Airway structural components drive airway smooth muscle remodeling in asthma

Proceedings of the American Thoracic Society

Volumn 6, Issue 8, 2009, Pages 683-692

  Dekkers, Bart G J ^a   Maarsingh, Harm ^a   Meurs, Herman ^a   Gosens, Reinoud ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Acetylcholine; Airway remodeling; Anticholinergics; Arginase; Extracellular matrix

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; ACETYLCHOLINE; ARGINASE; ARGININE; ARGINYLGLYCYLASPARTYLSERINE; CONNECTIVE TISSUE GROWTH FACTOR; CYCLIN D1; EPIDERMAL GROWTH FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; IPRATROPIUM BROMIDE; MUSCARINIC M2 RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PLATELET DERIVED GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VERY LATE ACTIVATION ANTIGEN 5;

ACETYLCHOLINE RELEASE; ALLERGIC ASTHMA; ASTHMA; BREATHING MUSCLE; BRONCHUS HYPERREACTIVITY; CHOLINERGIC SYSTEM; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RESPIRATORY EPITHELIUM; REVIEW; SMOOTH MUSCLE;

AIRWAY REMODELING; ASTHMA; CHRONIC DISEASE; EXTRACELLULAR MATRIX; HUMANS; MUSCLE, SMOOTH; PARASYMPATHETIC NERVOUS SYSTEM; RESPIRATORY MUCOSA; RESPIRATORY SYSTEM;

EID: 74849084373     PISSN: 15463222     EISSN: None     Source Type: Journal    
DOI: 10.1513/pats.200907-056DP     Document Type: Review

References (157)

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.
2. Postma DS, Kerstjens HA. Characteristics of airway hyperresponsiveness in asthma and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998;158:S187-S192.
3. Cockcroft DW, Davis BE. Mechanisms of airway hyperresponsiveness. J Allergy Clin Immunol 2006;118:551-559.
4. Jeffery PK. Remodeling in asthma and chronic obstructive lung disease. Am J Respir Crit Care Med 2001;164:S28-S38.
5. Lloyd CM, Robinson DS. Allergen-induced airway remodelling. Eur Respir J 2007;29:1020-1032.
6. Postma DS, Timens W. Remodeling in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc 2006;3:434-439.
7. 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.
8. Leguillette R, Laviolette M, Bergeron C, Zitouni NB, Kogut P, Solway J, Kashmar L, Hamid Q, Lauzon AM. Myosin, transgelin, and myosin light chain kinase: expression and function in asthma. Am J Respir Crit Care Med 2008;179:194-204.
9. Leguillette R, Lauzon AM. Molecular mechanics of smooth muscle contractile proteins in airway hyperresponsiveness and asthma. Proc Am Thorac Soc 2008;5:40-46.
10. Slats AM, Janssen K, van Schadewick A, van der Plas DT, Schot R, van den Aardweg JG, de Jongste JC, Hiemstra PS, Mauad T, Rabe KF, et al. Expression of smooth muscle and extracellular matrix proteins in relation to airway function in asthma. J Allergy Clin Immunol 2008; 121:1196-1202.
11. Matsumoto H, Moir LM, Oliver BG, Burgess JK, Roth M, Black JL, McParland BE. Comparison of gel contraction mediated by airway smooth muscle cells from patients with and without asthma. Thorax 2007;62:848-854.
12. Stephens NL, Fust A, Jiang H, Li W, Ma X. Isotonic relaxation of control and sensitized airway smooth muscle. Can J Physiol Pharmacol 2005;83:941-951.
13. 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.
14. Oliver MN, Fabry B, Marinkovic A, Mijailovich SM, Butler JP, Fredberg JJ. Airway hyperresponsiveness, remodeling, and smooth muscle mass: right answer, wrong reason? Am J Respir Cell Mol Biol 2007;37:264-272.
15. 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.
16. 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.
17. 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.
18. 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.
19. James AL, Bai TR, Mauad T, Abramson MJ, Dolhnikoff M, McKay KO, Maxwell PS, Elliot JG, Green FH. Airway smooth muscle thickness in asthma is related to severity but not duration of asthma. Eur Respir J 2009;34:1040-1045.
20. Bai TR, Cooper J, Koelmeyer T, Pare PD, Weir TD. The effect of age and duration of disease on airway structure in fatal asthma. Am J Respir Crit Care Med 2000;162:663-669.
21. Pepe C, Foley S, Shannon J, Lemiere C, Olivenstein R, Ernst P, Ludwig MS, Martin JG, Hamid Q. Differences in airway remodeling between subjects with severe and moderate asthma. J Allergy Clin Immunol 2005;116:544-549.
22. Burgess JK, Johnson PR, Ge Q, Au WW, Poniris MH, McParland BE, King G, Roth M, Black JL. Expression of connective tissue growth factor in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2003;167:71-77.
23. Chan V, Burgess JK, Ratoff JC, O'Connor BJ, Greenough A, Lee TH, Hirst SJ. Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006;174:379-385.
24. Simcock DE, Kanabar V, Clarke GW, Mahn K, Karner C, O'Connor BJ, Lee TH, Hirst SJ. Induction of angiogenesis by airway smooth muscle from patients with asthma. Am J Respir Crit Care Med 2008; 178:460-468.
25. Chambers LS, Black JL, Ge Q, Carlin SM, Au WW, Poniris M, Thompson J, Johnson PR, Burgess JK. PAR-2 activation, PGE2, and COX-2 in human asthmatic and nonasthmatic airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2003;285:L619-L627.
26. 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.
27. 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.
28. 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.
29. 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.
30. Xu KF, Vlahos R, Messina A, Bamford TL, Bertram JF, Stewart AG. Antigen-induced airway inflammation in the Brown Norway rat results in airway smooth muscle hyperplasia. J Appl Physiol 2002; 93:1833-1840.
31. Gosens R, Roscioni SS, Dekkers BG, Pera T, Schmidt M, Schaafsma D, Zaagsma J, Meurs H. Pharmacology of airway smooth muscle proliferation. Eur J Pharmacol 2008;585:385-397.
32. Payne DN, Rogers AV, Adelroth E, Bandi V, Guntupalli KK, Bush A, Jeffery PK. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med 2003;167: 78-82.
33. Regamey N, Ochs M, Hilliard TN, Muhlfeld C, Cornish N, Fleming L, Saglani S, Alton EW, Bush A, Jeffery PK, et al. Increased airway smooth muscle mass in children with asthma, cystic fibrosis, and non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med 2008;177: 837-843.
34. Saglani S, Payne DN, Zhu J, Wang Z, Nicholson AG, Bush A, Jeffery PK. Early detection of airway wall remodeling and eosinophilic inflammation in preschool wheezers. Am J Respir Crit Care Med 2007;176:858-864.
35. 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.
36. Henderson WR Jr, Chiang GK, Tien YT, Chi EY. Reversal of allergen-induced airway remodeling by CysLT1 receptor blockade. Am J Respir Crit Care Med 2006;173:718-728.
37. Vanacker NJ, Palmans E, Kips JC, Pauwels RA. Fluticasone inhibits but does not reverse allergen-induced structural airway changes. Am J Respir Crit Care Med 2001;163:674-679.
38. Holgate ST. The airway epithelium is central to the pathogenesis of asthma. Allergol Int 2008;57:1-10.
39. Holgate ST, Davies DE, Puddicombe S, Richter A, Lackie P, Lordan J, Howarth P. Mechanisms of airway epithelial damage: epithelial-mesenchymal interactions in the pathogenesis of asthma. Eur Respir J Suppl 2003;44:24s-29s.
40. Holgate ST, Holloway J, Wilson S, Bucchieri F, Puddicombe S, Davies DE. Epithelial-mesenchymal communication in the pathogenesis of chronic asthma. Proc Am Thorac Soc 2004;1:93-98.
41. Holgate ST, Davies DE, Powell RM, Howarth PH, Haitchi HM, Holloway JW. Local genetic and environmental factors in asthma disease pathogenesis: chronicity and persistence mechanisms. Eur Respir J 2007;29:793-803.
42. Moncada S, Palmer RM, Higgs EA. Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochem Pharmacol 1989;38:1709-1715.
43. Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol Rev 2004;84:731-765.
44. Yan ZQ, Hanson GK, Skoogh BE, Lotvall JO. Induction of nitric oxide synthase in a model of allergic occupational asthma. Allergy 1995;50: 760-764.
45. Maarsingh H, Zaagsma J, Meurs H. Arginine homeostasis in allergic asthma. Eur J Pharmacol 2008;585:375-384.
46. Kharitonov S, O'Connor BJ, Evans DJ, Barnes PJ. Allergen-induced late asthmatic reactions are associated with elevation of exhaled nitric oxide. Am J Respir Crit Care Med 1995;151:1894-1897.
47. Kharitonov SA, Yates D, Robbins RA, Logan-Sinclair R, Shinebourne EA, Barnes PJ. Increased nitric oxide in exhaled air of asthmatic patients. Lancet 1994;343:133-135.
48. de Boer J, Meurs H, Coers W, Koopal M, Bottone AE, Visser AC, Timens W, Zaagsma J. Deficiency of nitric oxide in allergen-induced airway hyperreactivity to contractile agonists after the early asthmatic reaction: an ex vivo study. Br J Pharmacol 1996;119:1109-1116.
49. Maarsingh H, Leusink J, Bos IST, Zaagsma J, Meurs H. Arginase strongly impairs neuronal nitric oxide-mediated airway smooth muscle relaxation in allergic asthma. Respir Res 2006;7:6.
50. Maarsingh H, Bossenga BE, Bos IST, Volders HH, Zaagsma J, Meurs H. L-Arginine deficiency causes airway hyperresponsiveness after the late asthmatic reaction. Eur Respir J 2009;34:191-199.
51. Mehta S, Drazen JM, Lilly CM. Endogenous nitric oxide and allergic bronchial hyperresponsiveness in guinea pigs. Am J Physiol 1997;273: L656-L662.
52. Samb A, Pretolani M, Dinh-Xuan AT, Ouksel H, Callebert J, Lisdero C, Aubier M, Boczkowski J. Decreased pulmonary and tracheal smooth muscle expression and activity of type 1 nitric oxide synthase (nNOS) after ovalbumin immunization and multiple aerosol challenge in guinea pigs. Am J Respir Crit Care Med 2001;164:149-154.
53. Schuiling M, Meurs H, Zuidhof AB, Venema N, Zaagsma J. Dual action of iNOS-derived nitric oxide in allergen-induced airway hyperreactivity in conscious, unrestrained guinea pigs. Am J Respir Crit Care Med 1998;158:1442-1449.
54. Schuiling M, Zuidhof AB, Bonouvrie MA, Venema N, Zaagsma J, Meurs H. Role of nitric oxide in the development and partial reversal of allergen-induced airway hyperreactivity in conscious, unrestrained guinea-pigs. Br J Pharmacol 1998;123:1450-1456.
55. Ricciardolo FL, Timmers MC, Geppetti P, van Schadewijk A, Brahim JJ, Sont JK, de Gouw HW, Hiemstra PS, van Krieken JH, Sterk PJ. Allergen-induced impairment of bronchoprotective nitric oxide synthesis in asthma. J Allergy Clin Immunol 2001;108:198-204.
56. Ricciardolo FLM, DiMaria GU, Mistretta A, Sapienza MA, Geppetti P. Impairment of bronchoprotection by nitric oxide in severe asthma. Lancet 1997;350:1297-1298.
57. de Boer J, Duyvendak M, Schuurman FE, Pouw FM, Zaagsma J,Meurs H. Role of L-arginine in the deficiency of nitric oxide and airway hyperreactivity after the allergen-induced early asthmatic reaction in guinea-pigs. Br J Pharmacol 1999;128:1114-1120.
58. Maarsingh H, Zuidhof AB, Bos IS, Van Duin M, Boucher JL, Zaagsma J, Meurs H. Arginase inhibition protects against allergic airway obstruction, hyperresponsiveness and inflammation. Am J Respir Crit Care Med 2008;178:565-573.
59. Xia Y, Zweier JL. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 1997;94:6954-6958.
60. de Boer J, Meurs H, Flendrig L, Koopal M, Zaagsma J. Role of nitric oxide and superoxide in allergen-induced airway hyperreactivity after the late asthmatic reaction in guinea-pigs. Br J Pharmacol 2001;133: 1235-1242.
61. Fischer BM, Voynow JA. Neutrophil elastase induces MUC5AC gene expression in airway epithelium via a pathway involving reactive oxygen species. Am J Respir Cell Mol Biol 2002;26:447-452.
62. Muijsers RB, van Ark I, Folkerts G, Koster AS, van Oosterhout AJ, Postma DS, Nijkamp FP. Apocynin and 1400 W prevents airway hyperresponsiveness during allergic reactions in mice. Br J Pharmacol 2001;134:434-440.
63. Sadeghi-Hashjin G, Folkerts G, Henricks PAJ, Verheyen AKCP, van der Linde HJ, Van Ark I, Coene A, Nijkamp FP. Peroxynitrite induces airway hyperresponsiveness in guinea pigs in vitro and in vivo. Am J Respir Crit Care Med 1996;153:1697-1701.
64. Hamad AM, Johnson SR, Knox AJ. Antiproliferative effects of NO and ANP in cultured human airway smooth muscle. Am J Physiol 1999;277:L910-L918.
65. Hamad AM, Knox AJ. Mechanisms mediating the antiproliferative effects of nitric oxide in cultured human airway smooth muscle cells. FEBS Lett 2001;506:91-96.
66. Patel HJ, Belvisi MG, Donnelly LE, Yacoub MH, Chung KF, Mitchell JA. Constitutive expressions of type I NOS in human airway smooth muscle cells: evidence for an antiproliferative role. FASEB J 1999;13: 1810-1816.
67. Kizawa Y, Ohuchi N, Saito K, Kusama T, Murakami H. Effects of endothelin-1 and nitric oxide on proliferation of cultured guinea pig bronchial smooth muscle cells. Comp Biochem Physiol C Toxicol Pharmacol 2001;128:495-501.
68. Pilz RB, Casteel DE. Regulation of gene expression by cyclic GMP. Circ Res 2003;93:1034-1046.
69. Kapadia MR, Eng JW, Jiang Q, Stoyanovsky DA, Kibbe MR. Nitric oxide regulates the 26S proteasome in vascular smooth muscle cells. Nitric Oxide 2009;20:279-288.
70. Sandirasegarane L, Charles R, Bourbon N, Kester M. NO regulates PDGF-induced activation of PKB but not ERK in A7r5 cells: implications for vascular growth arrest. Am J Physiol Cell Physiol 2000;279:C225-C235.
71. Estrada C, Gomez C, Martin-Nieto J, De Frutos T, Jimenez A, Villalobo A. Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem J 1997;326:369-376.
72. Murillo-Carretero M, Torroglosa A, Castro C, Villalobo A, Estrada C. S-Nitrosylation of the epidermal growth factor receptor: a regulatory mechanism of receptor tyrosine kinase activity. Free Radic Biol Med 2009;46:471-479.
73. Que LG, Kantrow SP, Jenkinson CP, Piantadosi CA, Huang YC. Induction of arginase isoforms in the lung during hyperoxia. Am J Physiol 1998;275:L96-L102.
74. Maarsingh H, Pera T, Meurs H. Arginase and pulmonary diseases. Naunyn Schmiedebergs Arch Pharmacol 2008;378:171-184.
75. Morris CR, Poljakovic M, Lavrisha L, Machado L, Kuypers FA, Morris SM Jr. Decreased arginine bioavailability and increased serum arginase activity in asthma. Am J Respir Crit Care Med 2004;170: 148-153.
76. North ML, Khanna N, Marsden PA, Grasemann H, Scott JA. Functionally important role for arginase 1 in the airway hyperres-ponsiveness of asthma. Am J Physiol Lung Cell Mol Physiol 2009;296: L911-L920.
77. Zimmermann N, King NE, Laporte J, Yang M, Mishra A, Pope SM, Muntel EE, Witte DP, Pegg AA, Foster PS, et al. Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J Clin Invest 2003;111:1863-1874.
78. Yang M, Rangasamy D, Matthaei KI, Frew AJ, Zimmmermann N, Mahalingam S, Webb DC, Tremethick DJ, Thompson PJ, Hogan SP, et al. Inhibition of arginase I activity by RNA interference attenuates IL-13-induced airways hyperresponsiveness. J Immunol 2006;177: 5595-5603.
79. Meurs H, McKay S, Maarsingh H, Hamer MA, Macic L, Molendijk N, Zaagsma J. Increased arginase activity underlies allergen-induced deficiency of cNOS-derived nitric oxide and airway hyperresponsiveness. Br J Pharmacol 2002;136:391-398.
80. Maarsingh H, de Boer J, Kauffman HF, Zaagsma J, Meurs H. Heparin normalizes allergen-induced nitric oxide deficiency and airway hyperresponsiveness. Br J Pharmacol 2004;142:1293-1299.
81. Meurs H, Maarsingh H, Zaagsma J. Arginase and asthma: novel insights into nitric oxide homeostasis and airway hyperresponsiveness. Trends Pharmacol Sci 2003;24:450-455.
82. Maarsingh H, Tio MA, Zaagsma J, Meurs H. Arginase attenuates inhibitory nonadrenergic noncholinergic nerve-induced nitric oxide generation and airway smooth muscle relaxation. Respir Res 2005;6: 23.
83. Hoet PH, Nemery B. Polyamines in the lung: polyamine uptake and polyamine-linked pathological or toxicological conditions. Am J Physiol Lung Cell Mol Physiol 2000;278:L417-L433.
84. Ricciardolo FL, Zaagsma J, Meurs H. The therapeutic potential of drugs targeting the arginase pathway in asthma. Expert Opin Investig Drugs 2005;14:1221-1231.
85. Wu G, Morris SM. Arginine metabolism: nitric oxide and beyond. Biochem J 1998;336:1-17.
86. Hobbs CA, Gilmour SK. High levels of intracellular polyamines promote histone acetyltransferase activity resulting in chromatin hyperacetylation. J Cell Biochem 2000;77:345-360.
87. Bergeron C, Boulet LP, Page N, Laviolette M, Zimmermann N, Rothenberg ME, Hamid Q. Influence of cigarette smoke on the arginine pathway in asthmatic airways: increased expression of arginase I. J Allergy Clin Immunol 2007;119:391-397.
88. Durante W, Liao L, Peyton KJ, Schafer AI. Thrombin stimulates vascular smooth muscle cell polyamine synthesis by inducing cationic amino acid transporter and ornithine decarboxylase gene expression. Circ Res 1998;83:217-223.
89. Durante W, Liao L, Reyna SV, Peyton KJ, Schafer AI. Transforming growth factor-beta(1) stimulates L-arginine transport and metabolism in vascular smooth muscle cells: role in polyamine and collagen synthesis. Circulation 2001;103:1121-1127.
90. Nelin LD, Chicoine LG, Reber KM, English BK, Young TL, Liu Y. Cytokine-induced endothelial arginase expression is dependent on epidermal growth factor receptor. Am J Respir Cell Mol Biol 2005;33: 394-401.
91. Thyberg J, Fredholm BB. Modulation of arterial smooth-muscle cells from contractile to synthetic phenotype requires induction of ornithine decarboxylase activity and polyamine synthesis. Exp Cell Res 1987;170:153-159.
92. Thyberg J, Fredholm BB. Induction of ornithine decarboxylase activity and putrescine synthesis in arterial smooth-muscle cells stimulated with platelet-derived growth-factor. Exp Cell Res 1987;170:160-169.
93. Maarsingh H, Ten Damme A, Joughi FA, Zaagsma J, Meurs H. Role for upregulation and activation of ornithine decarboxylase in platelet-derived growth factor (PDGF)-induced airway smooth muscle hypocontractility. Am J Respir Crit Care Med 2008;177:A488.
94. Maarsingh H, Bos IST, Westerhof-Humblot FJ, Zaagsma J, Meurs H. Increased arginase activity underlies airway hyperresponsiveness in a guinea pig model of chronic allergic asthma. Am J Respir Crit Care Med 2007;175:A522.
95. Kurosawa M, Shimizu Y, Tsukagoshi H, Ueki M. Elevated levels of peripheral-blood, naturally occurring aliphatic polyamines in bronchial asthmatic patients with active symptoms. Allergy 1992;47:638-643.
96. Wei LH, Wu G, Morris SM Jr, Ignarro LJ. Elevated arginase I expression in rat aortic smooth muscle cells increases cell proliferation. Proc Natl Acad Sci USA 2001;98:9260-9264.
97. Bauer PM, Fukuto JM, Buga GM, Pegg AE, Ignarro LJ. Nitric oxide inhibits ornithine decarboxylase by S-nitrosylation. Biochem Biophys Res Commun 1999;262:355-358.
98. Belmonte KE. Cholinergic pathways in the lungs and anticholinergic therapy for chronic obstructive pulmonary disease. Proc Am Thorac Soc 2005;2:297-304.
99. Racke K, Juergens UR, Matthiesen S. Control by cholinergic mechanisms. Eur J Pharmacol 2006;533:57-68.
100. Bos IS, Gosens R, Zuidhof AB, Schaafsma D, Halayko AJ, Meurs H, Zaagsma J. Inhibition of allergen-induced airway remodelling by tiotropium and budesonide: a comparison.Eur Respir J 2007;30:653-661.
101. Gosens R, Bos IS, Zaagsma J, Meurs H. Protective effects of tiotropium bromide in the progression of airway smooth muscle remodeling. Am J Respir Crit Care Med 2005;171:1096-1102.
102. Ohta S, Minoguchi K, Oda N, Chen X, Tanaka A, Tazaki T, Yamamoto Y, Yamamoto M, Watanabe Y, Adachi M. Effects of tiotropium bromide on allergen induced airway remodeling in murine model of chronic asthma. Am J Respir Crit Care Med 2007; 175:A464.
103. Gosens R, Zaagsma J, Grootte BM, Nelemans A, Meurs H. Acetylcholine: a novel regulator of airway smooth muscle remodelling? Eur J Pharmacol 2004;500:193-201.
104. Gosens R, Zaagsma J, Meurs H, Halayko AJ. Muscarinic receptor signaling in the pathophysiology of asthma and COPD. Respir Res 2006;7:73.
105. Myers AC. Transmission in autonomic ganglia. Respir Physiol 2001; 125:99-111.
106. Undem BJ, Myers AC. Cholinergic and noncholinergic parasympathetic control of airway smooth muscle. In: Zaagsma J, Meurs H, Roffel AF, editors. Muscarinic receptors in airways diseases. Basel: Birkhäuser Verlag; 2001. p. 1-24.
107. Spina D, Shah S, Harrison S. Modulation of sensory nerve function in the airways. Trends Pharmacol Sci 1998;19:460-466.
108. Undem BJ, Carr MJ. Pharmacology of airway afferent nerve activity. Respir Res 2001;2:234-244.
109. Allen IC, Hartney JM, Coffman TM, Penn RB, Wess J, Koller BH. Thromboxane A2 induces airway constriction through an M3 muscarinic acetylcholine receptor-dependent mechanism. Am J Physiol Lung Cell Mol Physiol 2006;290:L526-L533.
110. Santing RE, Pasman Y, Olymulder CG, Roffel AF, Meurs H, Zaagsma J. Contribution of a cholinergic reflex mechanism to allergen-induced bronchial hyperreactivity in permanently instrumented, unrestrained guinea-pigs. Br J Pharmacol 1995;114:414-418.
111. Coulson FR, Fryer AD. Muscarinic acetylcholine receptors and airway diseases. Pharmacol Ther 2003;98:59-69.
112. Fryer AD, Jacoby DB. Muscarinic receptors and control of airway smooth muscle. Am J Respir Crit Care Med 1998;158:S154-S160.
113. ten Berge RE, Santing RE, Hamstra JJ, Roffel AF, Zaagsma J. Dysfunction of muscarinic M2 receptors after the early allergic reaction: possible contribution to bronchial hyperresponsiveness in allergic guinea-pigs. Br J Pharmacol 1995;114:881-887.
114. Jacoby DB, Gleich GJ, Fryer AD. Human eosinophil major basic protein is an endogenous allosteric antagonist at the inhibitory muscarinic M2 receptor. J Clin Invest 1993;91:1314-1318.
115. Haag S, Matthiesen S, Juergens UR, Racke K. Muscarinic receptors mediate stimulation of collagen synthesis in human lung fibroblasts. Eur Respir J 2008;32:555-562.
116. Matthiesen S, Bahulayan A, Kempkens S, Haag S, Fuhrmann M, Stichnote C, Juergens UR, Racke K. Muscarinic receptors mediate stimulation of human lung fibroblast proliferation. Am J Respir Cell Mol Biol 2006;35:621-627.
117. Gosens R, Nelemans SA, Grootte Bromhaar MM, McKay S, Zaagsma J, Meurs H. Muscarinic M3-receptors mediate cholinergic synergism of mitogenesis in airway smooth muscle. Am J Respir Cell Mol Biol 2003;28:257-262.
118. Gosens R, Dueck G, Rector E, Nunes RO, Gerthoffer WT, Unruh H, Zaagsma J, Meurs H, Halayko AJ. Cooperative regulation of GSK-3 by muscarinic and PDGF receptors is associated with airway myocyte proliferation. Am J Physiol Lung Cell Mol Physiol 2007;293:L1348-L1358.
119. Krymskaya VP, Orsini MJ, Eszterhas AJ, Brodbeck KC, Benovic JL, Panettieri RA Jr, Penn RB. Mechanisms of proliferation synergy by receptor tyrosine kinase and G protein-coupled receptor activation in human airway smooth muscle. Am J Respir Cell Mol Biol 2000;23: 546-554.
120. Billington CK, Kong KC, Bhattacharyya R, Wedegaertner PB, Panettieri RA Jr, Chan TO, Penn RB. Cooperative regulation of p70S6 kinase by receptor tyrosine kinases and G protein-coupled receptors augments airway smooth muscle growth. Biochemistry 2005;44: 14595-14605.
121. Kong KC, Billington CK, Gandhi U, Panettieri RA Jr, Penn RB. Cooperative mitogenic signaling by G protein-coupled receptors and growth factors is dependent on G(q/11). FASEB J 2006;20: 1558-1560.
122. 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.
123. 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.
124. Halayko AJ, Kartha S, Stelmack GL, McConville J, Tam J, Camoretti-Mercado B, Forsythe SM, Hershenson MB, Solway J. Phophatidylinositol-3 kinase/mammalian target of rapamycin/p70S6K regulates contractile protein accumulation in airway myocyte differentiation. Am J Respir Cell Mol Biol 2004;31:266-275.
125. Nunes RO, Schmidt M, Dueck G, Baarsma H, Halayko AJ, Kerstjens HA, Meurs H, Gosens R. GSK-3/beta-catenin signaling axis in airway smooth muscle: role in mitogenic signaling. Am J Physiol Lung Cell Mol Physiol 2008;294:L1110-L1118.
126. 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.
127. Fairbank NJ, Connolly SC, Mackinnon JD, Wehry K, Deng L, Maksym GN. Airway smooth muscle cell tone amplifies contractile function in the presence of chronic cyclic strain. Am J Physiol Lung Cell Mol Physiol 2008;295:L479-L488.
128. Liu HW, Kassiri K, Voros A, Hiller CT, Wang L, Solway J, Halayko AJ. Gaq-receptor coupled signaling induces RHO-dependent transcription of smooth muscle specific genes in cultured canine airway myocytes. Am J Respir Crit Care Med 2002;165:A670.
129. Hasaneen NA, Zucker S, Cao J, Chiarelli C, Panettieri RA, Foda HD. Cyclic mechanical strain-induced proliferation and migration of human airway smooth muscle cells: role of EMMPRIN and MMPs. FASEB J 2005;19:1507-1509.
130. Tschumperlin DJ, Dai G, Maly IV, Kikuchi T, Laiho LH, McVittie AK, Haley KJ, Lilly CM, So PT, Lauffenburger DA, et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 2004;429:83-86.
131. Tschumperlin DJ, Drazen JM. Chronic effects of mechanical force on airways. Annu Rev Physiol 2006;68:563-583.
132. de Kluijver J, Schrumpf JA, Evertse CE, Sont JK, Roughley PJ, Rabe KF, Hiemstra PS, Mauad T, Sterk PJ. Bronchial matrix and inflammation respond to inhaled steroids despite ongoing allergen exposure in asthma. Clin Exp Allergy 2005;35:1361-1369.
133. Laitinen A, Altraja A, Kampe M, Linden M, Virtanen I, Laitinen LA. Tenascin is increased in airway basement membrane of asthmatics and decreased by an inhaled steroid. Am J Respir Crit Care Med 1997; 156:951-958.
134. Laitinen LA, Laitinen A. Inhaled corticosteroid treatment and extracellular matrix in the airways in asthma. Int Arch Allergy Immunol 1995;107:215-216.
135. Roberts CR, Walker DC, Schellenberg RR. Extracellular matrix. Clin Allergy Immunol 2002;16:143-178.
136. Roche WR, Beasley R, Williams JH, Holgate ST. Subepithelial fibrosis in the bronchi of asthmatics. Lancet 1989;1:520-524.
137. Wilson JW, Li X. The measurement of reticular basement membrane and submucosal collagen in the asthmatic airway. Clin Exp Allergy 1997;27:363-371.
138. Araujo BB, Dolhnikoff M, Silva LF, Elliot J, Lindeman JH, Ferreira DS, Mulder A, Gomes HA, Fernezlian SM, James A, et al. Extracellular matrix components and regulators in the airway smooth muscle in asthma. Eur Respir J 2008;32:61-69.
139. Pini L, Hamid Q, Shannon J, Lemelin L, Olivenstein R, Ernst P, Lemiere C, Martin JG, Ludwig MS. Differences in proteoglycan deposition in the airways of moderate and severe asthmatics. Eur Respir J 2007;29:71-77.
140. Roberts CR, Burke AK. Remodelling of the extracellularmatrix in asthma: proteoglycan synthesis and degradation. Can Respir J 1998;5:48-50.
141. Panettieri RA, Tan EM, Ciocca V, Luttmann MA, Leonard TB, Hay DW. Effects of LTD4 on human airway smooth muscle cell proliferation, matrix expression, and contraction In vitro: differential sensitivity to cysteinyl leukotriene receptor antagonists. Am J Respir Cell Mol Biol 1998;19:453-461.
142. Coutts A, Chen G, Stephens N, Hirst S, Douglas D, Eichholtz T, Khalil N. Release of biologically active TGF-beta from airway smooth muscle cells induces autocrine synthesis of collagen. Am J Physiol Lung Cell Mol Physiol 2001;280:L999-L1008.
143. Johnson PR, Black JL, Carlin S, Ge Q, Underwood PA. The production of extracellular matrix proteins by human passively sensitized airway smooth-muscle cells in culture: the effect of beclomethasone. Am J Respir Crit Care Med 2000;162:2145-2151.
144. Burgess JK, Ceresa C, Johnson SR, Kanabar V, Moir LM, Nguyen TT, Oliver BG, Schuliga M, Ward J. Tissue and matrix influences on airway smooth muscle function. Pulm Pharmacol Ther 2009;5:379-387.
145. Klagas I, Goulet S, Karakiulakis G, Zhong J, Baraket M, Black JL, Papakonstantinou E, Roth M. Decreased hyaluronan in airway smooth muscle cells from patients with asthma and COPD. Eur Respir J 2009;34:616-628.
146. An SS, Bai TR, Bates JH, Black JL, Brown RH, Brusasco V, Chitano P, Deng L, Dowell M, Eidelman DH, et al. Airway smooth muscle dynamics: a common pathway of airway obstruction in asthma. Eur Respir J 2007;29:834-860.
147. Dekkers BG, Schaafsma D, Nelemans SA, Zaagsma J, Meurs H. Extracellular matrix proteins differentially regulate airway smooth muscle phenotype and function. Am J Physiol Lung Cell Mol Physiol 2007;292:L1405-L1413.
148. Fernandes DJ, Bonacci JV, Stewart AG. Extracellular matrix, integrins, and mesenchymal cell function in the airways. Curr Drug Targets 2006;7:567-577.
149. Moir LM, Burgess JK, Black JL. Transforming growth factor beta(1) increases fibronectin deposition through integrin receptor alpha(5)-beta(1) on human airway smooth muscle. J Allergy Clin Immunol 2008;121:1034-1039.
150. Aumailley M, Gerl M, Sonnenberg A, Deutzmann R, Timpl R. Identification of the Arg-Gly-Asp sequence in laminin A chain as a latent cell-binding site being exposed in fragment P1. FEBS Lett 1990;262:82-86.
151. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. Ligand binding to integrins. J Biol Chem 2000;275:21785-21788.
152. Dekkers BG, Bos IS, Gosens R, Halayko AJ, Zaagsma J, Meurs H. Inhibition of airway smooth muscle remodeling in an animal model of chronic asthma by the integrin-blocking peptide RGDS. Am J Respir Crit Care Med 2009;179:A5600.
153. Hirst SJ, Twort CH, Lee TH. Differential effects of extracellular matrix proteins on human airway smooth muscle cell proliferation and phenotype. Am J Respir Cell Mol Biol 2000;23:335-344.
154. Tran T, McNeill KD, Gerthoffer WT, Unruh H, Halayko AJ. Endogenous laminin is required for human airway smooth muscle cell maturation. Respir Res 2006;7:117.
155. Dekkers BG, Schaafsma D, Tran T, Zaagsma J, Meurs H. Insulin-induced laminin expression promotes a hypercontractile airway smooth muscle phenotype. Am J Respir Cell Mol Biol 2009;41:494-504.
156. Tran T, Ens-Blackie K, Rector ES, Stelmack GL, McNeill KD, Tarone G, Gerthoffer WT, Unruh H, Halayko AJ. Laminin-binding Integrin {alpha}7 is Required for Contractile Phenotype Expression by Human Airway Myocyte. Am J Respir Cell Mol Biol 2007;37:668-680.
157. Kanabar V, Karner LC, Simcock DE, Mahn K, Nguyen NM, Cousins DJ, Lavender P, Hirst SJ. Integrin gene profiling in airway smooth muscle from asthmatics. Proc Am Thorac Soc 2007;4:A302.