Cross-talk between transforming growth factor-β1 and muscarinic M 2 receptors augments airway smooth muscle proliferation

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 1, 2013, Pages 18-27

  Oenema, Tjitske A ^a   Mensink, Gerrianne ^a   Smedinga, Lyanne ^a   Halayko, Andrew J ^b   Zaagsma, Johan ^a   Meurs, Herman ^a   Gosens, Reinoud ^a   Dekkers, Bart G J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Airway smooth muscle cell proliferation; Collagen Type I; Fibronectin; Muscarinic receptor; TGF 1

Indexed keywords

ARGINYLGLYCYLASPARTYLSERINE; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA 1; DAU 5884; FIBRONECTIN; GALLAMINE; MESSENGER RNA; METHACHOLINE; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR ANTAGONIST; PERTUSSIS TOXIN; PLATELET DERIVED GROWTH FACTOR; RNA 18S; SCLEROPROTEIN; TIOTROPIUM BROMIDE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

AIRWAY REMODELING; AIRWAY SMOOTH MUSCLE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CHOLINERGIC STIMULATION; CONTROLLED STUDY; DRUG EFFECT; DRUG RECEPTOR BINDING; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MITOGENESIS; MOLECULAR INTERACTION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

CELL LINE, TRANSFORMED; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; DNA REPLICATION; DRUG SYNERGISM; EXTRACELLULAR MATRIX; FIBRONECTINS; GALLAMINE TRIETHIODIDE; HUMANS; INTEGRIN ALPHA5BETA1; METHACHOLINE CHLORIDE; MITOGENS; MYOCYTES, SMOOTH MUSCLE; OLIGOPEPTIDES; PERTUSSIS TOXIN; RECEPTOR CROSS-TALK; RECEPTOR, MUSCARINIC M2; RESPIRATORY SYSTEM; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84883190789     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0261OC     Document Type: Article

References (62)

1. Wendt MK, Allington TM, Schiemann WP. Mechanisms of the epithelial-mesenchymal transition by TGF-beta. Future Oncol 2009;5:1145-1168.
2. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008;1782:197-228.
3. Baarsma HA, Menzen MH, Halayko AJ, Meurs H, Kerstjens HA, Gosens R. Beta-catenin signaling is required for TGF-beta1-induced extracellular matrix production by airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2011;301:L956-L965.
4. 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.
5. Ichimaru Y, Krimmer DI, Burgess JK, Black JL, Oliver BG. TGF-{beta} enhances deposition of perlecan from COPD airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2011;302:L325-L333.
6. Ruiz-Ortega M, Rodriguez-Vita J, Sanchez-Lopez E, Carvajal G, Egido J. TGF-beta signaling in vascular fibrosis. Cardiovasc Res 2007;74:196-206.
7. Bunni MA, Kramarenko II, Walker L, Raymond JR, Garnovskaya MN. Role of integrins in angiotensin II-induced proliferation of vascular smooth muscle cells. Am J Physiol Cell Physiol 2011;300:C647-C656.
8. 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.
9. Dekkers BG, Bos IS, Gosens R, Halayko AJ, Zaagsma J, Meurs H. The integrin-blocking peptide RGDS inhibits airway smooth muscle remodeling in a guinea pig model of allergic asthma.AmJ RespirCrit CareMed 2010;181:556-565.
10. Dekkers BG, Bos IS, Zaagsma J, Meurs H. Functional consequences of human airway smooth muscle phenotype plasticity. Br J Pharmacol 2011;166:359-367.
11. 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.
12. Roy J, Tran PK, Religa P, Kazi M, Henderson B, Lundmark K, Hedin U. Fibronectin promotes cell cycle entry in smooth muscle cells in primary culture. Exp Cell Res 2002;273:169-177.
13. Hedin UL, Daum G, Clowes AW. Disruption of integrin alpha 5 beta 1 signaling does not impair PDGF-BB-mediated stimulation of the extracellular signal-regulated kinase pathway in smooth muscle cells. J Cell Physiol 1997;172:109-116.
14. Moir LM, Johnson PR, Burgess JK, Black JL. Integrins mediate asthmatic airway smooth muscle cell proliferation. Presented at the Thoracic Society of Australia and New Zealand 2005 Annual Conference Meeting, March 18-23, 2005, Perth, Australia.
15. Nguyen TT, Ward JP, Hirst SJ. Beta1-integrins mediate enhancement of airway smooth muscle proliferation by collagen and fibronectin. Am J Respir Crit Care Med 2005;171:217-223.
16. Bottoms SE, Howell JE, Reinhardt AK, Evans IC, McAnulty RJ. TGFbeta isoform specific regulation of airway inflammation and remodelling in a murine model of asthma. PLoS ONE 2010;5:e9674.
17. Lee CG, Cho SJ, Kang MJ, Chapoval SP, Lee PJ, Noble PW, Yehualaeshet T, Lu B, Flavell RA, Milbrandt J, et al. Early growth response gene 1-mediated apoptosis is essential for transforming growth factor beta1-induced pulmonary fibrosis. J Exp Med 2004;200: 377-389.
18. Lee CG, Kang HR, Homer RJ, Chupp G, Elias JA. Transgenic modeling of transforming growth factor-beta(1): role of apoptosis in fibrosis and alveolar remodeling. Proc Am Thorac Soc 2006;3:418-423.
19. Black PN, Young PG, Skinner SJ. Response of airway smooth muscle cells to TGF-beta 1: effects on growth and synthesis of glycosaminoglycans. Am J Physiol 1996;271:L910-L917.
20. 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.
21. Michaeloudes C, Sukkar MB, Khorasani NM, Bhavsar PK, Chung KF. TGF-beta regulates Nox4, MnSOD and catalase expression, and IL-6 release in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2011;300:L295-L304.
22. Shin JH, Shim JW, Kim DS, Shim JY. TGF-beta effects on airway smooth muscle cell proliferation, VEGF release and signal transduction pathways. Respirology 2009;14:347-353.
23. Xie S, Sukkar MB, Issa R, Khorasani NM, Chung KF. Mechanisms of induction of airway smooth muscle hyperplasia by transforming growth factor-beta. Am J Physiol Lung Cell Mol Physiol 2007;293: L245-L253.
24. Grando SA, Kawashima K, Kirkpatrick CJ, Wessler I. Recent progress in understanding the non-neuronal cholinergic system in humans. Life Sci 2007;80:2181-2185.
25. Wessler I, Kirkpatrick CJ. Acetylcholine beyond neurons: the nonneuronal cholinergic system in humans. Br J Pharmacol 2008;154: 1558-1571.
26. 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.
27. 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.
28. 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.
29. Dekkers BG, Maarsingh H, Meurs H, Gosens R. Airway structural components drive airway smooth muscle remodeling in asthma. Proc Am Thorac Soc 2009;6:683-692.
30. Bos IST, 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.
31. 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.
32. Ohta S, Oda N, Yokoe T, Tanaka A, Yamamoto Y, Watanabe Y, Minoguchi K, Ohnishi T, Hirose T, Nagase H, et al. Effect of tiotropium bromide on airway inflammation and remodelling in a mouse model of asthma. Clin Exp Allergy 2010;40:1266-1275.
33. Pera T, Zuidhof A, Valadas J, Smit M, Schoemaker RG, Gosens R, Maarsingh H, Zaagsma J, Meurs H. Tiotropium inhibits pulmonary inflammation and remodelling in a guinea pig model of COPD. Eur Respir J 2011;38:789-796.
34. 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.
35. 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.
36. Gosens R, Stelmack GL, Dueck G, McNeill KD, Yamasaki A, Gerthoffer WT, Unruh H, Gounni AS, Zaagsma J, Halayko AJ. Role of caveolin-1 in p42/p44 MAP kinase activation and proliferation of human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2006;291:L523-L534.
37. Oenema TA, Kolahian S, Nanninga JE, Rieks D, Hiemstra PS, Zuyderduyn S, Halayko AJ, Meurs H, Gosens R. Pro-inflammatory mechanisms of muscarinic receptor stimulation in airway smooth muscle. Respir Res 2010;11:130.
38. Oenema TA, Smit M, Smedinga L, Racke K, Halayko AJ, Meurs H, Gosens R. Muscarinic receptor stimulation augments TGF-beta1-induced contractile protein expression by airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2012;303:L589-L597.
39. 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.
40. Ikushima H, Miyazono K. TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 2010;10:415-424.
41. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010;141:1117-1134.
42. Gosens R, Rieks D, Meurs H, Ninaber DK, Rabe KF, Nanninga J, Kolahian S, Halayko AJ, Hiemstra PS, Zuyderduyn S. Muscarinic M3 receptor stimulation increases cigarette smoke-induced IL-8 secretion by human airway smooth muscle cells. Eur Respir J 2009;34:1436-1443.
43. Roffel AF, Elzinga CR, Zaagsma J. Muscarinic M3 receptors mediate contraction of human central and peripheral airway smooth muscle. Pulm Pharmacol 1990;3:47-51.
44. Roffel AF, Meurs H, Elzinga CR, Zaagsma J. Characterization of the muscarinic receptor subtype involved in phosphoinositide metabolism in bovine tracheal smooth muscle. Br J Pharmacol 1990;99:293-296.
45. Roffel AF, Elzinga CR, Van Amsterdam RG, de Zeeuw RA, Zaagsma J. Muscarinic M2 receptors in bovine tracheal smooth muscle: discrepancies between binding and function. Eur J Pharmacol 1988;153: 73-82.
46. 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.
47. Gosens R, Baarsma HA, Heijink IH, Oenema TA, Halayko AJ, Meurs H, Schmidt M. De novo synthesis of {beta}-catenin via H-Ras and MEK regulates airway smooth muscle growth. FASEB J 2010;24:757-768.
48. Gawaziuk JPX, Sheikh F, Cheng ZQ, Cattini PA, Stephens NL. Transforming growth factor-beta as a differentiating factor for cultured smooth muscle cells. Eur Respir J 2007;30:643-652.
49. McMillan SJ, Xanthou G, Lloyd CM. Manipulation of allergen-induced airway remodeling by treatment with anti-TGF-beta antibody: effect on the SMAD signaling pathway. J Immunol 2005;174:5774-5780.
50. Kang HR, Cho SJ, Lee CG, Homer RJ, Elias JA. Transforming growth factor (TGF)-beta1 stimulates pulmonary fibrosis and inflammation via a BAX-dependent, BID-activated pathway that involves matrix metalloproteinase-12. J Biol Chem 2007;282:7723-7732.
51. Stouffer GA, Owens GK. TGF-beta promotes proliferation of cultured SMC via both PDGF-AA-dependent and PDGF-AA-independent mechanisms. J Clin Invest 1994;93:2048-2055.
52. 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.
53. Milara J, Serrano A, Peiro T, Gavalda A, Miralpeix M, Morcillo EJ, Cortijo J. Aclidinium inhibits human lung fibroblast to myofibroblast transition. Thorax 2012;67:229-237.
54. 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.
55. 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.
56. Cockcroft DW, Davis BE. Mechanisms of airway hyperresponsiveness. J Allergy Clin Immunol 2006;118:551-559.
57. Meurs H, Gosens R, Zaagsma J. Airway hyperresponsiveness in asthma: lessons from in vitro model systems and animal models. Eur Respir J 2008;32:487-502.
58. 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.
59. Grainge CL, Lau LC, Ward JA, Dulay V, Lahiff G, Wilson S, Holgate S, Davies DE, Howarth PH. Effect of bronchoconstriction on airway remodeling in asthma. N Engl J Med 2011;364:2006-2015.
60. Boulet LP, Laviolette M, Turcotte H, Cartier A, Dugas M, Malo JL, Boutet M. Bronchial subepithelial fibrosis correlates with airway responsiveness to methacholine. Chest 1997;112:45-52.
61. Slats AM, Janssen K, van Schadewijk 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.
62. Tatler AL, John AE, Jolly L, Habgood A, Porte J, Brightling C, Knox AJ, Pang L, Sheppard D, Huang X, et al. Integrin {alpha}v{beta}5-mediated TGF-{beta} activation by airway smooth muscle cells in asthma. J Immunol 2011;187:6094-6107.