Oncostatin M (OSM) primes IL-13- and IL-4-induced eotaxin responses in fibroblasts: Regulation of the type-II IL-4 receptor chains IL-4Rα and IL-13Rα1

Experimental Cell Research

Volumn 315, Issue 20, 2009, Pages 3486-3499

  Fritz, Dominik K ^a   Kerr, Christine ^a   Botelho, Fernando ^a   Stampfli, Martin ^a   Richards, Carl D ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Eotaxin 1; Fibroblasts; IL 13R 1; IL 4R ; Oncostatin M

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; EOTAXIN; GLYCOPROTEIN GP 130; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 6; ONCOSTATIN M; PHOSPHATIDYLINOSITOL 3 KINASE; STAT6 PROTEIN;

ANIMAL CELL; ARTICLE; ATOPY; CELL STRAIN 3T3; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; INFLAMMATION; LEUKOCYTE MIGRATION; LUNG FIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

EID: 70449532042     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.09.024     Document Type: Article

References (74)

1. Boulay J.L., and Paul W.E. Hematopoietin sub-family classification based on size, gene organization and sequence homology. Curr. Biol. 3 (1993) 573-581
2. Punnonen J., Aversa G., Cocks B.G., McKenzie A.N., Menon S., Zurawski G., de Waal Malefyt R., and de Vries J.E. Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 3730-3734
3. Batra V., Musani A.I., Hastie A.T., Khurana S., Carpenter K.A., Zangrilli J.G., and Peters S.P. Bronchoalveolar lavage fluid concentrations of transforming growth factor (TGF)-beta1, TGF-beta2, interleukin (IL)-4 and IL-13 after segmental allergen challenge and their effects on alpha-smooth muscle actin and collagen III synthesis by primary human lung fibroblasts. Clin. Exp. Allergy 34 (2004) 437-444
4. Lilly C.M., Nakamura H., Belostotsky O.I., Haley K.J., Garcia-Zepeda E.A., Luster A.D., and Israel E. Eotaxin expression after segmental allergen challenge in subjects with atopic asthma. Am. J. Respir. Crit. Care Med. 163 (2001) 1669-1675
5. Matsukura S., Stellato C., Georas S.N., Casolaro V., Plitt J.R., Miura K., Kurosawa S., Schindler U., and Schleimer R.P. Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 24 (2001) 755-761
6. Peng Q., Matsuda T., and Hirst S.J. Signaling pathways regulating interleukin-13-stimulated chemokine release from airway smooth muscle. Am. J. Respir. Crit. Care Med. 169 (2004) 596-603
7. Hoeck J., and Woisetschlager M. STAT6 mediates eotaxin-1 expression in IL-4 or TNF-alpha-induced fibroblasts. J. Immunol. 166 (2001) 4507-4515
8. Matsukura S., Stellato C., Plitt J.R., Bickel C., Miura K., Georas S.N., Casolaro V., and Schleimer R.P. Activation of eotaxin gene transcription by NF-kappa B and STAT6 in human airway epithelial cells. J. Immunol. 163 (1999) 6876-6883
9. Jose P.J., Griffiths-Johnson D.A., Collins P.D., Walsh D.T., Moqbel R., Totty N.F., Truong O., Hsuan J.J., and Williams T.J. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J. Exp. Med. 179 (1994) 881-887
10. Griffiths-Johnson D.A., Collins P.D., Rossi A.G., Jose P.J., and Williams T.J. The chemokine, eotaxin, activates guinea-pig eosinophils in vitro and causes their accumulation into the lung in vivo. Biochem. Biophys. Res. Commun. 197 (1993) 1167-1172
11. Rothenberg M.E., MacLean J.A., Pearlman E., Luster A.D., and Leder P. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J. Exp. Med. 185 (1997) 785-790
12. Nakamura H., Weiss S.T., Israel E., Luster A.D., Drazen J.M., and Lilly C.M. Eotaxin and impaired lung function in asthma. Am. J. Respir. Crit. Care Med. 160 (1999) 1952-1956
13. Lamkhioued B., Renzi P.M., Abi-Younes S., Garcia-Zepada E.A., Allakhverdi Z., Ghaffar O., Rothenberg M.D., Luster A.D., and Hamid Q. Increased expression of eotaxin in bronchoalveolar lavage and airways of asthmatics contributes to the chemotaxis of eosinophils to the site of inflammation. J. Immunol. 159 (1997) 4593-4601
14. Mattoli S., Stacey M.A., Sun G., Bellini A., and Marini M. Eotaxin expression and eosinophilic inflammation in asthma. Biochem. Biophys. Res. Commun. 236 (1997) 299-301
15. Ying S., Robinson D.S., Meng Q., Rottman J., Kennedy R., Ringler D.J., Mackay C.R., Daugherty B.L., Springer M.S., Durham S.R., Williams T.J., and Kay A.B. Enhanced expression of eotaxin and CCR3 mRNA and protein in atopic asthma. Association with airway hyperresponsiveness and predominant co-localization of eotaxin mRNA to bronchial epithelial and endothelial cells. Eur. J. Immunol. 27 (1997) 3507-3516
16. Zurawski S.M., Chomarat P., Djossou O., Bidaud C., McKenzie A.N., Miossec P., Banchereau J., and Zurawski G. The primary binding subunit of the human interleukin-4 receptor is also a component of the interleukin-13 receptor. J. Biol. Chem. 270 (1995) 13869-13878
17. Idzerda R.L., March C.J., Mosley B., Lyman S.D., Vanden Bos T., Gimpel S.D., Din W.S., Grabstein K.H., Widmer M.B., Park L.S., et al. Human interleukin 4 receptor confers biological responsiveness and defines a novel receptor superfamily. J. Exp. Med. 171 (1990) 861-873
18. Mosley B., Beckmann M.P., March C.J., Idzerda R.L., Gimpel S.D., VandenBos T., Friend D., Alpert A., Anderson D., Jackson J., et al. The murine interleukin-4 receptor: molecular cloning and characterization of secreted and membrane bound forms. Cell 59 (1989) 335-348
19. Vita N., Lefort S., Laurent P., Caput D., and Ferrara P. Characterization and comparison of the interleukin 13 receptor with the interleukin 4 receptor on several cell types. J. Biol. Chem. 270 (1995) 3512-3517
20. Hilton D.J., Zhang J.G., Metcalf D., Alexander W.S., Nicola N.A., and Willson T.A. Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 497-501
21. Aman M.J., Tayebi N., Obiri N.I., Puri R.K., Modi W.S., and Leonard W.J. cDNA cloning and characterization of the human interleukin 13 receptor alpha chain. J. Biol. Chem. 271 (1996) 29265-29270
22. Murata T., Taguchi J., and Puri R.K. Interleukin-13 receptor alpha' but not alpha chain: a functional component of interleukin-4 receptors. Blood 91 (1998) 3884-3891
23. Kondo M., Takeshita T., Ishii N., Nakamura M., Watanabe S., Arai K., and Sugamura K. Sharing of the interleukin-2 (IL-2) receptor gamma chain between receptors for IL-2 and IL-4. Science 262 (1993) 1874-1877
24. Russell S.M., Keegan A.D., Harada N., Nakamura Y., Noguchi M., Leland P., Friedmann M.C., Miyajima A., Puri R.K., Paul W.E., et al. Interleukin-2 receptor gamma chain: a functional component of the interleukin-4 receptor. Science 262 (1993) 1880-1883
25. Pernis A., Witthuhn B., Keegan A.D., Nelms K., Garfein E., Ihle J.N., Paul W.E., Pierce J.H., and Rothman P. Interleukin 4 signals through two related pathways. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7971-7975
26. Kotanides H., and Reich N.C. Interleukin-4-induced STAT6 recognizes and activates a target site in the promoter of the interleukin-4 receptor gene. J. Biol. Chem. 271 (1996) 25555-25561
27. Kuperman D., Schofield B., Wills-Karp M., and Grusby M.J. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187 (1998) 939-948
28. Akimoto T., Numata F., Tamura M., Takata Y., Higashida N., Takashi T., Takeda K., and Akira S. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187 (1998) 1537-1542
29. Tomkinson A., Kanehiro A., Rabinovitch N., Joetham A., Cieslewicz G., and Gelfand E.W. The failure of STAT6-deficient mice to develop airway eosinophilia and airway hyperresponsiveness is overcome by interleukin-5. Am. J. Respir. Crit. Care Med. 160 (1999) 1283-1291
30. Yang M., Hogan S.P., Henry P.J., Matthaei K.I., McKenzie A.N., Young I.G., Rothenberg M.E., and Foster P.S. Interleukin-13 mediates airways hyperreactivity through the IL-4 receptor-alpha chain and STAT-6 independently of IL-5 and eotaxin. Am. J. Respir. Cell Mol. Biol. 25 (2001) 522-530
31. Taga T., and Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15 (1997) 797-819
32. Ichihara M., Hara T., Kim H., Murate T., and Miyajima A. Oncostatin M and leukemia inhibitory factor do not use the same functional receptor in mice. Blood 90 (1997) 165-173
33. Gomez-Lechon M.J. Oncostatin M: signal transduction and biological activity. Life Sci. 65 (1999) 2019-2030
34. Fritz D.K., Kerr C., Tong L., Smyth D., and Richards C.D. Oncostatin-M up-regulates VCAM-1 and synergizes with IL-4 in eotaxin expression: involvement of STAT6. J. Immunol. 176 (2006) 4352-4360
35. Burfoot M.S., Rogers N.C., Watling D., Smith J.M., Pons S., Paonessaw G., Pellegrini S., White M.F., and Kerr I.M. Janus kinase-dependent activation of insulin receptor substrate 1 in response to interleukin-4, oncostatin M, and the interferons. J. Biol. Chem. 272 (1997) 24183-24190
36. Wang Y., Robledo O., Kinzie E., Blanchard F., Richards C., Miyajima A., and Baumann H. Receptor subunit-specific action of oncostatin M in hepatic cells and its modulation by leukemia inhibitory factor. J. Biol. Chem. 275 (2000) 25273-25285
37. Kang H.J., Kang J.S., Lee S.H., Hwang S.J., Chae S.W., Woo J.S., and Lee H.M. Upregulation of oncostatin m in allergic rhinitis. Laryngoscope 115 (2005) 2213-2216
38. Boniface K., Diveu C., Morel F., Pedretti N., Froger J., Ravon E., Garcia M., Venereau E., Preisser L., Guignouard E., Guillet G., Dagregorio G., Pene J., Moles J.P., Yssel H., Chevalier S., Bernard F.X., Gascan H., and Lecron J.C. Oncostatin M secreted by skin infiltrating T lymphocytes is a potent keratinocyte activator involved in skin inflammation. J. Immunol. 178 (2007) 4615-4622
39. O'Hara K.A., Kedda M.A., Thompson P.J., and Knight D.A. Oncostatin M: an interleukin-6-like cytokine relevant to airway remodelling and the pathogenesis of asthma. Clin. Exp. Allergy 33 (2003) 1026-1032
40. Faffe D.S., Flynt L., Mellema M., Moore P.E., Silverman E.S., Subramaniam V., Jones M.R., Mizgerd J.P., Whitehead T., Imrich A., Panettieri Jr. R.A., and Shore S.A. Oncostatin M causes eotaxin-1 release from airway smooth muscle: synergy with IL-4 and IL-13. J. Allergy Clin. Immunol. 115 (2005) 514-520
41. Langdon C., Kerr C., Tong L., Richards C.D., and Oncostatin M. regulates eotaxin expression in fibroblasts and eosinophilic inflammation in C57BL/6 mice. J. Immunol. 170 (2003) 548-555
42. Yamamoto S., Kobayashi I., Tsuji K., Nishi N., Muro E., Miyazaki M., Zaitsu M., Inada S., Ichimaru T., and Hamasaki Y. Upregulation of interleukin-4 receptor by interferon-gamma: enhanced interleukin-4-induced eotaxin-3 production in airway epithelium. Am. J. Respir. Cell Mol. Biol. 31 (2004) 456-462
43. Lugli S.M., Feng N., Heim M.H., Adam M., Schnyder B., Etter H., Yamage M., Eugster H.P., Lutz R.A., Zurawski G., and Moser R. Tumor necrosis factor alpha enhances the expression of the interleukin (IL)-4 receptor alpha-chain on endothelial cells increasing IL-4 or IL-13-induced Stat6 activation. J. Biol. Chem. 272 (1997) 5487-5494
44. Renz H., Domenico J., and Gelfand E.W. IL-4-dependent up-regulation of IL-4 receptor expression in murine T and B cells. J. Immunol. 146 (1991) 3049-3055
45. Ohara J., and Paul W.E. Up-regulation of interleukin 4/B-cell stimulatory factor 1 receptor expression. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 8221-8225
46. Rothenberg M.E., Luster A.D., and Leder P. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8960-8964
47. Zimmermann N., Hogan S.P., Mishra A., Brandt E.B., Bodette T.R., Pope S.M., Finkelman F.D., and Rothenberg M.E. Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J. Immunol. 165 (2000) 5839-5846
48. Hoeck J., and Woisetschlager M. Activation of eotaxin-3/CCLl26 gene expression in human dermal fibroblasts is mediated by STAT6. J. Immunol. 167 (2001) 3216-3222
49. Tong L., Smyth D., Kerr C., Catterall J., and Richards C.D. Mitogen-activated protein kinases Erk1/2 and p38 are required for maximal regulation of TIMP-1 by oncostatin M in murine fibroblasts. Cell. Signal. 16 (2004) 1123-1132
50. Hein H., Schluter C., Kulke R., Christophers E., Schroder J.M., and Bartels J. Genomic organization, sequence, and transcriptional regulation of the human eotaxin gene. Biochem. Biophys. Res. Commun. 237 (1997) 537-542
51. Garcia-Zepeda E.A., Rothenberg M.E., Weremowicz S., Sarafi M.N., Morton C.C., and Luster A.D. Genomic organization, complete sequence, and chromosomal location of the gene for human eotaxin (SCYA11), an eosinophil-specific CC chemokine. Genomics 41 (1997) 471-476
52. Smyth D.C., Kerr C., Li Y., Tang D., Richards C.D., and Oncostatin M. induction of eotaxin-1 expression requires the convergence of PI3′K and ERK1/2 MAPK signal transduction pathways. Cell. Signal. 20 (2008) 1142-1150
53. Dorado B., Martin-Saavedra F.M., Jerez M.J., and Ballester S. The activity of interleukin-4 receptor alpha-chain promoter is regulated by a GT box element. Mol. Immunol. 43 (2006) 1808-1816
54. Ihn H., LeRoy E.C., Trojanowska M., and Oncostatin M. stimulates transcription of the human alpha2(I) collagen gene via the Sp1/Sp3-binding site. J. Biol. Chem. 272 (1997) 24666-24672
55. Coyle A.J., Le Gros G., Bertrand C., Tsuyuki S., Heusser C.H., Kopf M., and Anderson G.P. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13 (1995) 54-59
56. Hogan S.P., Mould A., Kikutani H., Ramsay A.J., and Foster P.S. Aeroallergen-induced eosinophilic inflammation, lung damage, and airways hyperreactivity in mice can occur independently of IL-4 and allergen-specific immunoglobulins. J. Clin. Invest. 99 (1997) 1329-1339
57. Hogan S.P., Matthaei K.I., Young J.M., Koskinen A., Young I.G., Foster P.S., and A novel T. cell-regulated mechanism modulating allergen-induced airways hyperreactivity in BALB/c mice independently of IL-4 and IL-5. J. Immunol. 161 (1998) 1501-1509
58. Grunig G., Warnock M., Wakil A.E., Venkayya R., Brombacher F., Rennick D.M., Sheppard D., Mohrs M., Donaldson D.D., Locksley R.M., and Corry D.B. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282 (1998) 2261-2263
59. Walter D.M., McIntire J.J., Berry G., McKenzie A.N., Donaldson D.D., DeKruyff R.H., and Umetsu D.T. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J. Immunol. 167 (2001) 4668-4675
60. Wills-Karp M., Luyimbazi J., Xu X., Schofield B., Neben T.Y., Karp C.L., and Donaldson D.D. Interleukin-13: central mediator of allergic asthma. Science 282 (1998) 2258-2261
61. Taube C., Duez C., Cui Z.H., Takeda K., Rha Y.H., Park J.W., Balhorn A., Donaldson D.D., Dakhama A., and Gelfand E.W. The role of IL-13 in established allergic airway disease. J. Immunol. 169 (2002) 6482-6489
62. Ramalingam T.R., Pesce J.T., Sheikh F., Cheever A.W., Mentink-Kane M.M., Wilson M.S., Stevens S., Valenzuela D.M., Murphy A.J., Yancopoulos G.D., Urban Jr. J.F., Donnelly R.P., and Wynn T.A. Unique functions of the type II interleukin 4 receptor identified in mice lacking the interleukin 13 receptor alpha1 chain. Nat. Immunol. 9 (2008) 25-33
63. Laporte S.L., Juo Z.S., Vaclavikova J., Colf L.A., Qi X., Heller N.M., Keegan A.D., and Garcia K.C. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132 (2008) 259-272
64. Korzus E., Nagase H., Rydell R., and Travis J. The mitogen-activated protein kinase and JAK-STAT signaling pathways are required for an oncostatin M-responsive element-mediated activation of matrix metalloproteinase 1 gene expression. J. Biol. Chem. 272 (1997) 1188-1196
65. Amaral M.C., Miles S., Kumar G., and Nel A.E. Oncostatin-M stimulates tyrosine protein phosphorylation in parallel with the activation of p42MAPK/ERK-2 in Kaposi's cells. Evidence that this pathway is important in Kaposi cell growth. J. Clin. Invest. 92 (1993) 848-857
66. Humbles A.A., Lloyd C.M., McMillan S.J., Friend D.S., Xanthou G., McKenna E.E., Ghiran S., Gerard N.P., Yu C., Orkin S.H., and Gerard C. A critical role for eosinophils in allergic airways remodeling. Science 305 (2004) 1776-1779
67. Lee J.J., Dimina D., Macias M.P., Ochkur S.I., McGarry M.P., O'Neill K.R., Protheroe C., Pero R., Nguyen T., Cormier S.A., Lenkiewicz E., Colbert D., Rinaldi L., Ackerman S.J., Irvin C.G., and Lee N.A. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305 (2004) 1773-1776
68. Chen Q., Rabach L., Noble P., Zheng T., Lee C.G., Homer R.J., and Elias J.A. IL-11 receptor alpha in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 174 (2005) 2305-2313
69. Tang W., Geba G.P., Zheng T., Ray P., Homer R.J., Kuhn III C., Flavell R.A., and Elias J.A. Targeted expression of IL-11 in the murine airway causes lymphocytic inflammation, bronchial remodeling, and airways obstruction. J. Clin. Invest. 98 (1996) 2845-2853
70. Einarsson O., Geba G.P., Zhu Z., Landry M., and Elias J.A. Interleukin-11: stimulation in vivo and in vitro by respiratory viruses and induction of airways hyperresponsiveness. J. Clin. Invest. 97 (1996) 915-924
71. Einarsson O., Geba G.P., Panuska J.R., Zhu Z., Landry M., and Elias J.A. Asthma-associated viruses specifically induce lung stromal cells to produce interleukin-11, a mediator of airways hyperreactivity. Chest 107 (1995) 132S-133S
72. Minshall E., Chakir J., Laviolette M., Molet S., Zhu Z., Olivenstein R., Elias J.A., and Hamid Q. IL-11 expression is increased in severe asthma: association with epithelial cells and eosinophils. J. Allergy. Clin. Immunol. 105 (2000) 232-238
73. Kuhn III C., Homer R.J., Zhu Z., Ward N., Flavell R.A., Geba G.P., and Elias J.A. Airway hyperresponsiveness and airway obstruction in transgenic mice. Morphologic correlates in mice overexpressing interleukin (IL)-11 and IL-6 in the lung. Am. J. Respir. Cell Mol. Biol. 22 (2000) 289-295
74. Bain J., Plater L., Elliott M., Shapiro N., Hastie C.J., McLauchlan H., Kleverni I., Arthur J.S., Alessi D.S., and Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochemical. J. 408 (2007) 297-315