MD (2001) Cigarette smoking and hormone balance in women: new evidence in the anti-smoking campaign. Univ Tor Med J 79(1):8–11

Meek MD, Finch GL (1999) Diluted mainstream cigarette smoke condensates activate estrogen receptor and aryl hydrocarbon receptor-mediated gene transcription. Environ Res 80(1):9–17

Middlebrook G (1952) An apparatus for airborne infection of mice. Proc Soc Exp Biol Med 80(1):105–110

Miller LA, Hurst SD, Coffman RL, Tyler NK, Stovall MY, Chou DL, Putney LF, Gershwin LJ, Schelegle ES, Plopper CG, Hyde DM (2005) Airway generation-specific differences in the spatial distribution of immune cells and cytokines in allergen-challenged rhesus monkeys. Clin Exp Allergy 35(7):894–906

Mitchell VL, Gershwin LJ (2007) Progesterone and environmental tobacco smoke act synergistically to exacerbate the development of allergic asthma in a mouse model. Clin Exp Allergy 37(2):276–286

Moerloose KB, Robays LJ, Maes T, Brusselle GG, Tournoy KG, Joos GF (2006) Cigarette smoke exposure facilitates allergic sensitization in mice. Respir Res 7:49

Niimi A, Amitani R, Suzuki K, Tanaka E, Murayama T, Kuze F (1998) Eosinophilic inflammation in cough variant asthma. Eur Respir J 11(5):1064–1069

Pauli B, Reid R, Munt P, Wigle R, Forkert L (1989) Influence of the menstrual cycle on airway function in asthmatic and normal subjects. Am Rev Respir Dis 140(2):358–362

Rangel-Moreno J, Hartson L, Navarro C, Gaxiola M, Selman M, Randall TD (2006) Inducible bronchus-associated lymphoid tissue (iBALT) in patients with pulmonary complications of rheumatoid arthritis. J Clin Invest 116(12):3183–3194

Redmond AM, James AW, Nolan SH, Self TH (2004) Premenstrual asthma: emphasis on drug therapy options. J Asthma 41(7):687–693

Rumold R, Jyrala M, Diaz-Sanchez D (2001) Secondhand smoke induces allergic sensitization in mice. J Immunol 167(8):4765–4770

Seymour BWP, Friebertshauser KE, Peake JL, Pinkerton KE, Coffman RL, Gershwin LJ (2002) Gender differences in the allergic response of mice neonatally exposed to environmental tobacco smoke. Dev Immunol 9(1):47–54

Seymour BWP, Pinkerton KE, Friebertshauser KE, Coffman RL, Gershwin LJ (1997) Second-hand smoke is an adjuvant for T Helper-2 responses in a murine model of allergy. J Immunol 159:6169–6175

Shao R, Egeciolu E, Weijdegard B, Ljungstrom K, Ling C, Fernandez-Rodriguez J, Billig H (2006) Developmental and hormonal regulation of progesterone receptor A-form expression in female mouse lung in vivo: interaction with glucocorticoid receptors. J Endocrinol 190:857–870

Skobeloff E, Spivey W, St Clair S, Schoffstall J (1992) The influence of age and sex on asthma admissions. JAMA 268:3437–3440

Smith MN (2007) Medical encyclopedia: serum progesterone. MedlinePlus, US National Library of Medicine and the National Institutes of Health

Stanford KI, Mickleborough TD, Ray S, Lindley MR, Koceja DM, Stager JM (2006) Influence of menstrual cyle phase on pulmonary function in asthmatic athletes. Eur J Appl Physiol 96(6):703–710

Suda T, Chida K, Hayakawa H, Imokawa S, Iwata M, Nakamura H, Sato A (1999) Development of bronchus-associated lymphoid tissue in chronic hypersensitivity pneumonitis. Chest 115(2):357–363

Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L (2001) Progesterone as an immunomodulatory molecule. Int Immunopharmacol 1:1037–1048

Tan K, McFarlane L, Lipworth B (1997) Modulation of airway reactivity and peak flow variability in asthmatics receiving the oral contraceptive pill. Am J Respir Crit Care Med 155:1273–1277

Teague SV, Pinkerton KE, Goldsmith M, Gebremichael A, Chang S, Jenkins RA, Moneyhun JH (1994) Sidestream cigarette smoke generation and exposure system for environmental tobacco smoke studies. Inhal Toxicol 6:79–93

Trimble NJ, Botelho FM, Bauer CM, Fattouh R, Stampfli MR (2009) Adjuvant and anti-inflammatory properties of cigarette smoke in murine allergic airway inflammation. Am J Respir Cell Mol Biol 40(1):38–46

Troisi R, Speizer F, Willett W, Trichopoulos D, Rosner B (1995) Menopause, postmenopausal estrogen preparations and the risk of adult-onset asthma. A prospective cohort study. Am J Respir Crit Care Med 152:1183–1188

Van Hove CL, Moerloose K, Maes T, Joos GF, Tournoy KG (2008) Cigarette smoke enhances Th-2 driven airway inflammation and delays inhalational tolerance. Respir Res 9:42

Van Winkle LS, Evans MJ, Brown CD, Willits NH, Pinkerton KE, Plopper CG (2001) Prior exposure to aged and diluted sidestream cigarette smoke impairs bronchiolar injury and repair. Toxicol Sci 60(1):152–164

Venn A, Lewis S, Cooper M, Hill J, Britton J (1998) Questionnaire study of effect of sex and age on the prevalence of wheeze and asthma in adolescence. BMJ 316(7149):1945–1946

Vu Hai MT, Logeat F, Warembourg M, Milgrom E (1977) Hormonal control of progesterone receptors. Ann N Y Acad Sci 286:199–209

Walter MJ, Kajiwara N, Karanja P, Castro M, Holtzman MJ (2001) Interleukin 12 p40 production by barrier epithelial cells during airway inflammation. J Exp Med 193(3):339–351

Wood GA, Fata JE, Watson KLM, Khokha R (2007) Circulating hormones and estrous stage predict cellular and stromal remodeling in murine uterus 10.1530/REP-06-0302. Reproduction 133(5):1035–1044

Yoshimoto T, Wang CR, Yoneto T, Waki S, Sunaga S, Komagata Y, Mitsuyama M, Miyazaki J, Nariuchi H (1998) Reduced T helper 1 responses in IL-12 p40 transgenic mice. J Immunol 160(2):588–594