CCL20/CCR6 feedback exaggerates epidermal growth factor receptor-dependent MUC5AC mucin production in human airway epithelial (NCI-H292) cells

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3392-3400

  Kim, Suil ^a   Lewis, Courtney ^a   Nadel, Jay A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR6; EPIDERMAL GROWTH FACTOR RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MUCIN 5AC; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RECEPTOR BINDING; RESPIRATORY EPITHELIUM; UPREGULATION;

CARCINOMA, MUCOEPIDERMOID; CELL COMMUNICATION; CELL LINE, TUMOR; CHEMOKINE CCL20; FEEDBACK, PHYSIOLOGICAL; HUMANS; LIGANDS; LUNG NEOPLASMS; MUCIN 5AC; PHOSPHORYLATION; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CCR6; RESPIRATORY MUCOSA; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 79953166053     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003377     Document Type: Article

References (56)

1. Kuyper, L. M., P. D. Paré, J. C. Hogg, R. K. Lambert, D. Ionescu, R. Woods, and T. R. Bai. 2003. Characterization of airway plugging in fatal asthma. Am. J. Med. 115: 6-11.
2. Hogg, J. C., F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré. 2004. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med. 350: 2645-2653.
3. Burgel, P. R., D. Montani, C. Danel, D. J. Dusser, and J. A. Nadel. 2007. A morphometric study of mucins and small airway plugging in cystic fibrosis. Thorax 62: 153-161.
4. Davies, J. R., H. W. Hovenberg, C. J. Lindén, R. Howard, P. S. Richardson, J. K. Sheehan, and I. Carlstedt. 1996. Mucins in airway secretions from healthy and chronic bronchitic subjects. Biochem. J. 313: 431-439. (Pubitemid 26030130)
5. Groneberg, D. A., P. R. Eynott, S. Lim, T. Oates, R. Wu, I. Carlstedt, P. Roberts, B. McCann, A. G. Nicholson, B. D. Harrison, and K. F. Chung. 2002. Expression of respiratory mucins in fatal status asthmaticus and mild asthma. Histopathology 40: 367-373.
6. Groneberg, D. A., P. R. Eynott, T. Oates, S. Lim, R. Wu, I. Carlstedt, A. G. Nicholson, and K. F. Chung. 2002. Expression of MUC5AC and MUC5B mucins in normal and cystic fibrosis lung. Respir. Med. 96: 81-86.
7. Ordoñez, C. L., R. Khashayar, H. H. Wong, R. Ferrando, R. Wu, D. M. Hyde, J. A. Hotchkiss, Y. Zhang, A. Novikov, G. Dolganov, and J. V. Fahy. 2001. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am. J. Respir. Crit. Care Med. 163: 517-523.
8. Shao, M. X., I. F. Ueki, and J. A. Nadel. 2003. Tumor necrosis factor alpha-converting enzyme mediates MUC5AC mucin expression in cultured human airway epithelial cells. Proc. Natl. Acad. Sci. USA 100: 11618-11623.
9. Lemjabbar, H., and C. Basbaum. 2002. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat. Med. 8: 41-46.
10. Zhu, L., P. K. Lee, W. M. Lee, Y. Zhao, D. Yu, and Y. Chen. 2009. Rhinovirus-induced major airway mucin production involves a novel TLR3-EGFR-dependent pathway. Am. J. Respir. Cell Mol. Biol. 40: 610-619.
11. Takeyama, K., B. Jung, J. J. Shim, P. R. Burgel, T. Dao-Pick, I. F. Ueki, U. Protin, P. Kroschel, and J. A. Nadel. 2001. Activation of epidermal growth factor receptors is responsible for mucin synthesis induced by cigarette smoke. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L165-L172.
12. Takeyama, K., K. Dabbagh, H. M. Lee, C. Agustí, J. A. Lausier, I. F. Ueki, K. M. Grattan, and J. A. Nadel. 1999. Epidermal growth factor system regulates mucin production in airways. Proc. Natl. Acad. Sci. USA 96: 3081-3086.
13. Ohtsu, H., P. J. Dempsey, and S. Eguchi. 2006. ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291: C1-C10.
14. Starner, T. D., C. K. Barker, H. P. Jia, Y. Kang, and P. B. McCray, Jr. 2003. CCL20 is an inducible product of human airway epithelia with innate immune properties. Am. J. Respir. Cell Mol. Biol. 29: 627-633.
15. Pichavant, M., A. S. Charbonnier, S. Taront, A. Brichet, B. Wallaert, J. Pestel, A. B. Tonnel, and P. Gosset. 2005. Asthmatic bronchial epithelium activated by the proteolytic allergen Der p 1 increases selective dendritic cell recruitment. J. Allergy Clin. Immunol. 115: 771-778.
16. Demedts, I. K., K. R. Bracke, G. Van Pottelberge, D. Testelmans, G. M. Verleden, F. E. Vermassen, G. F. Joos, and G. G. Brusselle. 2007. Accumulation of dendritic cells and increased CCL20 levels in the airways of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 175: 998-1005.
17. Reibman, J., Y. Hsu, L. C. Chen, B. Bleck, and T. Gordon. 2003. Airway epithelial cells release MIP-3alpha/CCL20 in response to cytokines and ambient particulate matter. Am. J. Respir. Cell Mol. Biol. 28: 648-654.
18. Marcet, B., M. Horckmans, F. Libert, S. Hassid, J. M. Boeynaems, and D. Communi. 2007. Extracellular nucleotides regulate CCL20 release from human primary airway epithelial cells, monocytes and monocyte-derived dendritic cells. J. Cell. Physiol. 211: 716-727.
19. Bracke, K. R., A. I. D'hulst, T. Maes, K. B. Moerloose, I. K. Demedts, S. Lebecque, G. F. Joos, and G. G. Brusselle. 2006. Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice. J. Immunol. 177: 4350-4359.
20. Song, K. S., W. J. Lee, K. C. Chung, J. S. Koo, E. J. Yang, J. Y. Choi, and J. H. Yoon. 2003. 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. 278: 23243-23250.
21. Chen, Y., Y. H. Zhao, and R. Wu. 2001. Differential regulation of airway mucin gene expression and mucin secretion by extracellular nucleotide triphosphates. Am. J. Respir. Cell Mol. Biol. 25: 409-417.
22. Shao, M. X., T. Nakanaga, and J. A. Nadel. 2004. Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-alpha-converting enzyme in human airway epithelial (NCI-H292) cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L420-L427.
23. Greaves, D. R., W. Wang, D. J. Dairaghi, M. C. Dieu, B. Saint-Vis, K. Franz-Bacon, D. Rossi, C. Caux, T. McClanahan, S. Gordon, et al. 1997. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J. Exp. Med. 186: 837-844.
24. Keates, S., X. Han, C. P. Kelly, and A. C. Keates. 2007. Macrophageinflammatory protein-3alpha mediates epidermal growth factor receptor transactivation and ERK1/2 MAPK signaling in Caco-2 colonic epithelial cells via metalloproteinase-dependent release of amphiregulin. J. Immunol. 178: 8013-8021.
25. Nadel, J. A. 2007. Innate immune mucin production via epithelial cell surface signaling: relationship to allergic disease. Curr. Opin. Allergy Clin. Immunol. 7: 57-62.
26. Rose, M. C., and J. A. Voynow. 2006. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev. 86: 245-278.
27. Vroling, A. B., M. J. Jonker, T. M. Breit, W. J. Fokkens, and C. M. van Drunen. 2008. Comparison of expression profiles induced by dust mite in airway epithelia reveals a common pathway. Allergy 63: 461-467. (Pubitemid 351341825)
28. Burgel, P. R., S. C. Lazarus, D. C. Tam, I. F. Ueki, K. Atabai, M. Birch, and J. A. Nadel. 2001. Human eosinophils induce mucin production in airway epithelial cells via epidermal growth factor receptor activation. J. Immunol. 167: 5948-5954.
29. Shao, M. X., and J. A. Nadel. 2005. Neutrophil elastase induces MUC5AC mucin production in human airway epithelial cells via a cascade involving protein kinase C, reactive oxygen species, and TNF-alpha-converting enzyme. J. Immunol. 175: 4009-4016.
30. Kim, S., A. J. Schein, and J. A. Nadel. 2005. E-cadherin promotes EGFR-mediated cell differentiation and MUC5AC mucin expression in cultured human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L1049-L1060.
31. Polosa, R., G. Prosperini, S. H. Leir, S. T. Holgate, P. M. Lackie, and D. E. Davies. 1999. Expression of c-erbB receptors and ligands in human bronchial mucosa. Am. J. Respir. Cell Mol. Biol. 20: 914-923.
32. Longphre, M., D. Li, M. Gallup, E. Drori, C. L. Ordoñez, T. Redman, S. Wenzel, D. E. Bice, J. V. Fahy, and C. Basbaum. 1999. Allergen-induced IL-9 directly stimulates mucin transcription in respiratory epithelial cells. J. Clin. Invest. 104: 1375-1382.
33. Aarbiou, J., R. M. Verhoosel, S. Van Wetering, W. I. De Boer, J. H. Van Krieken, S. V. Litvinov, K. F. Rabe, and P. S. Hiemstra. 2004. Neutrophil defensins enhance lung epithelial wound closure and mucin gene expression in vitro. Am. J. Respir. Cell Mol. Biol. 30: 193-201.
34. Kim, S., and J. A. Nadel. 2009. Fibrinogen binding to ICAM-1 promotes EGFR-dependent mucin production in human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 297: L174-L183.
35. Zhang, Z., P. Oliver, J. R. Lancaster, Jr., P. O. Schwarzenberger, M. S. Joshi, J. Cork, and J. K. Kolls. 2001. Reactive oxygen species mediate tumor necrosis factor alpha-converting, enzyme-dependent ectodomain shedding induced by phorbol myristate acetate. FASEB J. 15: 303-305.
36. Fan, H., and R. Derynck. 1999. Ectodomain shedding of TGF-alpha and other transmembrane proteins is induced by receptor tyrosine kinase activation and MAP kinase signaling cascades. EMBO J. 18: 6962-6972. (Pubitemid 30000449)
37. Baselga, J., J. Mendelsohn, Y. M. Kim, and A. Pandiella. 1996. Autocrine regulation of membrane transforming growth factor-alpha cleavage. J. Biol. Chem. 271: 3279-3284.
38. Yang, C. C., H. Ogawa, M. B. Dwinell, D. F. McCole, L. Eckmann, and M. F. Kagnoff. 2005. Chemokine receptor CCR6 transduces signals that activate p130Cas and alter cAMP-stimulated ion transport in human intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 288: C321-C328.
39. Perrais, M., P. Pigny, M. C. Copin, J. P. Aubert, and I. Van Seuningen. 2002. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J. Biol. Chem. 277: 32258-32267.
40. Peschon, J. J., J. L. Slack, P. Reddy, K. L. Stocking, S. W. Sunnarborg, D. C. Lee, W. E. Russell, B. J. Castner, R. S. Johnson, J. N. Fitzner, et al. 1998. An essential role for ectodomain shedding in mammalian development. Science 282: 1281-1284. (Pubitemid 28524483)
41. Kim, J. H., S. Y. Lee, S. M. Bak, I. B. Suh, S. Y. Lee, C. Shin, J. J. Shim, K. H. In, K. H. Kang, and S. H. Yoo. 2004. Effects of matrix metalloproteinase inhibitor on LPS-induced goblet cell metaplasia. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L127-L133.
42. Kallal, L. E., M. A. Schaller, D. M. Lindell, S. A. Lira, and N. W. Lukacs. 2010. CCL20/CCR6 blockade enhances immunity to RSV by impairing recruitment of DC. Eur. J. Immunol. 40: 1042-1052.
43. Takeyama, K., J. V. Fahy, and J. A. Nadel. 2001. Relationship of epidermal growth factor receptors to goblet cell production in human bronchi. Am. J. Respir. Crit. Care Med. 163: 511-516.
44. O'Donnell, R. A., A. Richter, J. Ward, G. Angco, A. Mehta, K. Rousseau, D. M. Swallow, S. T. Holgate, R. Djukanovic, D. E. Davies, and S. J. Wilson. 2004. Expression of ErbB receptors and mucins in the airways of long term current smokers. Thorax 59: 1032-1040.
45. Izadpanah, A., M. B. Dwinell, L. Eckmann, N. M. Varki, and M. F. Kagnoff. 2001. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G710-G719.
46. Ben-Baruch, A., D. F. Michiel, and J. J. Oppenheim. 1995. Signals and receptors involved in recruitment of inflammatory cells. J. Biol. Chem. 270: 11703-11706.
47. Fujiie, S., K. Hieshima, D. Izawa, T. Nakayama, R. Fujisawa, H. Ohyanagi, and O. Yoshie. 2001. Proinflammatory cytokines induce liver and activation-regulated chemokine/macrophage inflammatory protein-3alpha/CCL20 in mucosal epithelial cells through NF-kappaB [correction of NK-kappaB]. Int. Immunol. 13: 1255-1263. (Pubitemid 32994525)
48. Kwon, J. H., S. Keates, S. Simeonidis, F. Grall, T. A. Libermann, and A. C. Keates. 2003. ESE-1, an enterocyte-specific Ets transcription factor, regulates MIP-3alpha gene expression in Caco-2 human colonic epithelial cells. J. Biol. Chem. 278: 875-884.
49. Liao, F., R. L. Rabin, C. S. Smith, G. Sharma, T. B. Nutman, and J. M. Farber. 1999. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J. Immunol. 162: 186-194.
50. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Aït-Yahia, F. Brière, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188: 373-386.
51. Lukacs, N. W., D. M. Prosser, M. Wiekowski, S. A. Lira, and D. N. Cook. 2001. Requirement for the chemokine receptor CCR6 in allergic pulmonary inflammation. J. Exp. Med. 194: 551-555.
52. Scapini, P., C. Laudanna, C. Pinardi, P. Allavena, A. Mantovani, S. Sozzani, and M. A. Cassatella. 2001. Neutrophils produce biologically active macrophage inflammatory protein-3alpha (MIP-3alpha)/CCL20 and MIP-3beta/CCL19. Eur. J. Immunol. 31: 1981-1988.
53. Kwon, J. H., S. Keates, L. Bassani, L. F. Mayer, and A. C. Keates. 2002. Colonic epithelial cells are a major site of macrophage inflammatory protein 3alpha (MIP-3alpha) production in normal colon and inflammatory bowel disease. Gut 51: 818-826.
54. Kaser, A., O. Ludwiczek, S. Holzmann, A. R. Moschen, G. Weiss, B. Enrich, I. Graziadei, S. Dunzendorfer, C. J.Wiedermann, E. Mürzl, et al. 2004. Increased expression of CCL20 in human inflammatory bowel disease. J. Clin. Immunol. 24: 74-85.
55. Puleston, J., M. Cooper, S. Murch, K. Bid, S. Makh, P. Ashwood, A. H. Bingham, H. Green, P. Moss, A. Dhillon, et al. 2005. A distinct subset of chemokines dominates the mucosal chemokine response in inflammatory bowel disease. Aliment. Pharmacol. Ther. 21: 109-120.
56. Finzi, L., M. X. Shao, F. Paye, C. Housset, and J. A. Nadel. 2009. Lipopolysaccharide initiates a positive feedback of epidermal growth factor receptor signaling by prostaglandin E2 in human biliary carcinoma cells. J. Immunol. 182: 2269-2276.