Epithelium-dependent modulation of responsiveness of airways from caveolin-1 knockout mice is mediated through cyclooxygenase-2 and 5-lipoxygenase

British Journal of Pharmacology

Volumn 167, Issue 3, 2012, Pages 548-560

  Sharma, Pawan ^a,b   Ryu, Min H ^a,b   Basu, Sujata ^a,b   Maltby, Sarah A ^a,b   Yeganeh, Behzad ^a,b   Mutawe, Mark M ^a,b   Mitchell, Richard W ^a,b   Halayko, Andrew J ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Biology of Breathing Group Manitoba Institute of Child Health   (Canada)

Author keywords

5 lipoxygenase; airway smooth muscle; caveolin 1; contraction; PGE2

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; CAVEOLIN 1; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ICOSATETRAENOIC ACID; INDOMETACIN; LEUKOTRIENE; METHACHOLINE; MONTELUKAST; ZILEUTON;

ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; CONTROLLED STUDY; ENZYME BINDING; ENZYME INHIBITION; FEMALE; IMMUNOBLOTTING; IMMUNOHISTOLOGY; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; MOUSE; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SMOOTH MUSCLE CONTRACTILITY; TRACHEA MUSCLE; WILD TYPE;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; ARACHIDONIC ACID; BRONCHIAL HYPERREACTIVITY; BRONCHOCONSTRICTION; CAVEOLIN 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; INDOMETHACIN; METHACHOLINE CHLORIDE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH; TRACHEA;

EID: 84866047129     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02014.x     Document Type: Article

References (64)

1. th Edition. Br J Pharmacol 164 (Suppl. 1): S1-S324.
2. Backlund MG, Mann JR, Dubois RN, (2005). Mechanisms for the prevention of gastrointestinal cancer: the role of prostaglandin E2. Oncology 69 (Suppl 1): 28-32.
3. Barnes PJ, Chung KF, Page CP, (1988). Inflammatory mediators and asthma. Pharmacol Rev 40: 49-84.
4. Chen SF, Liou JY, Huang TY, Lin YS, Yeh AL, Tam K, et al,. (2010a). Caveolin-1 facilitates cyclooxygenase-2 protein degradation. J Cell Biochem 109: 356-362.
5. Chen SH, Fahmi H, Shi Q, Benderdour M, (2010b). Regulation of microsomal prostaglandin E2 synthase-1 and 5-lipoxygenase-activating protein/5-lipoxygenase by 4-hydroxynonenal in human osteoarthritic chondrocytes. Arthritis Res Ther 12: R21.
6. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ, (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299.
7. Chung KF, Barnes PJ, (1999). Cytokines in asthma. Thorax 54: 825-857.
8. Churchill L, Chilton FH, Resau JH, Bascom R, Hubbard WC, Proud D, (1989). Cyclooxygenase metabolism of endogenous arachidonic acid by cultured human tracheal epithelial cells. Am Rev Respir Dis 140: 449-459.
9. Clarke DL, Dakshinamurti S, Larsson AK, Ward JE, Yamasaki A, (2009). Lipid metabolites as regulators of airway smooth muscle function. Pulm Pharmacol Ther 22: 426-435.
10. Cohen AW, Hnasko R, Schubert W, Lisanti MP, (2004). Role of caveolae and caveolins in health and disease. Physiol Rev 84: 1341-1379.
11. 2+) handling. Am J Physiol Lung Cell Mol Physiol 279: L1226-L1235.
12. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, et al,. (2001). Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293: 2449-2452.
13. Duniec ZM, Eling TE, Jetten AM, Gray TE, Nettesheim P, (1989). Arachidonic acid metabolism in normal and transformed rat tracheal epithelial cells and its possible role in the regulation of cell proliferation. Exp Lung Res 15: 391-408.
14. Eling TE, Danilowicz RM, Henke DC, Sivarajah K, Yankaskas JR, Boucher RC, (1986). Arachidonic acid metabolism by canine tracheal epithelial cells. Product formation and relationship to chloride secretion. J Biol Chem 261: 12841-12849.
15. Felley-Bosco E, Bender FC, Courjault-Gautier F, Bron C, Quest AF, (2000). Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc Natl Acad Sci U S A 97: 14334-14339.
16. Felley-Bosco E, Bender F, Quest AF, (2002). Caveolin-1-mediated post-transcriptional regulation of inducible nitric oxide synthase in human colon carcinoma cells. Biol Res 35: 169-176.
17. Fernandes LB, Preuss JM, Paterson JW, Goldie RG, (1990). Epithelium-derived inhibitory factor in human bronchus. Eur J Pharmacol 187: 331-336.
18. Fortner CN, Breyer RM, Paul RJ, (2001). EP2 receptors mediate airway relaxation to substance P, ATP, and PGE2. Am J Physiol Lung Cell Mol Physiol 281: L469-L474.
19. Gavett SH, Madison SL, Chulada PC, Scarborough PE, Qu W, Boyle JE, et al,. (1999). Allergic lung responses are increased in prostaglandin H synthase-deficient mice. J Clin Invest 104: 721-732.
20. Gherghiceanu M, Popescu LM, (2006). Caveolar nanospaces in smooth muscle cells. J Cell Mol Med 10: 519-528.
21. Gosens R, Dueck G, Gerthoffer WT, Unruh H, Zaagsma J, Meurs H, et al,. (2007a). p42/p44 MAP kinase activation is localized to caveolae-free membrane domains in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293: L1163-L1172.
22. Gosens R, Stelmack GL, Dueck G, Mutawe MM, Hinton M, McNeill KD, et al,. (2007b). Caveolae facilitate muscarinic receptor-mediated intracellular Ca2+ mobilization and contraction in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293: L1406-L1418.
23. Gosens R, Stelmack GL, Bos ST, Dueck G, Mutawe MM, Schaafsma D, et al,. (2010). Caveolin-1 is required for contractile phenotype expression by airway smooth muscle cells. J Cell Mol Med 15: 2430-2442.
24. Halayko AJ, Stelmack GL, (2005). The association of caveolae, actin, and the dystrophin-glycoprotein complex: a role in smooth muscle phenotype and function? Can J Physiol Pharmacol 83: 877-891.
25. Halayko AJ, Camoretti-Mercado B, Forsythe SM, Vieira JE, Mitchell RW, Wylam ME, et al,. (1999). Divergent differentiation paths in airway smooth muscle culture: induction of functionally contractile myocytes. Am J Physiol 276 (1 Pt 1): L197-L206.
26. Holtzman MJ, (1992). Arachidonic acid metabolism in airway epithelial cells. Annu Rev Physiol 54: 303-329.
27. Jasmin JF, Mercier I, Hnasko R, Cheung MW, Tanowitz HB, Dupuis J, et al,. (2004). Lung remodeling and pulmonary hypertension after myocardial infarction: pathogenic role of reduced caveolin expression. Cardiovasc Res 63: 747-755.
28. Kamishima T, Burdyga T, Gallagher JA, Quayle JM, (2007). Caveolin-1 and caveolin-3 regulate Ca2+ homeostasis of single smooth muscle cells from rat cerebral resistance arteries. Am J Physiol Heart Circ Physiol 293: H204-H214.
29. Khanapure SP, Garvey DS, Janero DR, Letts LG, (2007). Eicosanoids in inflammation: biosynthesis, pharmacology, and therapeutic frontiers. Curr Top Med Chem 7: 311-340.
30. Kojima F, Naraba H, Miyamoto S, Beppu M, Aoki H, Kawai S, (2004). Membrane-associated prostaglandin E synthase-1 is upregulated by proinflammatory cytokines in chondrocytes from patients with osteoarthritis. Arthritis Res Ther 6: R355-R365.
31. Le Saux CJ, Teeters K, Miyasato SK, Hoffmann PR, Bollt O, Douet V, et al,. (2008). Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J Biol Chem 283: 5760-5768.
32. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, Hansen SH, et al,. (1995). Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270: 15693-15701.
33. Liou JY, Deng WG, Gilroy DW, Shyue SK, Wu KK, (2001). Colocalization and interaction of cyclooxygenase-2 with caveolin-1 in human fibroblasts. J Biol Chem 276: 34975-34982.
34. Lynch KR, O'Neill GP, Liu Q, Im DS, Sawyer N, Metters KM, et al,. (1999). Characterization of the human cysteinyl leukotriene CysLT1 receptor. Nature 399: 789-793.
35. Marnett LJ, (2009). Mechanisms of cyclooxygenase-2 inhibition and cardiovascular side effects: the plot thickens. Cancer Prev Res (Phila) 2: 288-290.
36. Maxis K, Delalandre A, Martel-Pelletier J, Pelletier JP, Duval N, Lajeunesse D, (2006). The shunt from the cyclooxygenase to lipoxygenase pathway in human osteoarthritic subchondral osteoblasts is linked with a variable expression of the 5-lipoxygenase-activating protein. Arthritis Res Ther 8: R181.
37. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
38. Murata T, Lin MI, Huang Y, Yu J, Bauer PM, Giordano FJ, et al,. (2007). Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J Exp Med 204: 2373-2382.
39. Ndukwu IM, Solway J, Arbetter K, Uzendoski K, Leff AR, Mitchell RW, (1994). Immune sensitization augments epithelium-dependent spontaneous tone in guinea pig trachealis. Am J Physiol 266 (5 Pt 1): L485-L492.
40. Okamoto T, Schlegel A, Scherer PE, Lisanti MP, (1998). Caveolins, a family of scaffolding proteins for organizing 'preassembled signaling complexes' at the plasma membrane. J Biol Chem 273: 5419-5422.
41. Park SW, Kim HS, Choi MS, Jeong WJ, Heo DS, Kim KH, et al,. (2010). The effects of the stromal cell-derived cyclooxygenase-2 metabolite PGE2 on proliferation of colon cancer cells. J Pharmacol Exp Ther 336: 516-523.
42. Peebles RS Jr, Hashimoto K, Morrow JD, Dworski R, Collins RD, Hashimoto Y, et al,. (2002). Selective cyclooxygenase-1 and -2 inhibitors each increase allergic inflammation and airway hyperresponsiveness in mice. Am J Respir Crit Care Med 165: 1154-1160.
43. Perrone G, Zagami M, Altomare V, Battista C, Morini S, Rabitti C, (2007). COX-2 localization within plasma membrane caveolae-like structures in human lobular intraepithelial neoplasia of the breast. Virchows Arch 451: 1039-1045.
44. Peters-Golden M, Henderson WR Jr, (2007). Leukotrienes. N Engl J Med 357: 1841-1854.
45. Prakash YS, Thompson MA, Vaa B, Matabdin I, Peterson TE, He T, et al,. (2007). Caveolins and intracellular calcium regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293: L1118-L1126.
46. Raeburn D, Webber SE, (1994). Proinflammatory potential of the airway epithelium in bronchial asthma. Eur Respir J 7: 2226-2233.
47. Rodriguez DA, Tapia JC, Fernandez JG, Torres VA, Munoz N, Galleguillos D, et al,. (2009). Caveolin-1-mediated suppression of cyclooxygenase-2 via a beta-catenin-Tcf/Lef-dependent transcriptional mechanism reduced prostaglandin E2 production and surviving expression. Mol Biol Cell 20: 2297-2310.
48. Ruan YC, Wang Z, Du JY, Zuo WL, Guo JH, Zhang J, et al,. (2008). Regulation of smooth muscle contractility by the epithelium in rat vas deferens: role of ATP-induced release of PGE2. J Physiol 586 (Pt 20): 4843-4857.
49. Ryter SW, Lam HC, Chen ZH, Choi AM, (2011). Deadly triplex: smoke, autophagy, and apoptosis. Autophagy 7: 436-437.
50. Sala A, Folco G, Murphy RC, (2010). Transcellular biosynthesis of eicosanoids. Pharmacol Rep 62: 503-510.
51. Schaafsma D, Gosens R, Bos IS, Meurs H, Zaagsma J, Nelemans SA, (2005). Role of contractile prostaglandins and Rho-kinase in growth factor-induced airway smooth muscle contraction. Respir Res 6: 85.
52. Shakirova Y, Bonnevier J, Albinsson S, Adner M, Rippe B, Broman J, et al,. (2006). Increased Rho activation and PKC-mediated smooth muscle contractility in the absence of caveolin-1. Am J Physiol Cell Physiol 291: C1326-C1335.
53. Sharma P, Tran T, Stelmack GL, McNeill K, Gosens R, Mutawe MM, et al,. (2008). Expression of the dystrophin-glycoprotein complex is a marker for human airway smooth muscle phenotype maturation. Am J Physiol Lung Cell Mol Physiol 294: L57-L68.
54. Sharma P, Ghavami S, Stelmack GL, McNeill KD, Mutawe MM, Klonisch T, et al,. (2010). Beta-dystroglycan binds caveolin-1 in smooth muscle: a functional role in caveolae distribution and Ca2+ release. J Cell Sci 123 (Pt 18): 3061-3070.
55. Simons K, Toomre D, (2000). Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39.
56. Somara S, Gilmont RR, Martens JR, Bitar KN, (2007). Ectopic expression of caveolin-1 restores physiological contractile response of aged colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 293: G240-G249.
57. Stan RV, (2005). Structure of caveolae. Biochim Biophys Acta 1746: 334-348.
58. Taha R, Olivenstein R, Utsumi T, Ernst P, Barnes PJ, Rodger IW, et al,. (2000). Prostaglandin H synthase 2 expression in airway cells from patients with asthma and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 161 (2 Pt 1): 636-640.
59. Torres R, Herrerias A, Serra-Pages M, Roca-Ferrer J, Pujols L, Marco A, et al,. (2008). An intranasal selective antisense oligonucleotide impairs lung cyclooxygenase-2 production and improves inflammation, but worsens airway function, in house dust mite sensitive mice. Respir Res 9: 72.
60. Walls AF, Rhee YK, Gould DJ, Walters C, Robinson C, Church MK, et al,. (1991). Inflammatory mediators and cellular infiltration of the lungs in a guinea pig model of the late asthmatic reaction. Lung 169: 227-240.
61. Wasserman MA, (1988). Modulation of arachidonic acid metabolites as potential therapy of asthma. Agents Actions Suppl 23: 95-111.
62. de Weerd WF, Leeb-Lundberg LM, (1997). Bradykinin sequesters B2 bradykinin receptors and the receptor-coupled Galpha subunits Galphaq and Galphai in caveolae in DDT1 MF-2 smooth muscle cells. J Biol Chem 272: 17858-17866.
63. Wenzel SE, (1997). Arachidonic acid metabolites: mediators of inflammation in asthma. Pharmacotherapy 17 (1 Pt 2): 3S-12S.
64. Xia H, Khalil W, Kahm J, Jessurun J, Kleidon J, Henke CA, (2010). Pathologic caveolin-1 regulation of PTEN in idiopathic pulmonary fibrosis. Am J Pathol 176: 2626-2637.