Suppression of Toll-like receptor-mediated innate immune responses at the ocular surface by the membrane-associated mucins MUC1 and MUC16

Mucosal Immunology

Volumn 8, Issue 5, 2015, Pages 1000-1008

  Menon, B B ^a   Kaiser Marko, C ^a   Spurr Michaud, S ^a   Tisdale, A S ^a   Gipson, I K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; INTERLEUKIN 6; INTERLEUKIN 8; MUCIN; MUCIN 1; MUCIN 16; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CA 125 ANTIGEN; CYTOKINE; MEMBRANE PROTEIN; MUC1 PROTEIN, HUMAN; MUC1 PROTEIN, MOUSE; MUC16 PROTEIN, HUMAN; MUC16 PROTEIN, MOUSE; TLR2 PROTEIN, HUMAN; TLR2 PROTEIN, MOUSE; TLR5 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CORNEA EPITHELIUM; CYTOKINE RELEASE; ENUCLEATION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOREGULATION; IN VITRO STUDY; INNATE IMMUNITY; KNOCKOUT MOUSE; LISTERIA MONOCYTOGENES; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE MOUSE; ANIMAL; CONJUNCTIVA; CORNEA; GENETICS; IMMUNOLOGY; MICROBIOLOGY; TRANSFORMED CELL LINE;

ANIMALS; CA-125 ANTIGEN; CELL LINE, TRANSFORMED; CONJUNCTIVA; CORNEA; CYTOKINES; HUMANS; IMMUNITY, INNATE; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUCIN-1; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 5;

EID: 84939555672     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.127     Document Type: Article

References (58)

1. Perez-Vilar, J. & Hill, R.L. The structure and assembly of secreted mucins. J. Biol. Chem. 274, 31751-31754 (1999).
2. Kufe, D.W. Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 9, 874-885 (2009).
3. Hattrup, C.L. & Gendler, S.J. Structure and function of the cell surface (tethered) mucins. Ann. Rev. Physiol. 70, 431-457 (2008).
4. Bafna, S., Kaur, S. & Batra, S.K. Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29, 2893-2904 (2010).
5. Senapati, S., Das, S. & Batra, S.K. Mucin-interacting proteins: from function to therapeutics. Trends Biochem. Sci. 35, 236-245 (2010).
6. Govindarajan, B. & Gipson, I.K. Membrane-tethered mucins have multiple functions on the ocular surface. Exp. Eye Res. 90, 655-663 (2010).
7. Gipson, I.K. Distribution of mucins at the ocular surface. Exp. Eye Res. 78, 379-388 (2004).
8. Blalock, T.D. et al. Functions of MUC16 in corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 48, 4509-4518 (2007).
9. Gipson, I.K., Spurr-Michaud, S., Tisdale, A. & Menon, B.B. Comparison of the transmembrane mucins MUC1 and MUC16 in epithelial barrier function. PLoS One 9, e100393 (2014).
10. Keogh, B. & Parker, A.E. Toll-like receptors as targets for immune disorders. Trends Pharmacol. Sci. 32, 435-442 (2011).
11. Kumar, A., Zhang, J. & Yu, F.-S.X. Toll-like receptor 2-mediated expression of b-defensin-2 in human corneal epithelial cells. Microbes Infect. 8, 380-389 (2006).
12. Kumar, A., Zhang, J. & Yu, F.S. Toll-like receptor 3 agonist poly(I:C)-induced antiviral response in human corneal epithelial cells. Immunology 117, 11-21 (2006).
13. Huang, X., Du, W., McClellan, S.A., Barrett, R.P. & Hazlett, L.D. TLR4 is required for host resistance in Pseudomonas aeruginosa keratitis. Invest. Ophthalmol. Vis. Sci. 47, 4910-4916 (2006).
14. Johnson, A.C. et al. Activation of toll-like receptor (TLR)2, TLR4, and TLR9 in the mammalian cornea induces MyD88-dependent corneal inflammation. Invest. Ophthalmol. Vis. Sci. 46, 589-595 (2005).
15. Redfern, R.L., Reins, R.Y. & McDermott, A.M. Toll-like receptor activation modulates antimicrobial peptide expression by ocular surface cells. Exp. Eye Res. 92, 209-220 (2011).
16. Ueta, M. et al. Intracellularly expressed TLR2s and TLR4s contribution to an immunosilent environment at the ocular mucosal epithelium. J. Immunol. 173, 3337-3347 (2004).
17. Ueta, M., Hamuro, J., Kiyono, H. & Kinoshita, S. Triggering of TLR3 by polyI:C in human corneal epithelial cells to induce inflammatory cytokines. Biochem. Biophys. Res. Commun. 331, 285-294 (2005).
18. Redfern, R.L. & McDermott, A.M. Toll-like receptors in ocular surface disease. Exp. Eye Res. 90, 679-687 (2010).
19. Yu, F.-S.X. & Hazlett, L.D. Toll-like receptors and the eye. Invest. Ophthalmol. Vis. Sci. 47, 1255-1263 (2006).
20. Ueno, K. et al. MUC1 mucin is a negative regulator of toll-like receptor signaling. Am. J. Respir. Cell Mol. Biol. 38, 263-268 (2008).
21. Sheng, Y.H. et al. MUC1 and MUC13 differentially regulate epithelial inflammation in response to inflammatory and infectious stimuli. Mucosal Immunol. 6, 557-568 (2013).
22. Kim, K.C. & Lillehoj, E.P. MUC1 mucin: a peacemaker in the lung. Am. J. Respir. Cell Mol. Biol. 39, 644-647 (2008).
23. Guang,W., Ding, H., Czinn, S.J., Kim, K.C., Blanchard, T.G. & Lillehoj, E.P. Muc1 cell surface mucin attenuates epithelial inflammation in response to a common mucosal pathogen. J. Biol. Chem. 285, 20547-20557 (2010).
24. Lu,W. et al. Enhanced pulmonary clearance of Pseudomonas aeruginosa by Muc1 knockout mice. J. Immunol. 176, 3890-3894 (2006).
25. Williams, M.A. et al. Deletion of the mucin-like molecule Muc1 enhances dendritic cell activation in response to toll-like receptor ligands. J. Innate Immun. 2, 123-143 (2010).
26. Kato, K. et al. Membrane-tethered MUC1 mucin is phosphorylated by epidermal growth factor receptor in airway epithelial cells and associates with TLR5 to inhibit recruitment of MyD88. J. Immunol. 188, 2014-2022 (2012).
27. Kato, K., Lillehoj, E.P. & Kim, K.C. MUC1 regulates epithelial inflammation and apoptosis by PolyI:C through inhibition of Toll/IL-1 receptor-domaincontaining adapter-inducing IFN-beta (TRIF) recruitment to Toll-like receptor 3. Am. J. Respir. Cell Mol. Biol. 51, 446-454 (2014).
28. Zhang, J., Xu, K., Ambati, B. & Yu, F.-S.X. Toll-like receptor 5-mediated corneal epithelial inflammatory responses to Pseudomonas aeruginosa flagellin. Invest. Ophthalmol. Vis. Sci. 44, 4247-4254 (2003).
29. Song, P.I. et al. The expression of functional LPS receptor proteins CD14 and toll-like receptor 4 in human corneal cells. I Invest. Ophthalmol. Vis. Sci 42, 2867-2877 (2001).
30. Gipson, I.K., Spurr-Michaud, S., Argueso, P., Tisdale, A., Ng, T.F. & Russo, C.L. Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Invest. Ophthalmol. Vis. Sci. 44, 2496-2506 (2003).
31. Nakao, Y. et al. Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. J. Immunol. 174, 1566-1573 (2005).
32. Guan, Y. et al. Human TLRs 10 and 1 share commonmechanisms of innate immune sensing but not signaling. J. Immunol. 184, 5094-5103 (2010).
33. Hozono, Y. et al. Human corneal epithelial cells respond to ocularpathogenic, but not to nonpathogenic-flagellin. Biochem. Biophys. Res. Commun. 347, 238-247 (2006).
34. Li, J., Shen, J. & Beuerman, R.W. Expression of toll-like receptors in human limbal and conjunctival epithelial cells. Mol. Vis. 13, 813-822 (2007).
35. Marko, C.K., Menon, B.B., Chen, G.,Whitsett, J.A., Clevers, H. & Gipson, I.K. Spdef null mice lack conjunctival goblet cells and provide a model of dry eye. Am. J. Pathol. 183, 35-48 (2013).
36. Danjo, Y., Hazlett, L.D. & Gipson, I.K.C57BL/6 mice lacking Muc1 show no ocular surface phenotype. Invest. Ophthalmol. Vis. Sci. 41, 4080-4084 (2000).
37. Argueso, P., Guzman-Aranguez, A., Mantelli, F., Cao, Z., Ricciuto, J. & Panjwani, N. Association of cell surfacemucins with galectin-3 contributes to the ocular surface epithelial barrier. J. Biol. Chem. 284, 23037-23045 (2009).
38. Akita, K., Tanaka, M., Tanida, S., Mori, Y., Toda, M. & Nakada, H. CA125/ MUC16 interacts with Src family kinases, and over-expression of its C-terminal fragment in human epithelial cancer cells reduces cell-cell adhesion. Eur. J. Cell Biol. 92, 257-263 (2013).
39. Page, T.H., Smolinska, M., Gillespie, J., Urbaniak, A.M. & Foxwell, B.M. Tyrosine kinases and inflammatory signalling. Curr. Mol. Med. 9, 69-85 (2009).
40. Kardon, R. et al. Bacterial conjunctivitis in Muc1 null mice. Invest. Ophthalmol. Vis. Sci. 40, 1328-1335 (1999).
41. McAuley, J.L. et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J. Clin. Invest. 117, 2313-2324 (2007).
42. Linden, S.K. et al. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog. 5, e1000617 (2009).
43. Davies, J.R., Kirkham, S., Svitacheva, N., Thornton, D.J. & Carlstedt, I. MUC16 is produced in tracheal surface epitheliumand submucosal glands and is present in secretions from normal human airway and cultured bronchial epithelial cells. Int. J. Biochem. Cell Biol. 39, 1943-1954 (2007).
44. Li, Y., Kuwahara, H., Ren, J., Wen, G. & Kufe, D. The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin. J. Biol. Chem. 276, 6061-6064 (2001).
45. Haridas, D.,Ponnusamy, M.P.,Chugh,S., Lakshmanan, I., Seshacharyulu, P. & Batra, S.K. MUC16: molecular analysis and its functional implications in benign and malignant conditions. FASEB J 28, 4183-4199 (2014).
46. Govindarajan, B. et al. A metalloproteinase secreted by Streptococcus pneumoniae removes membrane mucin MUC16 from the epithelial glycocalyx barrier. PLoS One 7, e32418 (2012).
47. Spicer, A.P., Rowse, G.J., Lidner, T.K. & Gendler, S.J. Delayed mammary tumor progression in Muc-1 null mice. J. Biol. Chem. 270, 30093-30101 (1995).
48. Wang, Y. et al. MUC16 expression during embryogenesis, in adult tissues, and ovarian cancer in the mouse. Differentiation 76, 1081-1092 (2008).
49. Ioannidis, I., Ye, F., McNally, B., Willette, M. & Flano, E. Toll-like receptor expression and induction of type I and type III interferons in primary airway epithelial cells. J. Virol. 87, 3261-3270 (2013).
50. Martin, F.J. & Prince, A.S. TLR2 regulates gap junction intercellular communication in airway cells. J. Immunol. 180, 4986-4993 (2008).
51. Yamada, K., Ueta, M., Sotozono, C., Yokoi, N., Inatomi, T. & Kinoshita, S. Upregulation of Toll-like receptor 5 expression in the conjunctival epithelium of various human ocular surface diseases. Br. J. Ophthalmol. 98, 1116-1119 (2014).
52. Zarember, K.A. & Godowski, P.J. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 168, 554-561 (2002).
53. Hijiya, N. et al. Possible involvement of toll-like receptor 4 in endothelial cell activation of larger vessels in response to lipopolysaccharide. Pathobiology 70, 18-25 (2002).
54. Talreja, J., Kabir, M.H., B Filla, M., Stechschulte, D.J. & Dileepan, K.N. Histamine induces Toll-like receptor 2 and 4 expression in endothelial cells and enhances sensitivity to Gram-positive and Gram-negative bacterial cell wall components. Immunology 113, 224-233 (2004).
55. Maaser, C. et al. Human intestinal microvascular endothelial cells express Toll-like receptor 5: a binding partner for bacterial flagellin. J. Immunol. 172, 5056-5062 (2004).
56. Menon, B.B. & Govindarajan, B. Identification of an atypical zinc metalloproteinase, ZmpC, from an epidemic conjunctivitis-causing strain of Streptococcus pneumoniae. Microb. Pathog. 56, 40-46 (2013).
57. Blalock, T.D., Spurr-Michaud, S.J., Tisdale, A.S. & Gipson, I.K. Release of membrane-associated mucins from ocular surface epithelia. Invest. Ophthalmol. Vis. Sci. 49, 1864-1871 (2008).
58. Nichols, B.A., Chiappino, M.L. & Dawson, C.R. Demonstration of the mucous layer of the tear film by electron microscopy. Invest. Ophthalmol. Vis. Sci. 26, 464-473 (1985).