Homeostatic control of conjunctival mucosal goblet cells by NKT-derived IL-13

Mucosal Immunology

Volumn 4, Issue 4, 2011, Pages 397-408

  De Paiva, C S ^a   Raince, J K ^a   McClellan, A J ^a   Shanmugam, K P ^a   Pangelinan, S B ^a   Volpe, E A ^a   Corrales, R M ^a   Farley, W J ^a   Corry, D B ^b   Li, D Q ^a   Pflugfelder, S C ^a  

^a CULLEN EYE INSTITUTE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1 ANTIGEN; CYCLOSPORIN A; GAMMA INTERFERON; INTERLEUKIN 13; MESSENGER RNA; RAG1 PROTEIN; SCHIFF BASE; STAT6 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL ISOLATION; CELL SURFACE; CELL TYPE; CELLULAR STRESS RESPONSE; CONJUNCTIVA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DESICCATION; FEMALE; GENE EXPRESSION PROFILING; GENE LOCATION; GOBLET CELL; HOMEOSTASIS; KNOCKOUT GENE; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MALE; MOUSE; MUCOSAL IMMUNITY; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T CELL DEPLETION; WILD TYPE;

EID: 79959452051     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2010.82     Document Type: Article

References (72)

1. Nakamura, T., Nishida, K., Dota, A., Matsuki, M., Yamanishi, K. & Kinoshita, S. Elevated expression of transglutaminase 1 and keratinization- related proteins in conjunctiva in severe ocular surface disease. Invest. Ophthalmol. Vis. Sci. 42, 549-556 (2001) (Pubitemid 32206891)
2. Pflugfelder, S. C., Tseng, S. C. G., Yoshino, K., Monroy, D., Felix, C. & Reis, B. L. Correlation of goblet cell density and mucosal epithelial membrane mucin expression with rose bengal staining in patients with ocular irritation. Ophthalmology 104, 223-235 (1997). (Pubitemid 27088097)
3. Shahzeidi, S., Aujla, P. K., Nickola, T. J., Chen, Y., Alimam, M. Z. & Rose, M. C. Temporal analysis of goblet cells and mucin gene expression in murine models of allergic asthma. Exp. Lung Res. 29, 549-565 (2003) (Pubitemid 37463927)
4. Shim, J. J. et al. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils. Am. J. Physiol. Lung Cell Mol. Physiol. 280, L134-L140 (2001).
5. Kondo, M. et al. Elimination of IL-13 reverses established goblet cell metaplasia into ciliated epithelia in airway epithelial cell culture. Allergol. Int. 55, 329-336 (2006). (Pubitemid 44433603)
6. McDermott, J. R., Humphreys, N. E., Forman, S. P., Donaldson, D. D. & Grencis, R. K. Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J. Immunol. 175, 3207-3213 (2005) (Pubitemid 41170541)
7. Evans, C. M. & Koo, J. S. Airway mucus: the good, the bad, the sticky. Pharmacol. Ther. 121, 332-348 (2009)
8. Knop, N. & Knop, E. Conjunctiva-associated lymphoid tissue in the human eye. Invest. Ophthalmol. Vis. Sci. 41, 1270-1279 (2000) (Pubitemid 30261847)
9. Dua, H. S. et al. Mucosa specific lymphocytes in the human conjunctiva, corneoscleral limbus and lacrimal gland. Curr. Eye Res. 13, 87-93 (1994). (Pubitemid 24053158)
10. Dua, H. S., Gomes, J. A., Donoso, L. A. & Laibson, P. R. The ocular surface as part of the mucosal immune system: conjunctival mucosa-specific lymphocytes in ocular surface pathology. Eye (Lond). 9 (Pt 3), 261-267 (1995).
11. Bienenstock, J. & Befus, D. Gut-and bronchus-associated lymphoid tissue. Am. J. Anat. 170, 437-445 (1984)
12. Wotherspoon, A. C., Hardman-Lea, S. & Isaacson, P. G. Mucosa-associated lymphoid tissue (MALT) in the human conjunctiva. J. Pathol. 174, 33-37 (1994) (Pubitemid 24314862)
13. Chan, J. H., Amankwah, R., Robins, R. A., Gray T. & Dua, H. S. Kinetics of immune cell migration at the human ocular surface. Br. J. Ophthalmol. 92, 970-975 (2008) (Pubitemid 351969681)
14. Fuss, I. J. & Strober, W. The role of IL-13 and NK T cells in experimental and human ulcerative colitis. Mucosal. Immunol. 1 (Suppl 1), S31-S33 (2008).
15. Middendorp, S. & Nieuwenhuis, E. E. NKT cells in mucosal immunity. Mucosal Immunol. 2, 393-402 (2009)
16. Matangkasombut, P., Pichavant, M., Dekruyff, R. H. & Umetsu, D. T Natural killer T cells and the regulation of asthma. Mucosal Immunol. 2, 383-392 (2009)
17. Balato, A., Unutmaz, D. & Gaspari, A. A. Natural killer T cells: an unconventional T-cell subset with diverse effector and regulatory functions. J. Invest. Dermatol. 129, 1628-1642 (2009)
18. 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. 27, 536-541 (2002) (Pubitemid 35301807)
19. Laoukili, J. et al. IL-13 alters mucociliary differentiation and ciliary beating of human respiratory epithelial cells. J. Clin. Invest. 108, 1817-1824 (2001). (Pubitemid 34015127)
20. Walzer, T. et al. Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc. Natl. Acad. Sci. USA 104, 3384-3389 (2007). (Pubitemid 46364168)
21. Liu, Q. et al. IL-18 stimulates IL-13-mediated IFN-gamma-sensitive host resistance in vivo. Eur. J. Immunol. 36, 1187-1198 (2006)
22. Chen, H. & Paul, W. E. Cultured NK1.1+ CD4+ T cells produce large amounts of IL-4 and IFN-gamma upon activation by anti-CD3 or CD1 J. Immunol. 159, 2240-2249 (1997) (Pubitemid 127681014)
23. Beagley K. W. et al. Differences in intraepithelial lymphocyte T cell subsets isolated from murine small versus large intestine. J. Immunol. 154, 5611-5619 (1995).
24. Naiki, Y., Nishimura, H., Itohara, S. & Yoshikai, Y gammadelta T cells may dichotomously modulate infection with avirulent Salmonella choleraesuis via IFN-gamma and IL-13 in mice. Cell Immunol. 202, 61-69 (2000). (Pubitemid 30445647)
25. Park, S. W. et al. Interleukin-13 and its receptors in idiopathic interstitial pneumonia: clinical implications for lung function. J. Korean Med. Sci. 24, 614-620 (2009)
26. Arase, H., Saito, T., Phillips, J. H. & Lanier, L. L. Cutting edge: the mouse NK cell-associated antigen recognized by DX5 monoclonal antibody is CD49b (alpha 2 integrin, very late antigen-2). J. Immunol. 167, 1141-1144 (2001). (Pubitemid 32703106)
27. Niederkorn, J. Y. et al. Desiccating stress induces T cell-mediated Sjogren's syndrome-like lacrimal keratoconjunctivitis. J. Immunol. 176, 3950-3957 (2006). (Pubitemid 44264372)
28. de Paiva, C. S. et al. Apical corneal barrier disruption in experimental murine dry eye is abrogated by methylprednisolone and doxycycline. Invest. Ophthalmol. Vis. Sci. 47, 2847-2856 (2006). (Pubitemid 351639757)
29. de Paiva, C S. et al. Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp. Eye Res. 83, 526-535 (2006). (Pubitemid 43902774)
30. Luo, L., Li, D. Q., Doshi, A., Farley W., Corrales, R. M. & Pflugfelder, S. C. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest. Ophthalmol. Vis. Sci. 45, 4293-4301 (2004). (Pubitemid 39564653)
31. Pitcher, J. I. et al. Pharmacological cholinergic blockade stimulates inflammatory cytokine production in the mouse lacrimal gland. Invest. Ophthalmol. Vis. Sci. (in press) (2010).
32. De Paiva, C. S. et al. Dry eye-induced conjunctival epithelial squamous metaplasia is modulated by interferon-{gamma}. Invest. Ophthalmol. Vis. Sci. 48, 2553-2560 (2007). (Pubitemid 351261205)
33. De Paiva, C. S. et al. IL-17 disrupts corneal barrier following desiccating stress. Mucosal Immunol. 2, 243-253 (2009)
34. Sall, K., Stevenson, O. D., Mundorf, T. K. & Reis, B. L. Two multicenter, randomized studies of the efficacy and safety of cyclosporine ophthalmic emulsion in moderate to severe dry eye disease. CsA Phase 3 Study Group. Ophthalmology 107, 631-639 (2000). (Pubitemid 30191329)
35. Strong, B., Farley W., Stern, M. E. & Pflugfelder, S. C. Topical cyclosporine inhibits conjunctival epithelial apoptosis in experimental murine keratoconjunctivitis sicca. Cornea 24, 80-85 (2005). (Pubitemid 40053499)
36. Pangelinan, S. B. et al. Topical cyclosporine emulsion modulates immune response in experimental dry eye [abstr]. Invest. Ophthalmol. Vis. Sci. 49, 440 (2008).
37. Jiang, H., Harris, M. B. & Rothman, P. IL-4/IL-13 signaling beyond JAK/STAT J. Allergy Clin. Immunol. 105, 1063-1070 (2000). (Pubitemid 30418781)
38. Kaplan, M. H., Schindler, U., Smiley S. T. & Grusby M. J. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313-319 (1996) (Pubitemid 26132509)
39. Kuperman, D., Schofield, B., Wills-Karp, M. & Grusby M. J. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187, 939-948 (1998). (Pubitemid 28141667)
40. Akimoto, T. et al. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187, 1537-1542 (1998). (Pubitemid 28215412)
41. Corrales, R. M., Stern, M. E., de Paiva, C. S., Welch, J., Li, D. Q. & Pflugfelder, S. C. Desiccating stress stimulates expression of matrix metalloproteinases by the corneal epithelium. Invest. Ophthalmol. Vis. Sci. 47, 3293-3302 (2006) (Pubitemid 351639689)
42. Muhlen, K. A. et al. NK cells, but not NKT cells, are involved in Pseudomonas aeruginosa exotoxin A-induced hepatotoxicity in mice. J. Immunol. 172, 3034-3041 (2004) (Pubitemid 38263692)
43. Hazlett, L. D., Li, Q., Liu, J., McClellan, S., Du, W. & Barrett, R. P. NKT cells are critical to initiate an inflammatory response after Pseudomonas aeruginosa ocular infection in susceptible mice. J. Immunol. 179, 1138-1146 (2007).
44. Sentman, C. L., Kumar, V., Koo, G. & Bennett, M. Effector cell expression of NK1.1, a murine natural killer cell-specific molecule, and ability of mice to reject bone marrow allografts. J. Immunol. 142, 1847-1853 (1989) (Pubitemid 19081532)
45. Andoniou, C. E. et al. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat. Immunol. 6, 1011-1019 (2005) (Pubitemid 41486186)
46. Koo, G. C., Dumont, F. J., Tutt, M., Hackett, J. Jr. & Kumar, V The NK-1.1(-) mouse: a model to study differentiation of murine NK cells. J. Immunol. 137, 3742-3747 (1986). (Pubitemid 17215295)
47. Mutalithas, K. et al. Bronchoalveolar lavage invariant natural killer T cells are not increased in asthma. J. Allergy Clin. Immunol. 119, 1274-1276 (2007). (Pubitemid 46654191)
48. Rock, M., Yoder, S., Hoskins, A., Ajayi, W. U., Sheller, J. R. & Dworski, R. Effect of allergen challenge on the percentage of natural killer T cells in patients with atopic asthma. Ann. Allergy Asthma Immunol. 102, 432-437 (2009).
49. Vijayanand, P. et al. Invariant natural killer T cells in asthma and chronic obstructive pulmonary disease. N. Engl. J. Med. 356, 1410-1422 (2007) (Pubitemid 46556326)
50. Brown, D. R. et al. Beta 2-microglobulin-dependent NK1.1+ T cells are not essential for T helper cell 2 immune responses. J. Exp. Med. 184, 1295-1304 (1996). (Pubitemid 26354685)
51. Zhang, Y, Rogers, K. H. & Lewis, D. B. Beta 2-microglobulin-dependent T cells are dispensable for allergen-induced T helper 2 responses. J. Exp. Med. 184, 1507-1512 (1996). (Pubitemid 26354705)
52. Korsgren, M. et al. Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J. Exp. Med. 189, 553-562 (1999) (Pubitemid 29187377)
53. Das, J. et al. Natural killer T cells and CD8+ T cells are dispensable for T cell-dependent allergic airway inflammation. Nat. Med. 12, 1345-1346 (2006). (Pubitemid 44924486)
54. Reyes, N. J., Mayhew, E., Chen, P. W. & Niederkorn, J. Y. NKT cells are necessary for maximal expression of allergic conjunctivitis1. Int. Immunol. 22, 627-636 (2010).
55. Kaviratne, M. et al. IL-13 activates a mechanism of tissue fibrosis that is completely TGF-beta independent. J. Immunol. 173, 4020-4029 (2004) (Pubitemid 39280766)
56. Saw, V P. et al. Conjunctival interleukin-13 expression in mucous membrane pemphigoid and functional effects of interleukin-13 on conjunctival fibroblasts in vitro. Am. J. Pathol. 175, 2406-2415 (2009).
57. Cohn, L., Homer, R. J., Marinov, A., Rankin, J. & Bottomly, K. Induction of airway mucus production by T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186, 1737-1747 (1997) (Pubitemid 27506286)
58. Temann, U. A. et al. A novel role for murine IL-4 in vivo: induction of MUC5AC gene expression and mucin hypersecretion. Am. J. Respir. Cell Mol. Biol. 16, 471-478 (1997)
59. Zhu, Z. et al. Pulmonary expression of interleukin-13 causes inflammation mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103, 779-788 (1999). (Pubitemid 29152623)
60. Roat, M. I., Ohji, M., Hunt, L. E. & Thoft, R. A. Conjunctival epithelial cell hypermitosis and goblet cell hyperplasia in atopic keratoconjunctivitis. Am. J. Ophthalmol. 116, 456-463 (1993). (Pubitemid 23299491)
61. Diebold, Y., Chen, L. L., Tepavcevic, V., Ferdman, D., Hodges, R. R. & Dartt, D. A. Lymphocytic infiltration and goblet cell marker alteration in the conjunctiva of the MRL/MpJ-Fas(lpr) mouse model of Sjogren's syndrome. Exp. Eye Res. 84, 500-512 (2007) (Pubitemid 46204692)
62. Jabs, D. A. et al. Autoimmune Th2-mediated dacryoadenitis in MRL/MpJ mice becomes Th1-mediated in IL-4 deficient MRL/MpJ mice. Invest Ophthalmol. Vis. Sci. 48, 5624-5629 (2007). (Pubitemid 351260864)
63. Jabs, D. A., Lee, B., Whittum-Hudson, J. A. & Prendergast, R. A. Th1 versus Th2 immune responses in autoimmune lacrimal gland disease in MRL/Mp mice. Invest. Ophthalmol. Vis. Sci. 41, 826-831 (2000) (Pubitemid 30158895)
64. Porter, P. et al. Link between allergic asthma and airway mucosal infection suggested by proteinase-secreting household fungi. Mucosal Immunol. 2, 504-517 (2009)
65. Ford, J. G. et al. Il-13 and IFN-gamma: interactions in lung inflammation J. Immunol. 167, 1769-1777 (2001). (Pubitemid 32703181)
66. Irifune, K. et al. Adoptive transfer of T-helper cell type 1 clones attenuates an asthmatic phenotype in mice. Eur. Respir. J. 25, 653-659 (2005) (Pubitemid 40528758)
67. Brookes, S. M. et al. T cell clones from a Sjogren's syndrome salivary gland biopsy produce high levels of IL-10. Clin. Exp. Immunol. 103; 268-272(1996).
68. Mitsias, D. I. et al. The Th1/Th2 cytokine balance changes with the progress of the immunopathological lesion of Sjogren's syndrome. Clin. Exp. Immunol. 128, 562-568 (2002). (Pubitemid 34639321)
69. Haider, A. S. et al. Identification of cellular pathways of " type 1, " Th17T cells, and TNF-and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J. Immunol. 180, 1913-1920 (2008).
70. Liu, X. et al. Inhibitory effect of Cyclosporin A and corticosteroids on the production of IFN-gamma and IL-17 by T cells in Vogt-Koyanagi-Harada syndrome. Clin. Immunol. 131, 333-342 (2009)
71. Zhang, C., Zhang, J., Yang, B. & Wu, C. Cyclosporin A inhibits the production of IL-17 by memory Th17 cells from healthy individuals and patients with rheumatoid arthritis. Cytokine 42, 345-352 (2008)
72. Chi, W. et al. Production of interleukin-17 in Behcet's disease is inhibited by cyclosporin A. Mol. Vis. 16, 880-886 (2010).