Hypertrophic airway smooth muscle mass correlates with increased airway responsiveness in a murine model of asthma

American Journal of Respiratory Cell and Molecular Biology

Volumn 46, Issue 4, 2012, Pages 532-540

  Plant, Pamela J ^a,b   North, Michelle L ^a   Ward, Andrew ^b   Ward, Michael ^a,b   Khanna, Nivedita ^a   Correa, Judy ^a,b   Scott, Jeremy A ^a,b   Batt, Jane ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Airway smooth muscle; Apoptosis; Constant phase model; Hypertrophy; Proliferation

Indexed keywords

METHACHOLINE; OVALBUMIN;

AIRWAY DYNAMICS; AIRWAY RESISTANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTHMA; BREATHING MECHANICS; BREATHING MUSCLE; CELL PROLIFERATION; CLINICAL ASSESSMENT; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MODEL; FEMALE; IMMUNOHISTOCHEMISTRY; ISOLATED LUNG; MOUSE; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; RESPIRATORY TRACT INFLAMMATION; VENTILATOR;

AIRWAY RESISTANCE; ANIMALS; APOPTOSIS; ASTHMA; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; HYPERTROPHY; METHACHOLINE CHLORIDE; MICE; MICE, INBRED BALB C; MUSCLE, SMOOTH; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY;

MURINAE; MUS;

EID: 84859389700     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0293OC     Document Type: Article

References (38)

1. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745. (Pubitemid 30329053)
2. Busse W, Elias J, Sheppard D, Banks-Schlegel S. Airway remodeling and repair. Am J Respir Crit Care Med 1999;160:1035-1042. (Pubitemid 29442050)
3. Elias JA, Zhu Z, Chupp G, Homer RJ. Airway remodeling in asthma. J Clin Invest 1999;104:1001-1006.
4. Vignola AM, Kips J, Bousquet J. Tissue remodeling as a feature of persistent asthma. J Allergy Clin Immunol 2000;105:1041-1053. (Pubitemid 30418779)
5. Vignola AM, Chanez P, Bonsignore G, Godard P, Bousquet J. Structural consequences of airway inflammation in asthma. J Allergy Clin Immunol 2000;105:S514-S517. (Pubitemid 30109018)
6. Benayoun L, Druilhe A, Dombret MC, Aubier M, Pretolani M. Airway structural alterations selectively associated with severe asthma. Am J Respir Crit Care Med 2003;167:1360-1368. (Pubitemid 36609720)
7. Woodruff PG, Dolganov GM, Ferrando RE, Donnelly S, Hays SR, Solberg OD, Carter R, Wong HH, Cadbury PS, Fahy JV. Hyperplasia of smooth muscle in mild to moderate asthma without changes in cell size or gene expression. Am J Respir Crit Care Med 2004;169:1001-1006. (Pubitemid 38543637)
8. Jenkins HA, Cool C, Szefler SJ, Covar R, Brugman S, Gelfand EW, Spahn JD. Histopathology of severe childhood asthma: a case series. Chest 2003;124:32-41. (Pubitemid 36851328)
9. Lambert RK, Wiggs BR, Kuwano K, Hogg JC, Pare PD. Functional significance of increased airway smooth muscle in asthma and COPD. J Appl Physiol 1993;74:2771-2781. (Pubitemid 23201305)
10. Henderson WR Jr, Tang LO, Chu SJ, Tsao SM, Chiang GK, Jones F, Jonas M, Pae C, Wang H, Chi EY. A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am J Respir Crit Care Med 2002;165:108-116. (Pubitemid 34053366)
11. Southam DS, Ellis R, Wattie J, Inman MD. Components of airway hyperresponsiveness and their associations with inflammation and remodeling in mice. J Allergy Clin Immunol 2007;119:848-854. (Pubitemid 46527815)
12. Leigh R, Ellis R, Wattie J, Southam DS, De HM, Gauldie J, O'Byrne PM, Inman MD. Dysfunction and remodeling of the mouse airway persist after resolution of acute allergen-induced airway inflammation. Am J Respir Cell Mol Biol 2002;27:526-535. (Pubitemid 35301806)
13. Deng H, Dokshin GA, Lei J, Goldsmith AM, Bitar KN, Fingar DC, Hershenson MB, Bentley JK. Inhibition of glycogen synthase kinase-3beta is sufficient for airway smooth muscle hypertrophy. J Biol Chem 2008;283:10198-10207.
14. Goldsmith AM, Bentley JK, Zhou L, Jia Y, Bitar KN, Fingar DC, Hershenson MB. Transforming growth factor-beta induces airway smooth muscle hypertrophy. Am J Respir Cell Mol Biol 2006;34:247-254. (Pubitemid 43202473)
15. Halayko AJ, Solway J. Molecular mechanisms of phenotypic plasticity in smooth muscle cells. J Appl Physiol 2001;90:358-368. (Pubitemid 32038538)
16. Johnson PR, Roth M, Tamm M, Hughes M, Ge Q, King G, Burgess JK, Black JL. Airway smooth muscle cell proliferation is increased in asthma. Am J Respir Crit Care Med 2001;164:474-477. (Pubitemid 32778219)
17. Ma X, Cheng Z, Kong H, Wang Y, Unruh H, Stephens NL, Laviolette M. Changes in biophysical and biochemical properties of single bronchial smooth muscle cells from asthmatic subjects. Am J Physiol Lung Cell Mol Physiol 2002;283:L1181-L1189. (Pubitemid 35379249)
18. Borger P, Miglino N, Baraket M, Black JL, Tamm M, Roth M. Impaired translation of CCAAT/enhancer binding protein alpha mRNA in bronchial smooth muscle cells of asthmatic patients. J Allergy Clin Immunol 2009;123:639-645.
19. Ebina M, Takahashi T, Chiba T, Motomiya M. Cellular hypertrophy and hyperplasia of airway smooth muscles underlying bronchial asthma: a 3-D morphometric study. Am Rev Respir Dis 1993;148:720-726. (Pubitemid 23263786)
20. North ML, Khanna N, Marsden PA, Grasemann H, Scott JA. Functionally important role for arginase 1 in the airway hyperresponsiveness of asthma. Am J Physiol Lung Cell Mol Physiol 2009;296:L911-L920.
21. Tomioka S, Bates JH, Irvin CG. Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations. J Appl Physiol 2002;93:263-270. (Pubitemid 34686220)
22. Bates JH, Rincon M, Irvin CG. Animal models of asthma. Am J Physiol Lung Cell Mol Physiol 2009;297:L401-L410.
23. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 1992;72: 168-178.
24. Wagers S, Lundblad LK, Ekman M, Irvin CG, Bates JH. The allergic mouse model of asthma: normal smooth muscle in an abnormal lung? J Appl Physiol 2004;96:2019-2027. (Pubitemid 38661478)
25. Lundblad LK, Thompson-Figueroa J, Allen GB, Rinaldi L, Norton RJ, Irvin CG, Bates JH. Airway hyperresponsiveness in allergically inflamed mice: the role of airway closure. Am J Respir Crit Care Med 2007;175:768-774. (Pubitemid 46631787)
26. Hirota JA, Ellis R, Inman MD. Regional differences in the pattern of airway remodeling following chronic allergen exposure in mice. Respir Res 2006;7:120.
27. Cowan KN, Jones PL, Rabinovitch M. Regression of hypertrophied rat pulmonary arteries in organ culture is associated with suppression of proteolytic activity, inhibition of tenascin-C, and smooth muscle cell apoptosis. Circ Res 1999;84:1223-1233. (Pubitemid 29244784)
28. Bentley JK, Deng H, Linn MJ, Lei J, Dokshin GA, Fingar DC, Bitar KN, Henderson WR Jr, Hershenson MB. Airway smooth muscle hyperplasia and hypertrophy correlate with glycogen synthase kinase-3(beta) phosphorylation in a mouse model of asthma. Am J Physiol Lung Cell Mol Physiol 2009;296:L176-L184.
29. Bentley JK, Hershenson MB. Airway smooth muscle growth in asthma: proliferation, hypertrophy, and migration. Proc Am Thorac Soc 2008; 5:89-96.
30. 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 2007;36: 625-632. (Pubitemid 46676722)
31. Pinelli V, Marchica CL, Ludwig MS. Allergen-induced asthma in C57Bl/ 6 mice: hyper-responsiveness, inflammation and remodelling. Respir Physiol Neurobiol 2009;169:36-43.
32. Trian T, Benard G, Begueret H, Rossignol R, Girodet PO, Ghosh D, Ousova O, Vernejoux JM, Marthan R, Tunon-de-Lara JM, et al. Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med 2007;204: 3173-3181.
33. Roth M, Johnson PR, Borger P, Bihl MP, Rudiger JJ, King GG, Ge Q, Hostettler K, Burgess JK, Black JL, et al. Dysfunctional interaction of C/EBPalpha and the glucocorticoid receptor in asthmatic bronchial smooth-muscle cells. N Engl J Med 2004;351:560-574. (Pubitemid 39025173)
34. Johnson PR, Burgess JK, Underwood PA, Au W, Poniris MH, Tamm M, Ge Q, Roth M, Black JL. Extracellular matrix proteins modulate asthmatic airway smooth muscle cell proliferation via an autocrine mechanism. J Allergy Clin Immunol 2004;113:690-696. (Pubitemid 38530425)
35. Castro M, Rubin AS, Laviolette M, Fiterman J, De Andrade LM, Shah PL, Fiss E, Olivenstein R, Thomson NC, Niven RM, et al. Effectiveness and safety of bronchial thermoplasty in the treatment of severe asthma: a multicenter, randomized, double-blind, shamcontrolled clinical trial. Am J Respir Crit Care Med 2010;181:116-124.
36. Cox G, Thomson NC, Rubin AS, Niven RM, Corris PA, Siersted HC, Olivenstein R, Pavord ID, McCormack D, Chaudhuri R, et al. Asthma control during the year after bronchial thermoplasty. N Engl J Med 2007;356:1327-1337. (Pubitemid 46513298)
37. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 2005;37:1974-1984. (Pubitemid 41206815)
38. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/AKT pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 2004;14:395-403. (Pubitemid 38591410)