Innate immune mucin production via epithelial cell surface signaling: Relationship to allergic disease

Current Opinion in Allergy and Clinical Immunology

Volumn 7, Issue 1, 2007, Pages 57-62

  Nadel, Jay A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epidermal growth factor receptor activation; Epithelial surface signaling; Innate immunity; Mucus hypersecretion

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; METALLOPROTEINASE; MUCIN; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

AIRWAY OBSTRUCTION; ALLERGY; ASTHMA; AUTOCRINE EFFECT; BACTERICIDAL ACTIVITY; CELL SURFACE; CORRELATION ANALYSIS; ENZYME DEGRADATION; EPITHELIUM CELL; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; PARACRINE SIGNALING; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; EPITHELIAL CELLS; HUMANS; HYPERSENSITIVITY; IMMUNITY, NATURAL; MUCINS; SIGNAL TRANSDUCTION;

EID: 33846260489     PISSN: 15284050     EISSN: 14736322     Source Type: Journal    
DOI: 10.1097/ACI.0b013e328012ce22     Document Type: Review

References (57)

1. Zaas AK, Schwartz DA. Innate immunity and the lung: defense at the interface between host and environment. Trends Cardiovasc Med 2005; 15:195-202. Recent review focusing on lung epithelial cells and their cell surface receptors, and secreted molecules used in defense of the host against inhaled pathogens.
2. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 2002; 109:571-577.
3. Bals R, Hiemstra PS. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur Respir J 2004; 23:327-333.
4. Rogan MP, Geraghty P, Greene CM, et al. Antimicrobial proteins and polypeptides in pulmonary innate defence. Respir Res 2006; 7:29.
5. Widdicombe JG. Neurophysiology of the cough reflex. Eur Respir J 1995; 8:1193-1202.
6. Hamilton LM, Torres-Lozano C, Puddicombe SM, et al. The role of epidermal growth factor receptor in sustaining neutrophil inflammation in severe asthma. Clin Exp Allergy 2003; 33:233-240.
7. Richter A, O'Donnell RA, Powell RM, et al. Autocrine ligands for the epidermal growth factor receptor mediate interleukin-8 release from bronchial epithelial cells in response to cigarette smoke. Am J Respir Cell Mol Biol 2002; 27:85-90.
8. Takeyama K, Fahy JV, Nadel JA. Relationship of epidermal growth factor receptors to goblet cell production in human bronchi. Am J Respir Crit Care Med 2001; 163:511-516.
9. Kheradmand F, Folkesson HG, Shum L, et al. Transforming growth factoralpha enhances alveolar epithelial cell repair in a new in vitro model. Am J Physiol 1994; 267 (6 Pt 1):L728-L738.
10. Takeyama K, Dabbagh K, Lee HM, et al. Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 1999; 96:3081-3086.
11. Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 2006; 86:245-278. The authors provide an extensive, up-to-date review of airway mucin gene expression and mucin protein protection in both healthy humans and various diseases.
12. Desseyn JL, Aubert JP, Van Seuningen I, et al. Genomic organization of the 30 region of the human mucin gene MUC5B. J Biol Chem 1997; 272:16873-16883.
13. Gum JR Jr, Hicks JW, Toribara NW, et al. Molecular cloning of human intestinal mucin (MUC2) cDNA. Identification of the amino terminus and overall sequence similarity to prepro-von Willebrand factor. J Biol Chem 1994; 269:2440-2446.
14. Li D, Gallup M, Fan N, et al. Cloning of the amino-terminal and 50-flanking region of the human MUC5AC mucin gene and transcriptional up-regulation by bacterial exoproducts. J Biol Chem 1998; 273:6812-6820.
15. Meezaman D, Charles P, Daskal E, et al. Cloning and analysis of cDNA encoding a major airway glycoprotein, human tracheobronchial mucin (MUC5). J Biol Chem 1994; 269:12932-12939.
16. Harkema JR, Hotchkiss JA. Ozone- and endotoxin-induced mucous cell metaplasia in rat airway epithelium: novel animal models to study toxicant-induced epithelial transformation in airways. Toxicol Lett 1993; 68 (1-2):251-263.
17. Borchers MT, Wert SE, Leikauf GD. Acrolein-induced MUC5ac expression in rat airways. Am J Physiol 1998; 274 (4 Pt 1):L573-L581.
18. Longphre M, Li D, Gallup M, et al. Allergen-induced IL-9 directly stimulates mucin transcription in respiratory epithelial cells. J Clin Invest 1999; 104:1375-1382.
19. Kohri K, Ueki IF, Nadel J. Neutrophil elastase induces mucin production by ligand-dependent epidermal growth factor receptor activation. Am J Physiol Lung Cell Mol Physiol 2002; 283:L531-L540.
20. Voynow JA, Young LR, Wang Y, et al. Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells. Am J Physiol 1999; 276 (5 Pt 1):L835-L843.
21. Li JD, Feng W, Gallup M, et al. Activation of NF-kappaB via a Src-dependent Ras-MAPK-pp90rsk pathway is required for Pseudomonas aeruginosa-induced mucin overproduction in epithelial cells. Proc Natl Acad Sci USA 1998; 95:5718-5723.
22. Burgel PR, Nadel JA. Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 2004; 59:992-996.
23. Calafat J, Janssen H, Stahle-Backdahl M, et al. Human monocytes and neutrophils store transforming growth factor-alpha in a subpopulation of cytoplasmic granules. Blood 1997; 90:1255-1266.
24. Wong DT, Weller PF, Galli SJ, et al. Human eosinophils express transforming growth factor alpha. J Exp Med 1990; 172:673-681.
25. Daub H, Weiss FU, Wallasch C, et al. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 1996; 379: 557-560.
26. Dong J, Opresko LK, Dempsey PJ, et al. Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc Natl Acad Sci USA 1999; 96:6235-6240.
27. Prenzel N, Zwick E, Daub H, et al. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 1999; 402:884-888.
28. Kohri K, Ueki IF, Shim JJ, et al. Pseudomonas aeruginosa induces MUC5AC production via epidermal growth factor receptor. Eur Respir J 2002; 20:1263-1270.
29. Shao MX, Ueki IF, Nadel JA. Tumor necrosis factor alpha-converting enzyme mediates MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci USA 2003; 100:11618-11623.
30. Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 1997; 385:729-733.
31. Schlondorff J, Blobel CP. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci 1999; 112 (Pt 21):3603-3617.
32. Ordonez CL, Shaughnessy TE, Matthay MA, et al. Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma: Clinical and biologic significance. Am J Respir Crit Care Med 2000; 161 (4 Pt 1):1185-1190.
33. Lamblin C, Gosset P, Tillie-Leblond I, et al. Bronchial neutrophilia in patients with noninfectious status asthmaticus. Am J Respir Crit Care Med 1998; 157:397-402.
34. Wenzel SE, Szefler SJ, Leung DY, et al. Bronchoscopic evaluation of severe asthma. Persistent inflammation associated with high dose glucocorticoids. Am J Respir Crit Care Med 1997; 156 (3 Pt 1):737-743.
35. Shao MX, Nadel JA. 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 2005; 175:4009-4016. The authors describe a novel airway epithelial surface molecule, dual oxidase-1, that generate reactive oxygen species (ROS). They report that the released ROS activates a surface metalloprotease, tumor necrosis factor alpha-converting enzyme, which then cleaves and releases soluble epidermal growth factor receptor (EGFR) ligands. The released ligands bind to and activate EGFR, which produces a series of epithelial defensive signals that act in defense of the lungs.
36. Dempsey PJ, Garton K, Raines EW. Emerging roles of TACE as a key protease in ErbB ligand shedding. Mol Interv 2002; 2:136-141.
37. Proud D, Vio CP. Localization of immunoreactive tissue kallikrein in human trachea. Am J Respir Cell Mol Biol 1993; 8:16-19.
38. Casalino-Matsuda SM, Monzon ME, Forteza RM. Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am J Respir Cell Mol Biol 2006; 34:581-591. The authors describe an airway epithelial cascade whereby reactive oxygen species released from the epithelial cells stimulate apical xanthene/xanthine oxidase, causing hyaluronana depolymerization and activation of tissue kallikrein. Kallikrein enzymatically cleaves and releases epidermal growth factor (on epidermal growth factor receptor (EGFR) ligand), allowing epidermal growth factor to bind to and activate EGFR.
39. Arnold RS, Shi J, Murad E, et al. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci USA 2001; 98:5550-5555.
40. Zhang Z, Oliver P, Lancaster JR Jr, et al. Reactive oxygen species mediate tumor necrosis factor alpha-converting, enzyme-dependent ectodomain shedding induced by phorbol myristate acetate. FASEB J 2001; 15:303-305.
41. Shao MX, Nakanaga T, Nadel JA. 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 2004; 287:L420-L427.
42. De Deken X, Wang D, Many MC, et al. Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J Biol Chem 2000; 275:23227-23233.
43. Geiszt M, Witta J, Baffi J, et al. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J 2003; 17:1502-1504.
44. Shao MXG, Nadel JA. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci USA 2005; 102:767-772. This study expands the epidermal growth factor receptor surface signaling cascade and provides an important source of reactive oxygen species for epithelial cell signaling (and perhaps for other functions).
45. Schwarzer C, Machen TE, Illek B, et al. NADPH oxidase-dependent acid production in airway epithelial cells. J Biol Chem 2004; 279:36454-36461.
46. Dusser DJ, Djokic TD, Borson DB, et al. Cigarette smoke induces bronchoconstrictor hyperresponsiveness to substance P and inactivates airway neutral endopeptidase in the guinea pig. Possible role of free radicals. J Clin Invest 1989; 84:900-906.
47. Koff JL, Shao MX, Kim S, et al. Pseudomonas LPS accelerates wound repair via activation of a novel epithelial cell signaling cascade. J Immunol 2006 (in press).
48. Finzi L, Barbu V, Burgel PR, et al.MUC5AC, a gel-forming mucin accumulating in gallstone disease, is overproduced via an EGF-R pathway in the human gallbladder. Am J Pathol 2006 (in press).
49. Openshaw PJ, Turner-Warwick M. Observations on sputum production in patients with variable airflow obstruction; implications for the diagnosis of asthma and chronic bronchitis. Respir Med 1989; 83:25-31.
50. Lange P, Parner J, Vestbo J, et al. A 15-year follow-up study of ventilatory function in adults with asthma. N Engl J Med 1998; 339:1194-1200.
51. Ordonez CL, Khashayer R, Wong HH, et al. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am J Respir Crit Care Med 2001; 163:517-523.
52. Cardell BS, Pearson RS. Death in asthmatics. Thorax 1959; 14:341-352.
53. Aikawa T, Shimura S, Sasaki H, et al. Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack. Chest 1992; 101:916-921.
54. Carroll N, Elliot J, Morton A, et al. The structure of large and small airways in nonfatal and fatal asthma. Am Rev Respir Dis 1993; 147: 405-410.
55. Dunnill MS. The pathology of asthma, with special reference to changes in the bronchial mucosa. J Clin Pathol 1960; 13:27-33.
56. Rankin JA, Picarella DE, Geba GP, et al. Phenotypic and physiologic characterization of transgenic mice expressing interleukin 4 in the lung: lymphocytic and eosinophilic inflammation without airway hyperreactivity. Proc Natl Acad Sci USA 1996; 93:7821-7825.
57. Shim JJ, Dabbagh K, Ueki IF, et al. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils. Am J Physiol Lung Cell Mol Physiol 2001; 280:L134-L140.