IL-13 stimulates proliferation and expression of mucin and immunomodulatory genes in cultured conjunctival goblet cells

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 8, 2015, Pages 4186-4197

  Henriksson, Johanna Tukler ^a   Coursey, Terry G ^a   Corry, David B ^a   De Paiva, Cintia S ^a   Pflugfelder, Stephen C ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cell culture; Conjunctiva; Goblet cells; Interleukin 13

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CYTOKERATIN 7; EOTAXIN 3; EPIDERMAL GROWTH FACTOR; FAS LIGAND; INTERLEUKIN 13; MUCIN; MESSENGER RNA; MUC5AC PROTEIN, MOUSE; MUCIN 5AC;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CONJUNCTIVA EPITHELIUM; CONTROLLED STUDY; DOT HYBRIDIZATION; FEMALE; GOBLET CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TH2 CELL; WESTERN BLOTTING; YOUNG ADULT; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CONJUNCTIVA; DRY EYE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CONJUNCTIVA; DRY EYE SYNDROMES; FEMALE; GENE EXPRESSION REGULATION; GOBLET CELLS; INTERLEUKIN-13; MICE; MICE, INBRED C57BL; MUCIN 5AC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84939614676     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-15496     Document Type: Article

References (64)

1. Watsky MA, Jablonski MM, Edelhauser HF. Comparison of conjunctival and corneal surface areas in rabbit and human. Curr Eye Res. 1988;7:483–486
2. Govindarajan B, Gipson IK. Membrane-tethered mucins have multiple functions on the ocular surface. Exp Eye Res. 2010; 90:655–663
3. Gipson IK. Distribution of mucins at the ocular surface. Exp Eye Res. 2004;78:379–388
4. Zhang X, Volpe EA, Gandhi NB, et al. NK cells promote Th-17 mediated corneal barrier disruption in dry eye. PLoS One. 2012;7:e36822
5. Pflugfelder SC, Tseng SCG, Yoshino K, Monroy D, Felix C, Reis BL. Correlation of goblet cell density and mucosal epithelial membrane mucin expression with rose bengal staining in patients with ocular irritation. Ophthalmology. 1997;104:223–235
6. Pflugfelder SC, Corrales RM, de Paiva CS. T helper cytokines in dry eye disease. Exp Eye Res. 2013;117:118–125
7. Roat MI, Ohji M, Hunt LE, Thoft RA. Conjunctival epithelial cell hypermitosis and goblet cell hyperplasia in atopic keratoconjunctivitis. Am J Ophthalmol. 1993;116:456–463
8. Aragona P, Romeo GF, Puzzolo D, Micali A, Ferreri G. Impression cytology of the conjunctival epithelium in patients with vernal conjunctivitis. Eye (Lond). 1996;10(pt 1):82–85
9. Mannon P, Reinisch W. Interleukin 13 and its role in gut defence and inflammation. Postgrad Med J. 2013;89:448–456
10. Laoukili J, Perret E, Willems T, et al. IL-13 alters mucociliary differentiation and ciliary beating of human respiratory epithelial cells. J Clin Invest. 2001;108:1817–1824
11. Wu D, Ahrens R, Osterfeld H, et al. Interleukin-13 (IL-13)/IL-13 receptor alpha1 (IL-13Ralpha1) signaling regulates intestinal epithelial cystic fibrosis transmembrane conductance regulator channel-dependent Cl- secretion. J Biol Chem. 2011;286: 13357–13369
12. Kondo M, Tamaoki J, Takeyama K, et al. Elimination of IL-13 reverses established goblet cell metaplasia into ciliated epithelia in airway epithelial cell culture. Allergol Int. 2006; 55:329–336
13. Mannon P, Reinisch W. Interleukin 13 and its role in gut defence and inflammation. Postgrad Med J. 2013;89:448–456
14. Hershey GK. IL-13 receptors and signaling pathways: an evolving web. J Allergy Clin Immunol. 2003;111:677–690
15. Kasaian MT, Raible D, Marquette K, et al. IL-13 antibodies influence IL-13 clearance in humans by modulating scavenger activity of IL-13Ralpha2. J Immunol. 2011;187:561–569
16. Zhang JG, Hilton DJ, Willson TA, et al. Identification, purification, and characterization of a soluble interleukin (IL)-13-binding protein. Evidence that it is distinct from the cloned Il-13 receptor and Il-4 receptor alpha-chains. J Biol Chem. 1997;272:9474–9480
17. Lam H, Bleiden L, de Paiva CS, Farley W, Stern ME, Pflugfelder SC. Tear cytokine profiles in dysfunctional tear syndrome. Am J Ophthalmol. 2009;147:198–205
18. de Paiva CS, Raince JK, McClellan AJ, et al. Homeostatic control of conjunctival mucosal goblet cells by NKT-derived IL- 13. Mucosal Immunol. 2011;4:397–408
19. Contreras-Ruiz L, Ghosh-Mitra A, Shatos MA, Dartt DA, Masli S. Modulation of conjunctival goblet cell function by inflammatory cytokines. Mediators Inflamm. 2013;2013:636812
20. Songhet P, Barthel M, Stecher B, et al. Stromal IFN-gammaRsignaling modulates goblet cell function during Salmonella Typhimurium infection. PLoS One. 2011;6:e22459
21. Shatos MA, Rios JD, Tepavcevic V, Kano H, Hodges R, Dartt DA. Isolation, characterization, and propagation of rat conjunctival goblet cells in vitro. Invest Ophthalmol Vis Sci. 2001;42:1455–1464
22. Shatos MA, Rios JD, Horikawa Y, et al. Isolation and characterization of cultured human conjunctival goblet cells. Invest Ophthalmol Vis Sci. 2003;44:2477–2486
23. Kondo M, Tamaoki J, Takeyama K, Nakata J, Nagai A. Interleukin-13 induces goblet cell differentiation in primary cell culture from Guinea pig tracheal epithelium. Am J Respir Cell Mol Biol. 2002;27:536–541
24. Laoukili J, Perret E, Willems T, et al. IL-13 alters mucociliary differentiation and ciliary beating of human respiratory epithelial cells. J Clin Invest. 2001;108:1817–1824
25. Daugherty BL, Siciliano SJ, DeMartino JA, Malkowitz L, Sirotina A, Springer MS. Cloning, expression, and characterization of the human eosinophil eotaxin receptor. J Exp Med. 1996;183: 2349–2354
26. Sallusto F, Mackay CR, Lanzavecchia A. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science. 1997;277:2005–2007
27. Niess JH, Brand S, Gu X, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005;307:254–258
28. Banwell ME, Tolley NS, Williams TJ, Mitchell TJ. Regulation of human eotaxin-3/CCL26 expression: modulation by cytokines and glucocorticoids. Cytokine. 2002;17:317–323
29. Leverkoehne I, Gruber AD. The murine mCLCA3 (alias gob-5) protein is located in the mucin granule membranes of intestinal, respiratory, and uterine goblet cells. J Histochem Cytochem. 2002;50:829–838
30. Long AJ, Sypek JP, Askew R, et al. Gob-5 contributes to goblet cell hyperplasia and modulates pulmonary tissue inflammation. Am J Respir Cell Mol Biol. 2006;35:357–365
31. Kondo M, Nakata J, Arai N, et al. Niflumic acid inhibits goblet cell degranulation in a guinea pig asthma model. Allergol Int. 2012;61:133–142
32. Long AJ, Sypek JP, Askew R, et al. Gob-5 contributes to goblet cell hyperplasia and modulates pulmonary tissue inflammation. Am J Respir Cell Mol Biol. 2006;35:357–365
33. Lee CG, Homer RJ, Cohn L, et al. Transgenic overexpression of interleukin (IL)-10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and -independent pathways. J Biol Chem. 2002;277:35466–35474
34. Zhou Y, Dong Q, Louahed J, et al. Characterization of a calcium-activated chloride channel as a shared target of Th2 cytokine pathways and its potential involvement in asthma. Am J Respir Cell Mol Biol. 2001;25:486–491
35. Vignola AM, Chanez P, Chiappara G, et al. Evaluation of apoptosis of eosinophils, macrophages, and T lymphocytes in mucosal biopsy specimens of patients with asthma and chronic bronchitis. J Allergy Clin Immunol. 1999;103:563–573
36. Wadsworth SJ, Atsuta R, McIntyre JO, Hackett TL, Singhera GK, Dorscheid DR. IL-13 and TH2 cytokine exposure triggers matrix metalloproteinase 7-mediated Fas ligand cleavage from bronchial epithelial cells. J Allergy Clin Immunol. 2010;126: 366–374, 374
37. Druilhe A, Wallaert B, Tsicopoulos A, et al. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am J Respir Cell Mol Biol. 1998;19:747–757
38. Jayaraman S, Castro M, O’Sullivan M, Bragdon MJ, Holtzman MJ. Resistance to Fas-mediated T cell apoptosis in asthma. J Immunol. 1999;162:1717–1722
39. Younes M, Lechago J, Ertan A, Finnie D, Younes A. Decreased expression of Fas (CD95/APO1) associated with goblet cell metaplasia in Barrett’s esophagus. Hum Pathol. 2000;31:434–438
40. Watanabe N, Arase H, Kurasawa K, et al. Th1 and Th2 subsets equally undergo Fas-dependent and -independent activationinduced cell death. Eur J Immunol. 1997;27:1858–1864
41. Hahn S, Stalder T, Wernli M, et al. Down-modulation of CD4þT helper type 2 and type 0 cells by T helper type 1 cells via Fas/ Fas-ligand interaction. Eur J Immunol. 1995;25:2679–2685
42. Druilhe A, Wallaert B, Tsicopoulos A, et al. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am J Respir Cell Mol Biol. 1998;19:747–757
43. Zhang X, de Paiva CS, Su Z, Volpe EA, Li DQ, Pflugfelder SC. Topical interferon-gamma neutralization prevents conjunctival goblet cell loss in experimental murine dry eye. Exp Eye Res. 2014;118:117–124
44. Taupin D, Podolsky DK. Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol. 2003;4:721–732
45. Kjellev S. The trefoil factor family—small peptides with multiple functionalities. Cell Mol Life Sci. 2009;66:1350–1369
46. Albert TK, Laubinger W, Muller S, et al. Human intestinal TFF3 forms disulfide-linked heteromers with the mucus-associated FCGBP protein and is released by hydrogen sulfide. J Proteome Res. 2010;9:3108–3117
47. Kindon H, Pothoulakis C, Thim L, Lynch-Devaney K, Podolsky DK. Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein. Gastroenterology. 1995;109:516–523
48. Schulze U, Hampel U, Sel S, et al. Trefoil factor family peptide 3 (TFF3) is upregulated under experimental conditions similar to dry eye disease and supports corneal wound healing effects in vitro. Invest Ophthalmol Vis Sci. 2014;55:3037–3042
49. Krimi RB, Kotelevets L, Dubuquoy L, et al. Resistin-like molecule beta regulates intestinal mucous secretion and curtails TNBS-induced colitis in mice. Inflamm Bowel Dis. 2008;14:931–941
50. Nair MG, Guild KJ, Du Y, et al. Goblet cell-derived resistin-like molecule beta augments CD4þ T cell production of IFNgamma and infection-induced intestinal inflammation. J Immunol. 2008;181:4709–4715
51. Marko CK, Menon BB, Chen G, Whitsett JA, Clevers H, Gipson IK. SPDEF null mice lack conjunctival goblet cells and provide a model of dry eye. Am J Pathol. 2013;183:35–48
52. Turner J, Jones CE. Regulation of mucin expression in respiratory diseases. Biochem Soc Trans. 2009;37:877–881
53. Wan H, Kaestner KH, Ang SL, et al. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development. 2004;131:953–964
54. Zhen G, Park SW, Nguyenvu LT, et al. IL-13 and epidermal growth factor receptor have critical but distinct roles in epithelial cell mucin production. Am J Respir Cell Mol Biol. 2007;36:244–253
55. McKenzie RW, Jumblatt JE, Jumblatt MM. Quantification of MUC2 and MUC5AC transcripts in human conjunctiva. Invest Ophthalmol Vis Sci. 2000;41:703–708
56. Corrales RM, Calonge M, Herreras JM, Saez V, Chaves FJ. Human epithelium from conjunctival impression cytology expresses MUC7 mucin gene. Cornea. 2003;22:665–671
57. Spurr-Michaud S, Argueso P, Gipson I. Assay of mucins in human tear fluid. Exp Eye Res. 2007;84:939–950
58. Corrales RM, Narayanan S, Fernandez I, et al. Ocular mucin gene expression levels as biomarkers for the diagnosis of dry eye syndrome. Invest Ophthalmol Vis Sci. 2011;52:8363–8369
59. Berry M, Ellingham RB, Corfield AP. Human preocular mucins reflect changes in surface physiology. Br J Ophthalmol. 2004; 88:377–383
60. Dogru M, Okada N, Asano-Kato N, et al. Alterations of the ocular surface epithelial mucins 1, 2, 4 and the tear functions in patients with atopic keratoconjunctivitis. Clin Exp Allergy. 2006;36:1556–1565
61. Leonardi A, Curnow SJ, Zhan H, Calder VL. Multiple cytokines in human tear specimens in seasonal and chronic allergic eye disease and in conjunctival fibroblast cultures. Clin Exp Allergy. 2006;36:777–784
62. Yoshisue H, Hasegawa K. Effect of MMP/ADAM inhibitors on goblet cell hyperplasia in cultured human bronchial epithelial cells. Biosci Biotechnol Biochem. 2004;68:2024–2031
63. Iwashita J, Sato Y, Sugaya H, Takahashi N, Sasaki H, Abe T. mRNA of MUC2 is stimulated by IL-4, IL-13 or TNF-alpha through a mitogen-activated protein kinase pathway in human colon cancer cells. Immunol Cell Biol. 2003;81:275–282
64. Shan M, Gentile M, Yeiser JR, et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science. 2013;342:447–453.