Sex-specific lung remodeling and inflammation changes in experimental allergic asthma

Journal of Applied Physiology

Volumn 109, Issue 3, 2010, Pages 855-863

  Antunes, Mariana A ^a   Abreu, Soraia C ^a   Silva, Adriana L ^a   Parra Cuentas, Edwin R ^b   Ab'Saber, Alexandre M ^b   Capelozzi, Vera L ^b   Ferreira, Tatiana P T ^c   Martins, Marco A ^c   Silva, Patricia M R ^c   Rocco, Patricia R M ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Actin; Airway hyperresponsiveness; Collagen; Estrogen

Indexed keywords

AUTACOID; BRONCHODILATING AGENT; COLLAGEN; GELATINASE A; GELATINASE B; INTERLEUKIN 4; INTERLEUKIN 5; METHACHOLINE CHLORIDE; MMP2 PROTEIN, MOUSE; MMP9 PROTEIN, MOUSE; OVALBUMIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; ARTICLE; ASTHMA; BAGG ALBINO MOUSE; BRONCHUS HYPERREACTIVITY; CHRONIC DISEASE; COMPARATIVE STUDY; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; EXTRACELLULAR MATRIX; FEMALE; IMMUNOLOGY; INHALATION TEST; LUNG; LUNG LAVAGE; MALE; METABOLISM; MOUSE; OVARIECTOMY; PATHOLOGY; PATHOPHYSIOLOGY; PNEUMONIA; SEX DIFFERENCE; TIME; ULTRASTRUCTURE;

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHIAL PROVOCATION TESTS; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHODILATOR AGENTS; CHRONIC DISEASE; COLLAGEN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR MATRIX; FEMALE; INFLAMMATION MEDIATORS; INTERLEUKIN-4; INTERLEUKIN-5; LUNG; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; METHACHOLINE CHLORIDE; MICE; MICE, INBRED BALB C; OVALBUMIN; OVARIECTOMY; PNEUMONIA; SEX FACTORS; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77957110090     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00333.2010     Document Type: Article

References (40)

1. Abramson M, Kutin JJ, Raven J, Lanigan A, Czarny D, Walters EH. Risk factors for asthma among young adults in Melbourne, Australia. Respirology 1:291-297, 1996.
2. Antunes MA, Abreu SC, Damaceno-Rodrigues NR, Parra ER, Capelozzi VL, Pinart M, Romero PV, Silva PM, Martins MA, Rocco PR. Different strains of mice present distinct lung tissue mechanics and extracellular matrix composition in a model of chronic allergic asthma. Respir Physiol Neurobiol 165:202-207, 2009.
3. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MW. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med 3:1209-1215, 1997.
4. Barr RG, Wentowski CC, Grodstein F, Somers SC, Stampfer MJ, Schwartz J, Speizer FE, Camargo CA Jr. Prospective study of postmenopausal hormone use and newly diagnosed asthma and chronic obstructive pulmonary disease. Arch Intern Med 164:379-386, 2004.
5. Blacquiere MJ, Hylkema MN, Postma DS, Geerlings M, Timens W, Melgert BN. Airway inflammation and remodeling in two mouse models of asthma: comparison of males and females. Int Arch Allergy Immunol 153:173-181, 2010.
6. Card JW, Voltz JW, Ferguson CD, Carey MA, DeGraff LM, Peddada SD, Morgan DL, Zeldin DC. Male sex hormones promote vagally mediated reflex airway responsiveness to cholinergic stimulation. Am J Physiol Lung Cell Mol Physiol 292: L908-L914, 2007.
7. Carey MA, Card JW, Bradbury JA, Moorman MP, Haykal-Coates N, Gavett SH, Graves JP, Walker VR, Flake GP, Voltz JW, Zhu D, Jacobs ER, Dakhama A, Larsen GL, Loader JE, Gelfand EW, Germolec DR, Korach KS, Zeldin DC. Spontaneous airway hyperresponsiveness in estrogen receptor-alpha-deficient mice. Am J Respir Crit Care Med 175:126-135, 2007. (Pubitemid 46115083)
8. Corteling R, Trifilieff A. Gender comparison in a murine model of allergen-driven airway inflammation and the response to budesonide treatment. BMC Pharmacol 4:4, 2004.
9. Crawford WA, Beedham CG. The changing demographic pattern in asthma related to sex and age. A study of 13, 651 patients on sodium cromoglycate (Intal). Med J Aust 1:430-434, 1976.
10. Degano B, Prevost MC, Berger P, Molimard M, Pontier S, Rami J, Escamilla R. Estradiol decreases the acetylcholine-elicited airway reactivity in ovariectomized rats through an increase in epithelial acetylcholinesterase activity. Am J Respir Crit Care Med 164:1849-1854, 2001.
11. Dimitropoulou C, Drakopanagiotakis F, Chatterjee A, Snead C, Catravas JD. Estrogen replacement therapy prevents airway dysfunction in a murine model of allergen-induced asthma. Lung 187:116-127, 2009.
12. Dolhnikoff M, Morin J, Ludwig MS. Human lung parenchyma responds to contractile stimulation. Am J Respir Crit Care Med 158:1607-1612, 1998.
13. Eliasson O, Scherzer HH, DeGraff AC Jr. Morbidity in asthma in relation to the menstrual cycle. J Allergy Clin Immunol 77:87-94, 1986.
14. Ensom MH, Chong G, Beaudin B, Bai TR. Estradiol in severe asthma with premenstrual worsening. Ann Pharmacother 37:1610-1613, 2003.
15. Foster PS, Ming Y, Matthei KI, Young IG, Temelkovski J, Kumar RK. Dissociation of inflammatory and epithelial responses in a murine model of chronic asthma. Lab Invest 80:655-662, 2000.
16. Fullmer HM, Sheetz JH, Narkates AJ. Oxytalan connective tissue fibers: a review. J Oral Pathol 3:291-316, 1974.
17. Gilliver SC, Ruckshanthi JP, Hardman MJ, Nakayama T, Ashcroft GS. Sex dimorphism in wound healing: the roles of sex steroids and macrophage migration inhibitory factor. Endocrinology 149:5747-5757, 2008.
18. Grandas OH, Mountain DH, Kirkpatrick SS, Cassada DC, Stevens SL, Freeman MB, Goldman MH. Regulation of vascular smooth muscle cell expression and function of matrix metalloproteinases is mediated by estrogen and progesterone exposure. J Vasc Surg 49:185-191, 2009.
19. Huerta-Yepez S, Baay-Guzman GJ, Garcia-Zepeda R, Hernandez-Pando R, Vega MI, Gonzalez-Bonilla C, Bonavida B. 2-Methoxyestradiol (2-ME) reduces the airway inflammation and remodeling in an experimental mouse model. Clin Immunol 129:313-324, 2008.
20. Jeffery PK, Godfrey RW, Adelroth E, Nelson F, Rogers A, Johansson SA. Effects of treatment on airway inflammation and thickening of basement membrane reticular collagen in asthma. A quantitative light and electron microscopic study. Am Rev Respir Dis 145:890-899, 1992.
21. Locke NR, Royce SG, Wainewright JS, Samuel CS, Tang ML. Comparison of airway remodeling in acute, subacute, and chronic models of allergic airways disease. Am J Respir Cell Mol Biol 36:625-632, 2007.
22. Matsubara S, Swasey CH, Loader JE, Dakhama A, Joetham A, Ohnishi H, Balhorn A, Miyahara N, Takeda K, Gelfand EW. Estrogen determines sex differences in airway responsiveness after allergen exposure. Am J Respir Cell Mol Biol 38:501-508, 2008.
23. Mattos W, Lim S, Russell R, Jatakanon A, Chung KF, Barnes PJ. Matrix metalloproteinase-9 expression in asthma: effect of asthma severity, allergen challenge, and inhaled corticosteroids. Chest 122:1543-1552, 2002.
24. Melgert BN, Postma DS, Kuipers I, Geerlings M, Luinge MA, van der Strate BW, Kerstjens HA, Timens W, Hylkema MN. Female mice are more susceptible to the development of allergic airway inflammation than male mice. Clin Exp Allergy 35:1496-1503, 2005.
25. Minshall EM, Leung DY, Martin RJ, Song YL, Cameron L, Ernst P, Hamid Q. Eosinophil-associated TGF-beta1 mRNA expression and airways fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 17:326-333, 1997.
26. Montes GS. Structural biology of the fibres of the collagenous and elastic systems. Cell Biol Int 20:15-27, 1996.
27. Nathan BM, Hodges CA, Palmert MR. The use of mouse chromosome substitution strains to investigate the genetic regulation of pubertal timing. Mol Cell Endocrinol 254-255:103-108, 2006.
28. Real FG, Svanes C, Omenaas ER, Anto JM, Plana E, Jarvis D, Janson C, Neukirch F, Zemp E, Dratva J, Wjst M, Svanes K, Leynaert B, Sunyer J. Lung function, respiratory symptoms, and the menopausal transition. J Allergy Clin Immunol 121:72-80. e73, 2008.
29. Riffo-Vasquez Y, Ligeiro de Oliveira AP, Page CP, Spina D, Tavaresde-Lima W. Role of sex hormones in allergic inflammation in mice. Clin Exp Allergy 37:459-470, 2007.
30. Rocco PR, Negri EM, Kurtz PM, Vasconcellos FP, Silva GH, Capelozzi VL, Romero PV, Zin WA. Lung tissue mechanics and extracellular matrix remodeling in acute lung injury. Am J Respir Crit Care Med 164:1067-1071, 2001.
31. Silva PL, Passaro CP, Cagido VR, Bozza M, Dolhnikoff M, Negri EM, Morales MM, Capelozzi VL, Zin WA, Rocco PR. Impact of lung remodelling on respiratory mechanics in a model of severe allergic inflammation. Respir Physiol Neurobiol 160:239-248, 2008.
32. Stevenson S, Nelson LD, Sharpe DT, Thornton MJ. 17Beta-estradiol regulates the secretion of TGF-beta by cultured human dermal fibroblasts. J Biomater Sci Polym Ed 19:1097-1109, 2008.
33. Suzuki T, Sullivan DA. Estrogen stimulation of proinflammatory cytokine and matrix metalloproteinase gene expression in human corneal epithelial cells. Cornea 24:1004-1009, 2005.
34. Tanaka H, Komai M, Nagao K, Ishizaki M, Kajiwara D, Takatsu K, Delespesse G, Nagai H. Role of interleukin-5 and eosinophils in allergeninduced airway remodeling in mice. Am J Respir Cell Mol Biol 31:62-68, 2004.
35. Teodoro WR, Velosa AP, Witzel SS, Garippo AL, Farhat C, Parra ER, Sonohara S, Capelozzi VL, Yoshinari NH. Architectural remodelling in lungs of rabbits induced by type V collagen immunization: a preliminary morphologic model to study diffuse connective tissue diseases. Pathol Res Pract 200:681-691, 2004.
36. Troisi RJ, Speizer FE, Willett WC, Trichopoulos D, Rosner B. Menopause, postmenopausal estrogen preparations, and the risk of adult-onset asthma. A prospective cohort study. Am J Respir Crit Care Med 152:1183-1188, 1995.
37. Van Hove CL, Maes T, Cataldo DD, Gueders MM, Palmans E, Joos GF, Tournoy KG. Comparison of acute inflammatory and chronic structural asthma-like responses between C57BL/6 and BALB/c mice. Int Arch Allergy Immunol 149:195-207, 2009.
38. Weibel ER. Morphometry: stereological theory and practical methods. In: Models of Lung Disease-Microscopy and Structural Methods, edited by Gil J. New York: Dekker, 1990, p. 199-247.
39. Wen FQ, Liu XD, Terasaki Y, Fang QH, Kobayashi T, Abe S, Rennard SI. Interferon-gamma reduces interleukin-4-and interleukin-13-augmented transforming growth factor-beta2 production in human bronchial epithelial cells by targeting Smads. Chest 123:372S-373S, 2003.
40. Xisto DG, Farias LL, Ferreira HC, Picanco MR, Amitrano D, Lapa e Silva JR, Negri EM, Mauad T, Carnielli D, Silva LF, Capelozzi VL, Faffe DS, Zin WA, Rocco PR. Lung parenchyma remodeling in a murine model of chronic allergic inflammation. Am J Respir Crit Care Med 171:829-837, 2005.