Prostaglandins but not leukotrienes alter extracellular matrix protein deposition and cytokine release in primary human airway smooth muscle cells and fibroblasts

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 3, 2012, Pages

  Van Ly, David ^a,b   Burgess, Janette K ^a,b   Brock, Thomas G ^c   Lee, Tak H ^d   Black, Judith L ^a,b   Oliver, Brian G G ^a,b  

^a WOOLCOCK INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c Cayman Chemical   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Airway remodeling; Eicosanoids; Fibronectin; Tenascin C

Indexed keywords

FIBRONECTIN; INTERLEUKIN 6; INTERLEUKIN 8; LEUKOTRIENE; PROSTACYCLIN DERIVATIVE; PROSTAGLANDIN; PROSTAGLANDIN D2; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; SCLEROPROTEIN; TENASCIN; TRANSFORMING GROWTH FACTOR BETA;

ADOLESCENT; ADULT; AGED; AIRWAY REMODELING; ARTICLE; ASTHMA; BREATHING MUSCLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BREFELDIN A; BRONCHI; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FIBROBLASTS; FIBRONECTINS; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOTRIENES; MALE; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; PROSTAGLANDINS; PROTEIN SYNTHESIS INHIBITORS; TENASCIN; TRANSFORMING GROWTH FACTOR BETA; YOUNG ADULT;

EID: 84864746505     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00097.2012     Document Type: Article

References (70)

1. Aggarwal S, Moodley YP, Thompson PJ, Misso NL. Prostaglandin E2 and cysteinyl leukotriene concentrations in sputum: association with asthma severity and eosinophilic inflammation. Clin Exp Allergy 40: 85-93, 2010.
2. Altraja S, Kadai M, Rekker E, Altraja A. Synthesis of tenascin and laminin beta2 chain in human bronchial epithelial cells is enhanced by cysteinyl leukotrienes via CysLT1 receptor. Respir Res 9: 44, 2008.
3. Ammit AJ, Hoffman RK, Amrani Y, Lazaar AL, Hay DW, Torphy TJ, Penn RB, Panettieri RA Jr. Tumor necrosis factor-alpha-induced secretion of RANTES and interleukin-6 from human airway smooth-muscle cells. Modulation by cyclic adenosine monophosphate. Am J Respir Cell Mol Biol 23: 794-802, 2000.
4. Ammit AJ, Lazaar AL, Irani C, O'Neill GM, Gordon ND, Amrani Y, Penn RB, Panettieri RA Jr. Tumor necrosis factor-alpha-induced secretion of RANTES and interleukin-6 from human airway smooth muscle cells: modulation by glucocorticoids and beta-agonists. Am J Respir Cell Mol Biol 26: 465-474, 2002.
5. Annoni R, Lancas T, Tanigawa RY, de Medeiros Matsushita M, de Morais Fernezlian S, Bruno A, da Silva LF, Roughley PJ, Battaglia S, Dolhnikoff M, Hiemstra PS, Sterk PJ, Rabe KF, Mauad T. Extracellular matrix composition in chronic obstructive pulmonary disease. Eur Respir J. In press.
6. Araujo VC, Furuse C, Cury PR, Altemani A, Alves VA, de Araujo NS. Tenascin and fibronectin expression in carcinoma ex pleomorphic adenoma. Appl Immunohistochem Mol Morphol 16: 48-53, 2008.
7. Brink C. Leukotriene receptors: state of the art. Adv Exp Med Biol 525: 7-10, 2003.
8. Bucchieri F, Puddicombe SM, Lordan JL, Richter A, Buchanan D, Wilson SJ, Ward J, Zummo G, Howarth PH, Djukanovic R, Holgate ST, Davies DE. Asthmatic bronchial epithelium is more susceptible to oxidant-induced apoptosis. Am J Respir Cell Mol Biol 27: 179-185, 2002.
9. Burgess JK, Ge Q, Poniris MH, Boustany S, Twigg SM, Black JL, Johnson PR. Connective tissue growth factor and vascular endothelial growth factor from airway smooth muscle interact with the extracellular matrix. Am J Physiol Lung Cell Mol Physiol 290: L153-L161, 2006.
10. 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 174: 379-385, 2006.
11. Chang MC, Chang HH, Lee MY, Lin CC, Yeh HW, Yang TT, Lin PS, Tseng WY, Jeng JH. Prostaglandin F(2alpha)-induced interleukin-8 production in human dental pulp cells is associated with MEK/ERK signaling. J Endocrinol 35: 508-512, 2009.
12. Chiba T, Kanda A, Ueki S, Ito W, Kamada Y, Oyamada H, Saito N, Kayaba H, Chihara J. Prostaglandin D2 induces IL-8 and GM-CSF by bronchial epithelial cells in a CRTH2-independent pathway. Int Arch Allergy Immunol 141: 300-307, 2006.
13. Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M. Tenascin interferes with fibronectin action. Cell 53: 383-390, 1988.
14. Clarke DL, Belvisi MG, Smith SJ, Hardaker E, Yacoub MH, Meja KK, Newton R, Slater DM, Giembycz MA. Prostanoid receptor expression by human airway smooth muscle cells and regulation of the secretion of granulocyte colony-stimulating factor. Am J Physiol Lung Cell Mol Physiol 288: L238-L250, 2005.
15. Coleman RA, Smith WL, Narumiya S. International Union of Pharmacology classification of prostanoid receptors: properties, distribution, and structure of the receptors and their subtypes. Pharmacol Rev 46: 205-229, 1994.
16. Davies DE, Wicks J, Powell RM, Puddicombe SM, Holgate ST. Airway remodeling in asthma: new insights. J Allergy Clin Immunol 111: 215-225; quiz 226, 2003.
17. Fiebich BL, Schleicher S, Spleiss O, Czygan M, Hull M. Mechanisms of prostaglandin E2-induced interleukin-6 release in astrocytes: possible involvement of EP4-like receptors, p38 mitogen-activated protein kinase and protein kinase C. J Neurochem 79: 950-958, 2001.
18. Frolich JC. [Prostacyclin in hypertension]. Z Kardiol 81: 303-309, 1992.
19. George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079-1091, 1993.
20. Gloerich M, Bos JL. Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50: 355-375, 2010.
21. Hallstrand TS, Henderson WR Jr. An update on the role of leukotrienes in asthma. Curr Opin Allergy Clin Immunol 10: 60-66, 2010.
22. Hirata E, Arakawa Y, Shirahata M, Yamaguchi M, Kishi Y, Okada T, Takahashi JA, Matsuda M, Hashimoto N. Endogenous tenascin-C enhances glioblastoma invasion with reactive change of surrounding brain tissue. Cancer Sci 100: 1451-1459, 2009.
23. 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 23: 335-344, 2000.
24. Huang SK, Peters-Golden M. Eicosanoid lipid mediators in fibrotic lung diseases: ready for prime time? Chest 133: 1442-1450, 2008.
25. Huang SK, Wettlaufer SH, Chung J, Peters-Golden M. Prostaglandin E2 inhibits specific lung fibroblast functions via selective actions of PKA and Epac-1. Am J Respir Cell Mol Biol 39: 482-489, 2008.
26. Jackson DJ. The role of rhinovirus infections in the development of early childhood asthma. Curr Opin Allergy Clin Immunol 10: 133-138, 2010.
27. Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, Printz MC, Lee WM, Shult PA, Reisdorf E, Carlson-Dakes KT, Salazar LP, DaSilva DF, Tisler CJ, Gern JE, Lemanske RF Jr. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 178: 667-672, 2008.
28. Johnson PR, Armour CL, Carey D, Black JL. Heparin and PGE2 inhibit DNA synthesis in human airway smooth muscle cells in culture. Am J Physiol Lung Cell Mol Physiol 269: L514-L519, 1995.
29. 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 162: 2145-2151, 2000.
30. 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 113: 690-696, 2004.
31. Kang KH, Shim JJ, Banerjee M, Newman JH. PGF2 alpha causes bronchoconstriction and pulmonary vasoconstriction via thromboxane receptors in rat lung. Korean J Intern Med 11: 74-81, 1996.
32. Kohyama T, Liu XD, Wen FQ, Kim HJ, Takizawa H, Rennard SI. Prostaglandin D2 inhibits fibroblast migration. Eur Respir J 19: 684-689, 2002.
33. Kozawa O, Suzuki A, Tokuda H, Kaida T, Uematsu T. Interleukin-6 synthesis induced by prostaglandin E2: cross-talk regulation by protein kinase C. Bone 22: 355-360, 1998.
34. Kranenburg AR, Willems-Widyastuti A, Moori WJ, Sterk PJ, Ala-gappan VK, de Boer WI, Sharma HS. Enhanced bronchial expression of extracellular matrix proteins in chronic obstructive pulmonary disease. Am J Clin Pathol 126: 725-735, 2006.
35. Kuo C, Lim S, King NJ, Bartlett NW, Walton RP, Zhu J, Glanville N, Aniscenko J, Johnston SL, Burgess JK, Black JL, Oliver BG. Rhino-virus infection induces expression of airway remodelling factors in vitro and in vivo. Respirology 16: 367-377, 2011.
36. Kuo C, Lim S, King NJ, Johnston SL, Burgess JK, Black JL, Oliver BG. Rhinovirus infection induces extracellular matrix protein deposition in asthmatic and nonasthmatic airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 300: L951-L957, 2011.
37. Kuwano K, Hashino A, Noda K, Kosugi K, Kuwabara K. A long-acting and highly selective prostacyclin receptor agonist prodrug, 2-4-[(5,6-diphenylpyrazin-2-yl)(isopropylamino butoxy)]-N-(methylsulfony-l)acetamide (NS-304), ameliorates rat pulmonary hypertension with unique relaxant responses of its active form, {4-[(5,6-diphenylpyrazin-2-yl)(isopropyl)amino]butoxy}acetic acid (MRE-269), on rat pulmonary artery. J Pharmacol Exp Ther 326: 691-699, 2008.
38. 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 156: 951-958, 1997.
39. Liu MC, Bleecker ER, Lichtenstein LM, Kagey-Sobotka A, Niv Y, McLemore TL, Permutt S, Proud D, Hubbard WC. Evidence for elevated levels of histamine, prostaglandin D2, and other bronchocon-stricting prostaglandins in the airways of subjects with mild asthma. Am Rev Respir Dis 142: 126-132, 1990.
40. Lofdahl M, Kaarteenaho R, Lappi-Blanco E, Tornling G, Skold MC. Tenascin-C and alpha-smooth muscle actin positive cells are increased in the large airways in patients with COPD. Respir Res 12: 48, 2011.
41. Long JA, Fogel-Petrovic M, Knight DA, Thompson PJ, Upham JW. Higher prostaglandin e2 production by dendritic cells from subjects with asthma compared with normal subjects. Am J Respir Crit Care Med 170: 485-491, 2004.
42. Mackie EJ, Tucker RP. The tenascin-C knockout revisited. J Cell Sci 112: 3847-3853, 1999.
43. Marom B, Rahat MA, Lahat N, Weiss-Cerem L, Kinarty A, Bitter-man H. Native and fragmented fibronectin oppositely modulate monocyte secretion of MMP-9. J Leukoc Biol 81: 1466-1476, 2007.
44. Montuschi P, Kharitonov SA, Ciabattoni G, Barnes PJ. Exhaled leukotrienes and prostaglandins in COPD. Thorax 58: 585-588, 2003.
45. Mosher DF. A role for fibronectin in self-repair after ischemic injury. Nat Med 7: 290-292, 2001.
46. Nowak D, Grimminger F, Jorres R, Oldigs M, Rabe KF, Seeger W, Magnussen H. Increased LTB4 metabolites and PGD2 in BAL fluid after methacholine challenge in asthmatic subjects. Eur Respir J 6: 405-412, 1993.
47. Oga T, Matsuoka T, Yao C, Nonomura K, Kitaoka S, Sakata D, Kita Y, Tanizawa K, Taguchi Y, Chin K, Mishima M, Shimizu T, Naru-miya S. Prostaglandin F(2alpha) receptor signaling facilitates bleomycin-induced pulmonary fibrosis independently of transforming growth factor-beta. Nat Med 15: 1426-1430, 2009.
48. Olman MA. Beyond TGF-beta: a prostaglandin promotes fibrosis. Nat Med 15: 1360-1361, 2009.
49. 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 19: 453-461, 1998.
50. Paron I, Berchtold S, Voros J, Shamarla M, Erkan M, Hofler H, Esposito I. Tenascin-C enhances pancreatic cancer cell growth and motility and affects cell adhesion through activation of the integrin pathway. PLoS One 6: e21684, 2011.
51. Pavord ID, Ward R, Woltmann G, Wardlaw AJ, Sheller JR, Dworski R. Induced sputum eicosanoid concentrations in asthma. Am J Respir Crit Care Med 160: 1905-1909, 1999.
52. Pettipher R, Hansel TT, Armer R. Antagonism of the prostaglandin D2 receptors DP1 and CRTH2 as an approach to treat allergic diseases. Nat Rev Drug Discov 6: 313-325, 2007.
53. Profita M, Sala A, Bonanno A, Riccobono L, Siena L, Melis MR, Di Giorgi R, Mirabella F, Gjomarkaj M, Bonsignore G, Vignola AM. Increased prostaglandin E2 concentrations and cyclooxygenase-2 expression in asthmatic subjects with sputum eosinophilia. J Allergy Clin Immunol 112: 709-716, 2003.
54. Roscioni SS, Maarsingh H, Elzinga CR, Schuur J, Menzen M, Ha-layko AJ, Meurs H, Schmidt M. Epac as a novel effector of airway smooth muscle relaxation. J Cell Mol Med 15: 1551-1563, 2010.
55. Roth M, Soler M, Hornung M, Emmons LR, Stulz P, Perruchoud AP. Cell cultures from cryopreserved human lung tissue. Tissue Cell 24: 455-459, 1992.
56. Ruiz C, Huang W, Hegi ME, Lange K, Hamou MF, Fluri E, Oakeley EJ, Chiquet-Ehrismann R, Orend G. Growth promoting signaling by tenascin-C [corrected]. Cancer Res 64: 7377-7385, 2004.
57. Schafer M, Werner S. Cancer as an overhealing wound: an old hypothesis revisited. Nat Rev Mol Cell Biol 9: 628-638, 2008.
58. Shimbori C, Shiota N, Okunishi H. Effects of montelukast, a cysteinyl-leukotriene type 1 receptor antagonist, on the pathogenesis of bleomycin-induced pulmonary fibrosis in mice. Eur J Pharmacol 650: 424-430, 2011.
59. Siri A, Knauper V, Veirana N, Caocci F, Murphy G, Zardi L. Different susceptibility of small and large human tenascin-C isoforms to degradation by matrix metalloproteinases. J Biol Chem 270: 8650-8654, 1995.
60. Sladek K, Dworski R, Soja J, Sheller JR, Nizankowska E, Oates JA, Szczeklik A. Eicosanoids in bronchoalveolar lavage fluid of aspirin-intolerant patients with asthma after aspirin challenge. Am J Respir Crit Care Med 149: 940-946, 1994.
61. Stebbins KJ, Broadhead AR, Baccei CS, Scott JM, Truong YP, Coate H, Stock NS, Santini AM, Fagan P, Prodanovich P, Bain G, Stearns BA, King CD, Hutchinson JH, Prasit P, Evans JF, Lorrain DS. Pharmacological blockade of the DP2 receptor inhibits cigarette smoke-induced inflammation, mucus cell metaplasia, and epithelial hyperplasia in the mouse lung. J Pharmacol Exp Ther 332: 764-775, 2010.
62. Stratton R, Shiwen X. Role of prostaglandins in fibroblast activation and fibrosis. J Cell Commun Signal 4: 75-77, 2010.
63. Tavakoli S, Cowan MJ, Benfield T, Logun C, Shelhamer JH. Prostaglandin E(2)-induced interleukin-6 release by a human airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol 280: L127-L133, 2001.
64. Tokuda H, Kozawa O, Harada A, Uematsu T. Prostaglandin D2 induces interleukin-6 synthesis via Ca2+ mobilization in osteoblasts: regulation by protein kinase C. Prostaglandins Leukot Essent Fatty Acids 61: 189-194, 1999.
65. Wardlaw AJ, Hay H, Cromwell O, Collins JV, Kay AB. Leukotrienes, LTC4 and LTB4, in bronchoalveolar lavage in bronchial asthma and other respiratory diseases. J Allergy Clin Immunol 84: 19-26, 1989.
66. Whitaker CM, Wei H. An alternate cAMP pathway Epac promotes hippocampal long-term depression. J Physiol 587: 3067-3068, 2009.
67. Yu Y, Chadee K. Prostaglandin E2 stimulates IL-8 gene expression in human colonic epithelial cells by a posttranscriptional mechanism. J Immunol 161: 3746-3752, 1998.
68. Zagzag D, Capo V. Angiogenesis in the central nervous system: a role for vascular endothelial growth factor/vascular permeability factor and tenascin-C. Common molecular effectors in cerebral neoplastic and nonneoplastic "angiogenic diseases". Histol Histopathol 17: 301-321, 2002.
69. Zhong N, Zucker RS. cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J Neurosci 25: 208-214, 2005.
70. Zsila F, Bikadi Z, Lockwood SF. In vitro binding of leukotriene B4 (LTB4) to human serum albumin: evidence from spectroscopic, molecular modeling, and competitive displacement studies. Bioorg Med Chem Lett 15: 3725-3731, 2005.