The innate immune properties of airway mucosal surfaces are regulated by dynamic interactions between mucins and interacting proteins: The mucin interactome

Mucosal Immunology

Volumn 9, Issue 6, 2016, Pages 1442-1454

  Radicioni, G ^a   Cao, R ^a   Carpenter, J ^a   Ford, A A ^a   Wang, T T ^a   Li, Y ^a   Kesimer, M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; GALECTIN 3; GLOBULAR PROTEIN; GLUTATHIONE TRANSFERASE; MUCIN; MUCIN 5B; CARRIER PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING; PROTEOME;

ARTICLE; CELLULAR SECRETION; CONTROLLED STUDY; COVALENT BOND; HUMAN; HUMAN CELL; HYDRATION; HYDROPHOBICITY; INNATE IMMUNITY; MUCUS; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; RESPIRATORY TRACT MUCOSA; VISCOELASTICITY; CHEMISTRY; IMMUNOLOGY; METABOLISM; MUCOSAL IMMUNITY; PROCEDURES; RESPIRATORY MUCOSA;

CARRIER PROTEINS; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; MUCINS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; RESPIRATORY MUCOSA;

EID: 84991711125     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.27     Document Type: Article

References (42)

1. Kesimer, M., Ehre, C., Burns, K.A., Davis, C.W., Sheehan, J.K., & Pickles, R.J. Molecular organization of the mucins and glycocalyx underlying mucus transport over mucosal surfaces of the airways. Mucosal Immunol. 6, 379-392 (2013
2. Sheehan, J.K., Kesimer, M., & Pickles, R. Innate immunity and mucus structure and function. Novartis Found. Symp. 279, 155-166 (2006). discussion 167-169, 216-269
3. Rubin, B.K. Physiology of airway mucus clearance. Respir. Care 47, 761-768 (2002
4. Rogers, D.F. Mucus hypersecretion in chronic obstructive pulmonary disease. Novartis Found. Symp. 234, 65-77 (2001). discussion 77-83
5. Rubin, B.K. Mucus structure and properties in cystic fibrosis. Paediatr. Respir. Rev. 8, 4-7 (2007
6. Sheehan, J.K., Richardson, P.S., Fung, D.C., Howard, M., & Thornton, D.J. Analysis of respiratory mucus glycoproteins in asthma: a detailed study from a patient who died in status asthmaticus. Am. J. Respir. CellMol. Biol. 13, 748-756 (1995
7. Ali, M., Lillehoj, E.P., Park, Y., Kyo, Y., & Kim, K.C. Analysis of the proteome of human airway epithelial secretions. Proteome Sci. 9, 4 (2011
8. Kesimer,M., et al. Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L92-L100 (2009
9. Nicholas, B., et al. Shotgun proteomic analysis of human-induced sputum. Proteomics 6, 4390-4401 (2006
10. Button, B., et al. A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337, 937-941 (2012
11. Thornton,D.J.,Rousseau,K.&McGuckin,M.A.Structure and function of the polymericmucins in airwaysmucus. Annu. Rev. Physiol. 70, 459-486 (2008
12. Thornton, D.J., Carlstedt, I., Howard, M., Devine, P.L., Price, M.R., & Sheehan, J.K. Respiratory mucins: identification of core proteins and glycoforms. Biochem. J. 316 (Pt 3), 967-975 (1996
13. Kesimer, M., et al. Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J. 23, 1858-1868 (2009
14. Madsen, J., Mollenhauer, J., & Holmskov, U. Review: Gp-340/DMBT1 in mucosal innate immunity. Innate Immun. 16, 160-167 (2010
15. Kesimer, M., Makhov, A.M., Griffith, J.D., Verdugo, P., & Sheehan, J.K. Unpacking a gel-forming mucin: a view of MUC5B organization after granular release. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L15-L22 (2010
16. Peh, W.Y., Reimhult, E., Teh, H.F., Thomsen, J.S., & Su, X. Understanding ligand binding effects on the conformation of estrogen receptor alpha-DNA complexes: a combinational quartz crystal microbalance with dissipation and surface plasmon resonance study. Biophys J. 92, 4415-4423 (2007
17. Cao, R., Wang, T.T., DeMaria, G., Sheehan, J.K., & Kesimer, M. Mapping the protein domain structures of the respiratory mucins: a mucin proteome coverage study. J Proteome Res. 11, 4013-4023 (2012
18. Raynal, B.D., Hardingham, T.E., Sheehan, J.K., & Thornton, D.J. Calciumdependent protein interactions in MUC5B provide reversible cross-links in salivary mucus. J. Biol. Chem. 278, 28703-28710 (2003
19. Rubinstein MaD, A.V. Associations leading to formation of reversible networks and gels. Curr. Opin. Colloid Interface Sci. 4, 83-87 (1999
20. Chassenieux, C., Nicolai, T., & Benyahia, L. Rheology of associative polymer solutions. Curr. Opin. Colloid Interface Sci. 16, 18-26 (2011
21. Verdugo, P. Supramolecular dynamics of mucus. Cold Spring Harb. Perspect. Med. 2, 1-14 (2012
22. Ridley, C., et al. Assembly of the respiratory mucin MUC5B: a new model for a gel-forming mucin. J. Biol. Chem. 289, 16409-16420 (2014
23. Meyer, E.E., Rosenberg, K.J., & Israelachvili, J. Recent progress in understanding hydrophobic interactions. Proc. Natl. Acad. Sci. USA 103, 15739-15746 (2006
24. Bromberg, L.E., & Barr, D.P. Self-Association ofmucin. Biomacromolecules 1, 325-334 (2000
25. Kesimer, M., & Sheehan, J.K. Analyzing the functions of large glycoconjugates through the dissipative properties of their absorbed layers using the gel-forming mucin MUC5B as an example. Glycobiology 18, 463-472 (2008
26. Hayes, J.D., & Pulford, D.J. The glutathione S-transferase supergene family: regulation of GSTand the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 30, 445-600 (1995
27. Woodward, A.M., Mauris, J. & Argueso, P. Binding of transmembrane mucins to galectin-3 limits erpesvirus 1 infection of human corneal keratinocytes. J. Virol. 87, 5841-5847 (2013
28. Argueso, P. Glycobiology of the ocular surface: mucins and lectins. Jpn. J. Ophthalmol. 57, 150-155 (2013
29. Byrd, J.C., & Bresalier, R.S.Mucins and mucin binding proteins in colorectal cancer. Cancer Metastasis Rev. 23, 77-99 2004
30. Argueso, P., Guzman-Aranguez, A., Mantelli, F., Cao, Z., Ricciuto, J., & Panjwani, N. Association of cell surface mucins with galectin-3 contributes to the ocular surface epithelial barrier. J. Biol. Chem. 284, 23037-23045 (2009
31. Seelenmeyer, C., Wegehingel, S., Lechner, J., & Nickel, W. The cancer antigen CA125 represents a novel counter receptor for galectin-1. J. Cell Sci. 116 (Pt 7), 1305-1318 (2003
32. Senapati, S., Das, S., & Batra, S.K. Mucin-interacting proteins: from function to therapeutics. Trends Biochem. Sci. 35, 236-245 (2010
33. Wiede, A., Jagla, W., Welte, T., Kohnlein, T., Busk, H., & Hoffmann, W. Localization of TFF3, a new mucus-Associated peptide of the human respiratory tract. Am. J. Respir. Crit. Care Med. 159 (4 Pt 1), 1330-1335 (1999
34. Jagla, W., et al. Secretion of TFF-peptides by human salivary glands. Cell Tissue Res. 298, 161-166 (1999
35. Kobayashi, K., et al. Distribution and partial characterisation of IgG Fc binding protein in various mucin producing cells and body fluids. Gut 51, 169-176 (2002
36. Johansson,M.E., Thomsson, K.A., &Hansson, G.C. Proteomic analyses of the twomucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein. J. Proteome Res. 8, 3549-3557 (2009
37. Kesimer, M., et al. Excess secretion of gel-forming mucins and associated innate defense proteins with defective mucin un-packaging underpin gallbladder mucocele formation in dogs. PLoS One 10, e0138988 (2015
38. McInturff, B.H., Ribeiro, P., Abdullah, C., Kesimer, L., & Gel-forming, M. mucins in response to infection and inflammation in normal and cystic fibrosis airways. Pediatr. Pulmonol. 50, S225 (2015
39. Fulcher, M.L., Gabriel, S., Burns, K.A., Yankaskas, J.R., & Randell, S.H. Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107, 183-206 (2005
40. Pickles, R.J., McCarty, D., Matsui, H., Hart, P.J., Randell, S.H., & Boucher, R.C. Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer. J. Virol. 72, 6014-6023 (1998
41. Kesimer, M., & Sheehan, J.K. Mass spectrometric analysis of mucin core proteins. Methods Mol. Biol. 842, 67-79 (2012
42. Thornton, D.J., et al. Salivary mucin MG1 is comprised almost entirely of different glycosylated forms of the MUC5B gene product. Glycobiology 9, 293-302 (1999