NF-κB mediates IL-1β- and IL-17A-induced MUC5B expression in airway epithelial cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 2, 2011, Pages 246-252

  Fujisawa, Tomoyuki ^a,c   Chang, Mary Mann Jong ^a   Velichko, Sharlene ^a   Thai, Philip ^a   Hung, Li Yin ^a   Huang, Fei ^a   Phuong, Newton ^a   Chen, Yin ^b   Wu, Reen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cytokines; Gene regulation; Lung; Mucin; Transcription factors

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; MESSENGER RNA; MUCIN 5B; SMALL INTERFERING RNA; SYNAPTOTAGMIN I;

ARTICLE; BINDING SITE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PROTEIN BINDING; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM;

BLOTTING, WESTERN; BRONCHI; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-17; INTERLEUKIN-1BETA; MUCIN-5B; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RESPIRATORY SYSTEM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 80051640917     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0313OC     Document Type: Article

References (46)

1. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 2002;109:571-577. (Pubitemid 34204834)
2. Thai P, Loukoianov A, Wachi S, Wu R. Regulation of airway mucin gene expression. Annu Rev Physiol 2008;70:405-429. (Pubitemid 351738186)
3. Kim WD. Lung mucus: a clinician's view. Eur Respir J 1997;10:1914-1917. (Pubitemid 27368389)
4. Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 2006;86:245-278.
5. Chen Y, Zhao YH, Di YP, Wu R. Characterization of human mucin 5b gene expression in airway epithelium and the genomic clone of the amino-terminal and 5′-flanking region. Am J Respir Cell Mol Biol 2001;25:542-553. (Pubitemid 33087104)
6. Kirkham S, Kolsum U, Rousseau K, Singh D, Vestbo J, Thornton DJ. Muc5b is the major mucin in the gel phase of sputum in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008;178:1033-1039.
7. Chen Y, Zhao YH, Wu R. In silico cloning of mouse Muc5b gene and upregulation of its expression in mouse asthma model. Am J Respir Crit Care Med 2001;164:1059-1066. (Pubitemid 32971659)
8. Song KS, Lee WJ, Chung KC, Koo JS, Yang EJ, Choi JY, Yoon JH. Interleukin-1 beta and tumor necrosis factor-alpha induce Muc5ac overexpression through a mechanism involving ERK/p38 mitogen-activated protein kinases-MSK1-CREB activation in human airway epithelial cells. J Biol Chem 2003;278:23243-23250. (Pubitemid 36830137)
9. Young HW, Williams OW, Chandra D, Bellinghausen LK, Perez G, Suarez A, Tuvim MJ, Roy MG, Alexander SN, Moghaddam SJ, et al. Central role of Muc5ac expression in mucous metaplasia and its regulation by conserved 5′ elements. Am J Respir Cell Mol Biol 2007;37:273-290. (Pubitemid 350067607)
10. Fujisawa T, Ide K, Holtzman MJ, Suda T, Suzuki K, Kuroishi S, Chida K, Nakamura H. Involvement of the p38 MAPK pathway in IL-13-induced mucous cell metaplasia in mouse tracheal epithelial cells. Respirology 2008;13:191-202. (Pubitemid 351388781)
11. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. Regulation of airway MUC5AC expression by IL-1β and IL-17A: the NF-κB paradigm. J Immunol 2009;183:6236-6243.
12. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 2003;278:17036-17043. (Pubitemid 36799579)
13. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999;18:6853-6866.
14. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008;132:344-362.
15. Sun SC, Ley SC. New insights into NF-kappaB regulation and function. Trends Immunol 2008;29:469-478.
16. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-260. (Pubitemid 28183365)
17. Hart LA, Krishnan VL, Adcock IM, Barnes PJ, Chung KF. Activation and localization of transcription factor, nuclear factor-kappaB, in asthma. Am J Respir Crit Care Med 1998;158:1585-1592.
18. Di Stefano A, Caramori G, Oates T, Capelli A, Lusuardi M, Gnemmi I, Ioli F, Chung KF, Donner CF, Barnes PJ, et al. Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur Respir J 2002;20:556-563.
19. Broide DH, Lawrence T, Doherty T, Cho JY, Miller M, McElwain K, McElwain S, Karin M. Allergen-induced peribronchial fibrosis and mucus production mediated by IkappaB kinase beta-dependent genes in airway epithelium. Proc Natl Acad Sci USA 2005;102:17723-17728. (Pubitemid 41803564)
20. Poynter ME, Cloots R, van Woerkom T, Butnor KJ, Vacek P, Taatjes DJ, Irvin CG, Janssen-Heininger YM. NF-kappa B activation in airways modulates allergic inflammation but not hyperresponsiveness. J Immunol 2004;173:7003-7009. (Pubitemid 39541089)
21. Preciado D, Lin J, Wuertz B, Rose M. Cigarette smoke activates NF kappa B and induces Muc5b expression in mouse middle ear cells. Laryngoscope 2008;118:464-471. (Pubitemid 351640618)
22. Chen R, Lim JH, Jono H, Gu XX, Kim YS, Basbaum CB, Murphy TF, Li JD. Nontypeable Haemophilus influenzae lipoprotein P6 induces Muc5ac mucin transcription via TLR2-TAK1-dependent p38 MAPK-AP1 and Ikkbeta-IkappaBalpha-NF- kappaB signaling pathways. Biochem Biophys Res Commun 2004;324:1087-1094. (Pubitemid 39361620)
23. Kraft M, Adler KB, Ingram JL, Crews AL, Atkinson TP, Cairns CB, Krause DC, Chu HW. Mycoplasma pneumoniae induces airway epithelial cell expression of Muc5ac in asthma. Eur Respir J 2008;31:43-46.
24. Kadota J, Matsubara Y, Ishimatsu Y, Ashida M, Abe K, Shirai R, Iida K, Kawakami K, Taniguchi H, Fujii T, et al. Significance of IL-1beta and IL-1 receptor antagonist (IL-1ra) in bronchoalveolar lavage fluid (BALF) in patients with diffuse panbronchiolitis (DPB). Clin Exp Immunol 1996;103:461-466.
25. Gessner C, Scheibe R, Wotzel M, Hammerschmidt S, Kuhn H, Engelmann L, Hoheisel G, Gillissen A, Sack U, Wirtz H. Exhaled breath condensate cytokine patterns in chronic obstructive pulmonary disease. Respir Med 2005;99:1229-1240. (Pubitemid 41245308)
26. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 2007;87:1047-1082. (Pubitemid 47084676)
27. Subramaniam S, Stansberg C, Cunningham C. The interleukin 1 receptor family. Dev Comp Immunol 2004;28:415-428. (Pubitemid 38177445)
28. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007;25:821-852. (Pubitemid 46697925)
29. Ye P, Garvey PB, Zhang P, Nelson S, Bagby G, Summer WR, Schwarzenberger P, Shellito JE, Kolls JK. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am J Respir Cell Mol Biol 2001;25:335-340. (Pubitemid 32918915)
30. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001;194:519-527. (Pubitemid 32835046)
31. Moseley TA, Haudenschild DR, Rose L, Reddi AH. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 2003;14:155-174. (Pubitemid 36389528)
32. Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N, Olivenstein R, Elias J, Chakir J. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 2001;108:430-438. (Pubitemid 32881066)
33. Traves SL, Donnelly LE. Th17 cells in airway diseases. Curr Mol Med 2008;8:416-426.
34. Huang F, Kao CY, Wachi S, Thai P, Ryu J, Wu R. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J Immunol 2007;179:6504-6513.
35. Kao CY, Kim C, Huang F, Wu R. Requirements for two proximal NF-kappaB binding sites and IkappaB-zeta in IL-17A-induced human beta-defensin 2 expression by conducting airway epithelium. J Biol Chem 2008;283:15309-15318.
36. Kao CY, Chen Y, Thai P, Wachi S, Huang F, Kim C, Harper RW, Wu R. IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol 2004;173:3482-3491. (Pubitemid 39142059)
37. Kao CY, Huang F, Chen Y, Thai P, Wachi S, Kim C, Tam L, Wu R. Upregulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway. J Immunol 2005;175:6676-6685. (Pubitemid 41598911)
38. Yankaskas JR, Haizlip JE, Conrad M, Koval D, Lazarowski E, Paradiso AM, Rinehart CA Jr, Sarkadi B, Schlegel R, Boucher RC. Papilloma virus immortalized tracheal epithelial cells retain a well-differentiated phenotype. Am J Physiol 1993;264:C1219-C1230. (Pubitemid 23158828)
39. Lin H, Carlson DM, St George JA, Plopper CG, Wu R. An ELISA method for the quantitation of tracheal mucins from human and nonhuman primates. Am J Respir Cell Mol Biol 1989;1:41-48.
40. Wu YCD, Wu R, Reddy SP, Lee YC, Chang MM. Distinctive epidermal growth factor receptor/extracellular regulated kinase-independent and -dependent signaling pathways in the induction of airway mucin 5B and mucin 5AC expression by phorbol 12-myristate 13-acetate. Am J Pathol 2007;170:20-32. (Pubitemid 47339186)
41. Wu DY, Wu R, Chen Y, Tarasova N, Chang MM. PMA stimulates MUC5B gene expression through an SP1-based mechanism in airway epithelial cells. Am J Respir Cell Mol Biol 2007;37:589-597. (Pubitemid 350058190)
42. Gray T, Coakley R, Hirsh A, Thornton D, Kirkham S, Koo JS, Burch L, Boucher R, Nettesheim P. Regulation of MUC5AC mucin secretion and airway surface liquid metabolism by IL-1beta in human bronchial epithelia. Am J Physiol Lung Cell Mol Physiol 2004;286:320-330.
43. Cheng DS, Han W, Chen SM, Sherrill TP, Chont M, Park GY, Sheller JR, Polosukhin VV, Christman JW, Yull FE, et al. Airway epithelium controls lung inflammation and injury through the NF-kappa B pathway. J Immunol 2007;178:6504-6513. (Pubitemid 46717434)
44. Haegens A, Barrett TF, Gell J, Shukla A, Macpherson M, Vacek P, Poynter ME, Butnor KJ, Janssen-Heininger YM, Steele C, et al. Airway epithelial NF-kappaB activation modulates asbestos-induced inflammation and mucin production in vivo. J Immunol 2007;178:1800-1808. (Pubitemid 46154652)
45. Pantano C, Ather JL, Alcorn JF, Poynter ME, Brown AL, Guala AS, Beuschel SL, Allen GB, Whittaker LA, Bevelander M, et al. Nuclear factor-kappaB activation in airway epithelium induces inflammation and hyperresponsiveness. Am J Respir Crit Care Med 2008;177:959-969. (Pubitemid 351717589)
46. Choi HJ, Chung YS, Kim HJ, Moon UY, Choi YH, Van Seuningen I, Baek SJ, Yoon HG, Yoon JH. Signal pathway of 17beta-estradiol-induced MUC5B expression in human airway epithelial cells. Am J Respir Cell Mol Biol 2009;40:168-178.