Caveolin-1 is required for contractile phenotype expression by airway smooth muscle cells

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 11, 2011, Pages 2430-2442

  Gosens, Reinoud ^a,b,c   Stelmack, Gerald L ^a,b   Bos, Sophie T ^c   Dueck, Gordon ^a,b   Mutawe, Mark M ^a,b   Schaafsma, Dedmer ^a,b   Unruh, Helmut ^a   Gerthoffer, William T ^d   Zaagsma, Johan ^c   Meurs, Herman ^c   Halayko, Andrew J ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MANITOBA INSTITUTE OF CHILD HEALTH   (Canada)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Airway remodelling; Asthma; Caveolae; Phenotype plasticity; TGF 1

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CALCIUM BINDING PROTEIN; CALPONIN; CAVEOLIN 1; INITIATION FACTOR 4E; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1;

AIRWAY REMODELING; ANIMAL; ARTICLE; ASTHMA; BIOSYNTHESIS; CAVEOLA; CELL CULTURE; DOG; GENETICS; GUINEA PIG; HUMAN; METABOLISM; MUSCLE CELL; MUSCLE CONTRACTION; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; RESPIRATORY SYSTEM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ACTINS; AIRWAY REMODELING; ANIMALS; ASTHMA; CALCIUM-BINDING PROTEINS; CAVEOLAE; CAVEOLIN 1; CELLS, CULTURED; DOGS; EUKARYOTIC INITIATION FACTOR-4E; GUINEA PIGS; HUMANS; MICROFILAMENT PROTEINS; MUSCLE CELLS; MUSCLE CONTRACTION; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; RESPIRATORY SYSTEM; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

CAVIA; EUKARYOTA;

EID: 80054952112     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01246.x     Document Type: Article

References (67)

1. An SS, Bai TR, Bates JH, et al Airway smooth muscle dynamics: a common pathway of airway obstruction in asthma. Eur Respir J. 2007; 29: 834-60.
2. Halayko AJ, Solway J. Molecular mechanisms of phenotypic plasticity in smooth muscle cells. J Appl Physiol. 2001; 90: 358-68.
3. Halayko AJ, Tran T, Ji SY, et al Airway smooth muscle phenotype and function: interactions with current asthma therapies. Curr Drug Targets. 2006; 7: 525-40.
4. Halayko AJ, Tran T, Gosens R. Phenotype and functional plasticity of airway smooth muscle: role of caveolae and caveolins. Proc Am Thorac Soc. 2008; 5: 80-8.
5. Darby PJ, Kwan CY, Daniel EE. Caveolae from canine airway smooth muscle contain the necessary components for a role in Ca(2+) handling. Am J Physiol Lung Cell Mol Physiol. 2000; 279: L1226-35.
6. Gosens R, Stelmack GL, Dueck G, et al 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: L523-34.
7. Gosens R, Stelmack GL, Dueck G, et al Caveolae facilitate muscarinic receptor-mediated intracellular Ca2+ mobilization and contraction in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L1406-18.
8. Prakash YS, Thompson MA, Vaa B, et al Caveolins and intracellular calcium regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L1118-26.
9. Gosens R, Mutawe M, Martin S, et al Caveolae and caveolins in the respiratory system. Curr Mol Med. 2008; 8: 741-53.
10. Hill MM, Bastiani M, Luetterforst R, et al PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell. 2008; 132: 113-24.
11. Bastiani M, Liu L, Hill MM, et al MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol. 2009; 185: 1259-73.
12. Halayko AJ, Stelmack GL. The association of caveolae, actin, and the dystrophin-glycoprotein complex: a role in smooth muscle phenotype and function Can J Physiol Pharmacol. 2005; 83: 877-91.
13. Sotgia F, Lee JK, Das K, et al Caveolin-3 directly interacts with the C-terminal tail of beta -dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem. 2000; 275: 38048-58.
14. Sharma P, Tran T, Stelmack GL, et al Expression of the dystrophin-glycoprotein complex is a marker for human airway smooth muscle phenotype maturation. Am J Physiol Lung Cell Mol Physiol. 2008; 294: L57-68.
15. Sharma P, Ghavami S, Stelmack GL, et al beta-Dystroglycan binds caveolin-1 in smooth muscle: a functional role in caveolae distribution and Ca2+ release. J Cell Sci. 2010; 123: 3061-70.
16. Couet J, Sargiacomo M, Lisanti MP. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem. 1997; 272: 30429-38.
17. Liu P, Ying Y, Ko YG, et al Localization of platelet-derived growth factor-stimulated phosphorylation cascade to caveolae. J Biol Chem. 1996; 271: 10299-303.
18. Rothberg KG, Heuser JE, Donzell WC, et al Caveolin, a protein component of caveolae membrane coats. Cell. 1992; 68: 673-82.
19. Yamamoto M, Toya Y, Jensen RA, et al Caveolin is an inhibitor of platelet-derived growth factor receptor signaling. Exp Cell Res. 1999; 247: 380-8.
20. Gosens R, Dueck G, Gerthoffer WT, et al p42/p44 MAP kinase activation is localized to caveolae-free membrane domains in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol. 2007; 292: L1163-72.
21. Daniel EE, El-Yazbi A, Cho WJ. Caveolae and calcium handling, a review and a hypothesis. J Cell Mol Med. 2006; 10: 529-44.
22. Daniel EE, Eteraf T, Sommer B, et al The role of caveolae and caveolin 1 in calcium handling in pacing and contraction of mouse intestine. J Cell Mol Med. 2009; 13: 352-64.
23. Drab M, Verkade P, Elger M, et al Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 2001; 293: 2449-52.
24. Dreja K, Voldstedlund M, Vinten J, et al Cholesterol depletion disrupts caveolae and differentially impairs agonist-induced arterial contraction. Arterioscler Thromb Vasc Biol. 2002; 22: 1267-72.
25. Je HD, Gallant C, Leavis PC, et al Caveolin-1 regulates contractility in differentiated vascular smooth muscle. Am J Physiol Heart Circ Physiol. 2004; 286: H91-8.
26. Shakirova Y, Mori M, Ekman M, et al Human urinary bladder smooth muscle is dependent on membrane cholesterol for cholinergic activation. Eur J Pharmacol. 2010; 634: 142-8.
27. Schlenz H, Kummer W, Jositsch G, et al Muscarinic receptor-mediated bronchoconstriction is coupled to caveolae in murine airways. Am J Physiol Lung Cell Mol Physiol. 2009; doi:.
28. Sommer B, Montano LM, Carbajal V, et al Extraction of membrane cholesterol disrupts caveolae and impairs serotonergic (5-HT2A) and histaminergic (H1) responses in bovine airway smooth muscle: role of Rho-kinase. Can J Physiol Pharmacol. 2009; 87: 180-95.
29. Benayoun L, Druilhe A, Dombret MC, et al Airway structural alterations selectively associated with severe asthma. Am J Respir Crit Care Med. 2003; 167: 1360-8.
30. Ma X, Cheng Z, Kong H, et al Changes in biophysical and biochemical properties of single bronchial smooth muscle cells from asthmatic subjects. Am J Physiol Lung Cell Mol Physiol. 2002; 283: L1181-9.
31. Dekkers BG, Maarsingh H, Meurs H, et al Airway structural components drive airway smooth muscle remodeling in asthma. Proc Am Thorac Soc. 2009; 6: 683-92.
32. Leguillette R, Laviolette M, Bergeron C, et al Myosin, transgelin, and myosin light chain kinase: expression and function in asthma. Am J Respir Crit Care Med. 2008; 179: 194-204.
33. Woodruff PG, Dolganov GM, Ferrando RE, et al 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: 1001-6.
34. Halayko AJ, Rector E, Stephens NL. Airway smooth muscle cell proliferation: characterization of subpopulations by sensitivity to heparin inhibition. Am J Physiol. 1998; 274: L17-25.
35. Halayko AJ, Stelmack GL, Yamasaki A, et al Distribution of phenotypically disparate myocyte subpopulations in airway smooth muscle. Can J Physiol Pharmacol. 2005; 83: 104-16.
36. Halayko AJ, Camoretti-Mercado B, Forsythe SM, et al Divergent differentiation paths in airway smooth muscle culture: induction of functionally contractile myocytes. Am J Physiol. 1999; 276: L197-206.
37. Halayko AJ, Kartha S, Stelmack GL, et al Phophatidylinositol-3 kinase/mammalian target of rapamycin/p70S6K regulates contractile protein accumulation in airway myocyte differentiation. Am J Respir Cell Mol Biol. 2004; 31: 266-75.
38. Tran T, Ens-Blackie K, Rector ES, et al Laminin-binding integrin {alpha}7 is required for contractile phenotype expression by human airway myocyte. Am J Respir Cell Mol Biol. 2007; 37: 668-80.
39. Ghavami S, Mutawe MM, Hauff K, et al Statin-triggered cell death in primary human lung mesenchymal cells involves p53-PUMA and release of Smac and Omi but not cytochrome c. Biochim Biophys Acta. 2010; 1803: 452-67.
40. Tran J, Kung SK. Lentiviral vectors mediate stable and efficient gene delivery into primary murine natural killer cells. Mol Ther. 2007; 15: 1331-9.
41. Meurs H, Santing RE, Remie R, et al A guinea pig model of acute and chronic asthma using permanently instrumented and unrestrained animals. Nat Protoc. 2006; 1: 840-7.
42. Bos IS, Gosens R, Zuidhof AB, et al Inhibition of allergen-induced airway remodelling by tiotropium and budesonide: a comparison. Eur Respir J. 2007; 30: 653-61.
43. Gosens R, Bos IS, Zaagsma J, et al Protective effects of tiotropium bromide in the progression of airway smooth muscle remodeling. Am J Respir Crit Care Med. 2005; 171: 1096-102.
44. Halayko AJ, Salari H, Ma X, et al Markers of airway smooth muscle cell phenotype. Am J Physiol. 1996; 270: L1040-51.
45. Goldsmith AM, Bentley JK, Zhou L, et al Transforming growth factor-beta induces airway smooth muscle hypertrophy. Am J Respir Cell Mol Biol. 2006; 34: 247-54.
46. Gawaziuk JP, X, Sheikh F, et al Transforming growth factor-beta as a differentiating factor for cultured smooth muscle cells. Eur Respir J. 2007; 30: 643-52.
47. Zhou L, Li J, Goldsmith AM, et al Human bronchial smooth muscle cell lines show a hypertrophic phenotype typical of severe asthma. Am J Respir Crit Care Med. 2004; 169: 703-11.
48. Zhou L, Goldsmith AM, Bentley JK, et al 4E-binding protein phosphorylation and eukaryotic initiation factor-4E release are required for airway smooth muscle hypertrophy. Am J Respir Cell Mol Biol. 2005; 33: 195-202.
49. Thyberg J, Roy J, Tran PK, et al Expression of caveolae on the surface of rat arterial smooth muscle cells is dependent on the phenotypic state of the cells. Lab Invest. 1997; 77: 93-101.
50. Thyberg J. Differences in caveolae dynamics in vascular smooth muscle cells of different phenotypes. Lab Invest. 2000; 80: 915-29.
51. Isshiki M, Anderson RG. Function of caveolae in Ca2+ entry and Ca2+-dependent signal transduction. Traffic. 2003; 4: 717-23.
52. Gherghiceanu M, Popescu LM. Caveolar nanospaces in smooth muscle cells. J Cell Mol Med. 2006; 10: 519-28.
53. Popescu LM, Gherghiceanu M, Mandache E, et al Caveolae in smooth muscles: nanocontacts. J Cell Mol Med. 2006; 10: 960-90.
54. Peterson TE, Guicciardi ME, Gulati R, et al Caveolin-1 can regulate vascular smooth muscle cell fate by switching platelet-derived growth factor signaling from a proliferative to an apoptotic pathway. Arterioscler Thromb Vasc Biol. 2003; 23: 1521-7.
55. Razani B, Zhang XL, Bitzer M, et al Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem. 2001; 276: 6727-38.
56. Le Saux CJ, Teeters K, Miyasato SK, et al Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J Biol Chem. 2008; 283: 5760-8.
57. Kim S, Lee Y, Seo JE, et al Caveolin-1 increases basal and TGF-beta1-induced expression of type I procollagen through PI-3 kinase/Akt/mTOR pathway in human dermal fibroblasts. Cell Signal. 2008; 20: 1313-9.
58. Peng F, Zhang B, Wu D, et al TGF{beta}-Induced RhoA Activation and Fibronectin Production in Mesangial Cells Requires Caveolae. Am J Physiol Renal Physiol. 2008; 295: F153-64.
59. Wang XM, Zhang Y, Kim HP, et al Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med. 2006; 203: 2895-906.
60. Achcar RO, Demura Y, Rai PR, et al Loss of caveolin and heme oxygenase expression in severe pulmonary hypertension. Chest. 2006; 129: 696-705.
61. Patel HH, Zhang S, Murray F, et al Increased smooth muscle cell expression of caveolin-1 and caveolae contribute to the pathophysiology of idiopathic pulmonary arterial hypertension. FASEB J. 2007; 21: 2970-9.
62. Hogg JC, Chu F, Utokaparch S, et al The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004; 350: 2645-53.
63. Jeffery PK. Remodeling and inflammation of bronchi in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2004; 1: 176-83.
64. Jiang H, Rao K, Halayko AJ, et al Ragweed sensitization-induced increase of myosin light chain kinase content in canine airway smooth muscle. Am J Respir Cell Mol Biol. 1992; 7: 567-73.
65. Jiang H, Rao K, Liu X, et al Increased Ca2+ and myosin phosphorylation, but not calmodulin activity in sensitized airway smooth muscles. Am J Physiol. 1995; 268: L739-46.
66. Opazo Saez AM, Seow CY, Pare PD. Peripheral airway smooth muscle mechanics in obstructive airways disease. Am J Respir Crit Care Med. 2000; 161: 910-7.
67. Trian T, Benard G, Begueret H, et al Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med. 2007; 204: 3173-81.