IL-13 dampens human airway epithelial innate immunity through induction of IL-1 receptor-associated kinase M

Journal of Allergy and Clinical Immunology

Volumn 129, Issue 3, 2012, Pages

  Wu, Qun ^a   Jiang, Di ^a   Smith, Sean ^a   Thaikoottathil, Jyoti ^a   Martin, Richard J ^a   Bowler, Russell P ^a   Chu, Hong Wei ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

airway epithelial cells; IL 1 receptor associated kinase M; IL 13; Toll like receptor 2

Indexed keywords

BETA DEFENSIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 13; INTERLEUKIN 8; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; PROTEIN KINASE B; TOLL LIKE RECEPTOR 2;

ARTICLE; ASTHMA; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFECTION SENSITIVITY; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; TH2 CELL; UPREGULATION;

EID: 84857797243     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2011.10.043     Document Type: Article

References (74)

1. S.S. Braman The global burden of asthma Chest 130 suppl 2006 4S 12S (Pubitemid 44107231)
2. C.M. Sevin, and R.S. Peebles Jr. Infections and asthma: new insights into old ideas Clin Exp Allergy 40 2010 1142 1154
3. C. Pilette, S.R. Durham, J.P. Vaerman, and Y. Sibille Mucosal immunity in asthma and chronic obstructive pulmonary disease: a role for immunoglobulin A? Proc Am Thorac Soc 1 2004 125 135
4. G.Y. Park, N. Hu, X. Wang, R.T. Sadikot, F.E. Yull, and M. Joo Conditional regulation of cyclooxygenase-2 in tracheobronchial epithelial cells modulates pulmonary immunity Clin Exp Immunol 150 2007 245 254 (Pubitemid 47609558)
5. S. Akira, and K. Takeda Toll-like receptor signalling Nat Rev Immunol 4 2004 499 511 (Pubitemid 38931765)
6. B. Beutler, K. Hoebe, X. Du, and R.J. Ulevitch How we detect microbes and respond to them: the Toll-like receptors and their transducers J Leukoc Biol 74 2003 479 485 (Pubitemid 38040374)
7. C.J. Hertz, Q. Wu, E.M. Porter, Y.J. Zhang, K.H. Weismuller, and P.J. Godowski Activation of Toll-like receptor 2 on human tracheobronchial epithelial cells induces the antimicrobial peptide human beta defensin-2 J Immunol 171 2003 6820 6826 (Pubitemid 37532117)
8. Q. Wu, R.J. Martin, S. Lafasto, B.J. Efaw, J.G. Rino, and R.J. Harbeck Toll-like receptor 2 down-regulation in established mouse allergic lungs contributes to decreased Mycoplasma clearance Am J Respir Crit Care Med 177 2008 720 729 (Pubitemid 351490559)
9. Q. Wu, D. Jiang, M.N. Minor, R.J. Martin, and H.W. Chu In vivo function of airway epithelial TLR2 in host defense against bacterial infection Am J Physiol Lung Cell Mol Physiol 300 2011 L579 L586
10. J.A. Elias, C.G. Lee, T. Zheng, B. Ma, R.J. Homer, and Z. Zhu New insights into the pathogenesis of asthma J Clin Invest 111 2003 291 297 (Pubitemid 36182201)
11. S.L. Prescott New concepts of cytokines in asthma: is the Th2/Th1 paradigm out the window? J Paediatr Child Health 39 2003 575 579 (Pubitemid 37463938)
12. I. Nomura, E. Goleva, M.D. Howell, Q.A. Hamid, P.Y. Ong, and C.F. Hall Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes J Immunol 171 2003 3262 3269 (Pubitemid 37093553)
13. K.O. Kisich, C.W. Carspecken, S. Fieve, M. Boguniewicz, and D.Y. Leung Defective killing of Staphylococcus aureus in atopic dermatitis is associated with reduced mobilization of human beta-defensin-3 J Allergy Clin Immunol 122 2008 62 68
14. M. Ramanathan Jr., W.K. Lee, E.W. Spannhake, and A.P. Lane Th2 cytokines associated with chronic rhinosinusitis with polyps down-regulate the antimicrobial immune function of human sinonasal epithelial cells Am J Rhinol 22 2008 115 121 (Pubitemid 351570549)
15. T. Mueller, T. Terada, I.M. Rosenberg, O. Shibolet, and D.K. Podolsky Th2 cytokines down-regulate TLR expression and function in human intestinal epithelial cells J Immunol 176 2006 5805 5814
16. J. Su, Q. Xie, I. Wilson, and L. Li Differential regulation and role of interleukin-1 receptor associated kinase-M in innate immunity signaling Cell Signal 19 2007 1596 1601 (Pubitemid 46818922)
17. K. Nakashima, T. Hirota, K. Obara, M. Shimizu, A. Jodo, and M. Kameda An association study of asthma and related phenotypes with polymorphisms in negative regulator molecules of the TLR signaling pathway J Hum Genet 51 2006 284 291
18. K.C. Barnes, J.D. Neely, D.L. Duffy, L.R. Freidhoff, D.R. Breazeale, and C. Schou Linkage of asthma and total serum IgE concentration to markers on chromosome 12q: evidence from Afro-Caribbean and Caucasian populations Genomics 37 1996 41 50 (Pubitemid 26341832)
19. B.A. Raby, E.K. Silverman, R. Lazarus, C. Lange, D.J. Kwiatkowski, and S.T. Weiss Chromosome 12q harbors multiple genetic loci related to asthma and asthma-related phenotypes Hum Mol Genet 12 2003 1973 1979 (Pubitemid 37038806)
20. L. Balaci, M.C. Spada, N. Olla, G. Sole, L. Loddo, and F. Anedda IRAK-M is involved in the pathogenesis of early-onset persistent asthma Am J Hum Genet 80 2007 1103 1114 (Pubitemid 47579346)
21. H. Wesche, X. Gao, X. Li, C.J. Kirschning, G.R. Stark, and Z. Cao IRAK-M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family J Biol Chem 274 1999 19403 19410
22. K. Kobayashi, L.D. Hernandez, J.E. Galan, C.A. Janeway Jr., R. Medzhitov, and R.A. Flavell IRAK-M is a negative regulator of Toll-like receptor signaling Cell 110 2002 191 202 (Pubitemid 34876547)
23. S.E. Wenzel, J.B. Trudeau, D.A. Kaminsky, J. Cohn, R.J. Martin, and J.Y. Westcott Effect of 5-lipoxygenase inhibition on bronchoconstriction and airway inflammation in nocturnal asthma Am J Respir Crit Care Med 152 1995 897 905
24. K.M. Britten, P.H. Howarth, and W.R. Roche Immunohistochemistry on resin sections: a comparison of resin embedding techniques for small mucosal biopsies Biotech Histochem 68 1993 271 280 (Pubitemid 23305102)
25. H.W. Chu, J.L. Halliday, R.J. Martin, D.Y. Leung, S.J. Szefler, and S.E. Wenzel Collagen deposition in large airways may not differentiate severe asthma from milder forms of the disease Am J Respir Crit Care Med 158 1998 1936 1944 (Pubitemid 29008836)
26. H.W. Chu, J.B. Trudeau, S. Balzar, and S.E. Wenzel Peripheral blood and airway tissue expression of transforming growth factor beta by neutrophils in asthmatic subjects and normal control subjects J Allergy Clin Immunol 106 2000 1115 1123 (Pubitemid 32006266)
27. C.A. Gross, R.P. Bowler, R.M. Green, A.R. Weinberger, C. Schnell, and H.W. Chu beta2-agonists promote host defense against bacterial infection in primary human bronchial epithelial cells BMC Pulm Med 10 2010 30
28. Q. Shen, Y. Bai, K.C. Chang, Y. Wang, T.P. Burris, and L.P. Freedman Liver X receptor-retinoid X receptor (LXR-RXR) heterodimer cistrome reveals coordination of LXR and AP1 signaling in keratinocytes J Biol Chem 286 2011 14554 14563
29. W.W. Hwang-Verslues, and F.M. Sladek Nuclear receptor hepatocyte nuclear factor 4alpha1 competes with oncoprotein c-Myc for control of the p21/WAF1 promoter Mol Endocrinol 22 2008 78 90
30. Y. Refaeli, K.A. Field, B.C. Turner, A. Trumpp, and J.M. Bishop The protooncogene MYC can break B cell tolerance Proc Natl Acad Sci U S A 102 2005 4097 4102 (Pubitemid 40388561)
31. H.W. Chu, J. Thaikoottathil, J.G. Rino, G. Zhang, Q. Wu, and T. Moss Function and regulation of SPLUNC1 protein in Mycoplasma infection and allergic inflammation J Immunol 179 2007 3995 4002
32. H.S. Farghaly, I.S. Blagbrough, D.A. Medina-Tato, and M.L. Watson Interleukin 13 increases contractility of murine tracheal smooth muscle by a phosphoinositide 3-kinase p110delta-dependent mechanism Mol Pharmacol 73 2008 1530 1537 (Pubitemid 351574842)
33. V. Zacharioudaki, A. Androulidaki, A. Arranz, G. Vrentzos, A.N. Margioris, and C. Tsatsanis Adiponectin promotes endotoxin tolerance in macrophages by inducing IRAK-M expression J Immunol 182 2009 6444 6451
34. H.T. Chen, H.K. Tsou, C.J. Hsu, C.H. Tsai, C.H. Kao, and Y.C. Fong Stromal cell-derived factor-1/CXCR4 promotes IL-6 production in human synovial fibroblasts J Cell Biochem 112 2011 1219 1227
35. L.L. Hubbard, and B.B. Moore IRAK-M regulation and function in host defense and immune homeostasis Infect Dis Rep 2010 2
36. N. Oshima, S. Ishihara, M.A. Rumi, M.M. Aziz, Y. Mishima, and C. Kadota A20 is an early responding negative regulator of Toll-like receptor 5 signalling in intestinal epithelial cells during inflammation Clin Exp Immunol 159 2010 185 198
37. D.A. Searing, Y. Zhang, J.R. Murphy, P.J. Hauk, E. Goleva, and D.Y. Leung Decreased serum vitamin D levels in children with asthma are associated with increased corticosteroid use J Allergy Clin Immunol 125 2010 995 1000
38. M. Sanak, A. Gielicz, G. Bochenek, M. Kaszuba, E. Nizankowska-Mogilnicka, and A. Szczeklik Targeted eicosanoid lipidomics of exhaled breath condensate provide a distinct pattern in the aspirin-intolerant asthma phenotype J Allergy Clin Immunol 127 2011 1141 1147 e2
39. C.J. Scotton, F.O. Martinez, M.J. Smelt, M. Sironi, M. Locati, and A. Mantovani Transcriptional profiling reveals complex regulation of the monocyte IL-1 beta system by IL-13 J Immunol 174 2005 834 845 (Pubitemid 40103564)
40. V. Batra, A.I. Musani, A.T. Hastie, S. Khurana, K.A. Carpenter, and J.G. Zangrilli 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 (Pubitemid 38373007)
41. E.N. Atochina-Vasserman, C. Winkler, H. Abramova, F. Schaumann, N. Krug, and A.J. Gow Segmental allergen challenge alters multimeric structure and function of surfactant protein D in humans Am J Respir Crit Care Med 183 2011 856 864
42. Y.Y. He, J.L. Huang, R.H. Sik, J. Liu, M.P. Waalkes, and C.F. Chignell Expression profiling of human keratinocyte response to ultraviolet A: implications in apoptosis J Invest Dermatol 122 2004 533 543 (Pubitemid 38281080)
43. K.P. Jayapal, R.J. Philp, Y.J. Kok, M.G. Yap, D.H. Sherman, and T.J. Griffin Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor PLoS One 3 2008 e2097
44. F.J. Sheedy, E. Palsson-McDermott, E.J. Hennessy, C. Martin, J.J. O'Leary, and Q. Ruan Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21 Nat Immunol 11 2010 141 147
45. P. Escoll, C. del Fresno, L. Garcia, G. Valles, M.J. Lendinez, and F. Arnalich Rapid up-regulation of IRAK-M expression following a second endotoxin challenge in human monocytes and in monocytes isolated from septic patients Biochem Biophys Res Commun 311 2003 465 472 (Pubitemid 37340100)
46. T. Kawai, and S. Akira Signaling to NF-kappaB by Toll-like receptors Trends Mol Med 13 2007 460 469
47. M.A. Dobrovolskaia, A.E. Medvedev, K.E. Thomas, N. Cuesta, V. Toshchakov, and T. Ren Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-kappa B signaling pathway components J Immunol 170 2003 508 519 (Pubitemid 36026178)
48. T. Birchler, R. Seibl, K. Buchner, S. Loeliger, R. Seger, and J.P. Hossle Human Toll-like receptor 2 mediates induction of the antimicrobial peptide human beta-defensin 2 in response to bacterial lipoprotein Eur J Immunol 31 2001 3131 3137 (Pubitemid 33100504)
49. M.N. Becker, G. Diamond, M.W. Verghese, and S.H. Randell CD14-dependent lipopolysaccharide-induced beta-defensin-2 expression in human tracheobronchial epithelium J Biol Chem 275 2000 29731 29736 (Pubitemid 32043854)
50. T. Tomita, T. Nagase, E. Ohga, Y. Yamaguchi, M. Yoshizumi, and Y. Ouchi Molecular mechanisms underlying human beta-defensin-2 gene expression in a human airway cell line (LC2/ad) Respirology 7 2002 305 310
51. J. Wehkamp, J. Harder, K. Wehkamp, B. Wehkamp-von Meissner, M. Schlee, and C. Enders NF-kappaB- and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium Infect Immun 72 2004 5750 5758 (Pubitemid 39303685)
52. S. Janssens, and R. Beyaert Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members Mol Cell 11 2003 293 302 (Pubitemid 36293825)
53. S. Flannery, and A.G. Bowie The interleukin-1 receptor-associated kinases: critical regulators of innate immune signalling Biochem Pharmacol 80 2010 1981 1991
54. B.W. Booth, K.B. Adler, J.C. Bonner, F. Tournier, and L.D. Martin Interleukin-13 induces proliferation of human airway epithelial cells in vitro via a mechanism mediated by transforming growth factor-alpha Am J Respir Cell Mol Biol 25 2001 739 743 (Pubitemid 33124691)
55. S.M. Lankford, M. Macchione, A.L. Crews, S.A. McKane, N.J. Akley, and L.D. Martin Modeling the airway epithelium in allergic asthma: interleukin-13- induced effects in differentiated murine tracheal epithelial cells In Vitro Cell Dev Biol Anim 41 2005 217 224 (Pubitemid 41504525)
56. B.W. Booth, T. Sandifer, E.L. Martin, and L.D. Martin IL-13-induced proliferation of airway epithelial cells: mediation by intracellular growth factor mobilization and ADAM17 Respir Res 8 2007 51
57. S.E. Wenzel, J.B. Trudeau, D.A. Kaminsky, J. Cohn, R.J. Martin, and J.Y. Westcott Effect of 5-lipoxygenase inhibition on bronchoconstriction and airway inflammation in nocturnal asthma Am J Respir Crit Care Med 152 1995 897 905
58. K.M. Britten, P.H. Howarth, and W.R. Roche Immunohistochemistry on resin sections: a comparison of resin embedding techniques for small mucosal biopsies Biotech Histochem 68 1993 271 280 (Pubitemid 23305102)
59. H.W. Chu, J.L. Halliday, R.J. Martin, D.Y. Leung, S.J. Szefler, and S.E. Wenzel Collagen deposition in large airways may not differentiate severe asthma from milder forms of the disease Am J Respir Crit Care Med 158 1998 1936 1944 (Pubitemid 29008836)
60. H.W. Chu, J.B. Trudeau, S. Balzar, and S.E. Wenzel Peripheral blood and airway tissue expression of transforming growth factor beta by neutrophils in asthmatic subjects and normal control subjects J Allergy Clin Immunol 106 2000 1115 1123 (Pubitemid 32006266)
61. C.A. Gross, R.P. Bowler, R.M. Green, A.R. Weinberger, C. Schnell, and H.W. Chu beta2-agonists promote host defense against bacterial infection in primary human bronchial epithelial cells BMC Pulm Med 10 2010 30
62. H.W. Chu, J. Thaikoottathil, J.G. Rino, G. Zhang, Q. Wu, and T. Moss Function and regulation of SPLUNC1 protein in Mycoplasma infection and allergic inflammation J Immunol 179 2007 3995 4002
63. H.W. Chu, S. Balzar, G.J. Seedorf, J.Y. Westcott, J.B. Trudeau, and P. Silkoff Transforming growth factor-beta2 induces bronchial epithelial mucin expression in asthma Am J Pathol 165 2004 1097 1106 (Pubitemid 39297717)
64. J. Xiang, J. Rir-Sim-Ah, and Y. Tesfaigzi IL-9 and IL-13 induce mucous cell metaplasia that is reduced by IFN-gamma in a Bax-mediated pathway Am J Respir Cell Mol Biol 38 2008 310 317 (Pubitemid 351567700)
65. T.H. Yeh, S.Y. Lee, and W.C. Hsu Expression of SPLUNC1 protein in nasal polyp epithelial cells in air-liquid interface culture treated with IL-13 Am J Rhinol Allergy 24 2010 17 20
66. V. Batra, A.I. Musani, A.T. Hastie, S. Khurana, K.A. Carpenter, and J.G. Zangrilli 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 (Pubitemid 38373007)
67. S.W. Han, and J. Roman Fibronectin induces cell proliferation and inhibits apoptosis in human bronchial epithelial cells: pro-oncogenic effects mediated by PI3-kinase and NF-kappa B Oncogene 25 2006 4341 4349 (Pubitemid 44100504)
68. S. Shahabuddin, R. Ji, P. Wang, E. Brailoiu, N. Dun, and Y. Yang CXCR3 chemokine receptor-induced chemotaxis in human airway epithelial cells: role of p38 MAPK and PI3K signaling pathways Am J Physiol Cell Physiol 291 2006 C34 C39
69. P. Mendez-Samperio, A. Trejo, and A. Perez Mycobacterium bovis Bacillus Calmette-Guerin (BCG) stimulates IL-10 production via the PI3K/Akt and p38 MAPK pathways in human lung epithelial cells Cell Immunol 251 2008 37 42
70. Q. Shen, Y. Bai, K.C. Chang, Y. Wang, T.P. Burris, and L.P. Freedman Liver X receptor-retinoid X receptor (LXR-RXR) heterodimer cistrome reveals coordination of LXR and AP1 signaling in keratinocytes J Biol Chem 286 2011 14554 14563
71. W.W. Hwang-Verslues, and F.M. Sladek Nuclear receptor hepatocyte nuclear factor 4alpha1 competes with oncoprotein c-Myc for control of the p21/WAF1 promoter Mol Endocrinol 22 2008 78 90
72. Y. Refaeli, K.A. Field, B.C. Turner, A. Trumpp, and J.M. Bishop The protooncogene MYC can break B cell tolerance Proc Natl Acad Sci U S A 102 2005 4097 4102 (Pubitemid 40388561)
73. S.M. Smith, A.P. Moran, S.P. Duggan, S.E. Ahmed, A.S. Mohamed, and H.J. Windle Tribbles 3: a novel regulator of TLR2-mediated signaling in response to Helicobacter pylori lipopolysaccharide J Immunol 186 2011 2462 2471
74. M. Nasso, G. Fedele, F. Spensieri, R. Palazzo, P. Costantino, and R. Rappuoli Genetically detoxified pertussis toxin induces Th1/Th17 immune response through MAPKs and IL-10-dependent mechanisms J Immunol 183 2009 1892 1899