Directional secretomes reflect polarity-specific functions in an in vitro model of human bronchial epithelium

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 2, 2014, Pages 292-300

  Pillai, Dinesh K ^a,b   Sankoorikal, Binu John V ^b   Johnson, Eric ^b   Seneviratne, Angelo N ^b   Zurko, Jessica ^b   Brown, Kristy J ^a,b   Hathout, Yetrib ^a,b   Rose, Mary C ^a,b  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Bronchial epithelium; Proteome; Secreted proteins; Secretome

Indexed keywords

DESMOGLEIN 2; LIPOCORTIN 4; MUCIN 5AC; MUCIN 5B; PROTEOME;

ARTICLE; BRONCHUS MUCOSA; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG DISEASE; MOLECULAR PATHOLOGY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEOMICS; RESPIRATORY EPITHELIUM; WESTERN BLOTTING;

ASTHMA; CELL DIFFERENTIATION; CELL POLARITY; CELLS, CULTURED; DESMOGLEIN 2; EPITHELIAL CELLS; HUMANS; LUNG; RESPIRATORY MUCOSA;

EID: 84893271107     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0188OC     Document Type: Article

References (50)

1. Simons K, Wandinger-Ness A. Polarized sorting in epithelia. Cell 1990; 62:207-210.
2. Feigin ME, Muthuswamy SK. Polarity proteins regulate mammalian cellcell junctions and cancer pathogenesis. Curr Opin Cell Biol 2009;21: 694-700.
3. Feigin ME, Muthuswamy SK. ErbB receptors and cell polarity: new pathways and paradigms for understanding cell migration and invasion. Exp Cell Res 2009;315:707-716.
4. Homolya L, Steinberg TH, Boucher RC. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J Cell Biol 2000;150:1349-1360.
5. Malavia NK, Raub CB, Mahon SB, Brenner M, Panettieri RA Jr, George SC. Airway epithelium stimulates smooth muscle proliferation. Am J Respir Cell Mol Biol 2009;41:297-304.
6. Wong AM, Chow AW, Au SC, Wong CC, Ko WH. Apical versus basolateral P2Y(6) receptor-mediated Cl(-) secretion in immortalized bronchial epithelia. Am J Respir Cell Mol Biol 2009; 40:733-745.
7. Holgate ST, Lackie PM, Davies DE, Roche WR, Walls AF. The bronchial epithelium as a key regulator of airway inflammation and remodelling in asthma. Clin Exp Allergy 1999;29:90-95.
8. Davies DE. The role of the epithelium in airway remodeling in asthma. Proc Am Thorac Soc 2009;6:678-682.
9. Regamey N, Jeffery PK, Alton EW, Bush A, Davies JC. Airway remodelling and its relationship to inflammation in cystic fibrosis. Thorax 2011;66:624-629.
10. Burgel PR, Bourdin A, Chanez P, Chabot F, Chaouat A, Chinet T, de Blic J, Devillier P, Deschildre A, Didier A, et al. Update on the roles of distal airways in COPD. Eur Respir Rev 2011;20:7-22.
11. Gharib SA, Vaisar T, Aitken ML, Park DR, Heinecke JW, Fu X. Mapping the lung proteome in cystic fibrosis. J Proteome Res 2009;8: 3020-3028.
12. McMorran BJ, Patat SA, Carlin JB, Grimwood K, Jones A, Armstrong DS, Galati JC, Cooper PJ, Byrnes CA, Francis PW, et al. Novel neutrophilderived proteins in bronchoalveolar lavage fluid indicate an exaggerated inflammatory response in pediatric cystic fibrosis patients. Clin Chem 2007;53:1782-1791.
13. Sloane AJ, Lindner RA, Prasad SS, Sebastian LT, Pedersen SK, Robinson M, Bye PT, Nielson DW, Harry JL. Proteomic analysis of sputum from adults and children with cystic fibrosis and from control subjects. Am J Respir Crit Care Med 2005;172: 1416-1426.
14. Gray RD, MacGregor G, Noble D, Imrie M, Dewar M, Boyd AC, Innes JA, Porteous DJ, Greening AP. Sputum proteomics in inflammatory and suppurative respiratory diseases. Am J Respir Crit Care Med 2008; 178:444-452.
15. Wu J, Kobayashi M, Sousa EA, Liu W, Cai J, Goldman SJ, Dorner AJ, Projan SJ, Kavuru MS, Qiu Y, et al. Differential proteomic analysis of bronchoalveolar lavage fluid in asthmatics following segmental antigen challenge. Mol Cell Proteomics 2005;4:1251-1264.
16. Wu R, Yankaskas J, Cheng E, Knowles MR, Boucher R. Growth and differentiation of human nasal epithelial cells in culture: serum-free, hormone-supplemented medium and proteoglycan synthesis. Am Rev Respir Dis 1985;132:311-320.
17. Kondo M, Finkbeiner WE, Widdicombe JH. Cultures of bovine tracheal epithelium with differentiated ultrastructure and ion transport. In Vitro Cell Dev Biol 1993;29A:19-24.
18. Fulcher ML, Gabriel S, Burns KA, Yankaskas J, Randell SH. Human cell culture protocols. Totowa, NJ: Humana Press; 2005.
19. Gruenert DC, Finkbeiner WE, Widdicombe JH. Culture and transformation of human airway epithelial cells. Am J Physiol 1995; 268:L347-L360.
20. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 1998;95:1005-1015.
21. Davies DE, Wicks J, Powell RM, Puddicombe SM, Holgate ST. Airway remodeling in asthma: new insights. J Allergy Clin Immunol 2003; 111:215-225, quiz 226.
22. Kesimer M, Kirkham S, Pickles RJ, Henderson AG, Alexis NE, Demaria G, Knight D, Thornton DJ, Sheehan JK. Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways? Am J Physiol Lung Cell Mol Physiol 2009;296: L92-L100.
23. Freishtat RJ, Watson AM, Benton AS, Iqbal SF, Pillai DK, Rose MC, Hoffman EP. Asthmatic airway epithelium is intrinsically inflammatory and mitotically dyssynchronous. Am J Respir Cell Mol Biol 2011;44:863-869.
24. An E, Lu X, Flippin J, Devaney JM, Halligan B, Hoffman EP, Strunnikova N, Csaky K, Hathout Y. Secreted proteome profiling in human RPE cell cultures derived from donors with age related macular degeneration and age matched healthy donors. J Proteome Res 2006;5:2599-2610.
25. Zhang A, Williamson CD, Wong DS, Bullough MD, Brown KJ, Hathout Y, Colberg-Poley AM. Quantitative proteomic analyses of human cytomegalovirus- induced restructuring of endoplasmic reticulummitochondrial contacts at late times of infection. Mol Cell Proteomics 2011;10:M111 009936.
26. Hathout Y, Flippin J, Fan C, Liu P, Csaky K. Metabolic labeling of human primary retinal pigment epithelial cells for accurate comparative proteomics. J Proteome Res 2005;4:620-627.
27. Kesimer M, Scull M, Brighton B, DeMaria G, Burns K, O'Neal W, Pickles RJ, Sheehan JK. Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 2009;23:1858-1868.
28. Thomas PD, Kejariwal A, Campbell MJ, Mi H, Diemer K, Guo N, Ladunga I, Ulitsky-Lazareva B, Muruganujan A, Rabkin S, et al. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res 2003;31:334-341.
29. Choi H, Fermin D, Nesvizhskii AI. Significance analysis of spectral count data in label-free shotgun proteomics. Mol Cell Proteomics 2008;7:2373-2385.
30. Bernacki SH, Nelson AL, Abdullah L, Sheehan JK, Harris A, Davis CW, Randell SH. Mucin gene expression during differentiation of human airway epithelia in vitro: muc4 and muc5b are strongly induced. Am J Respir Cell Mol Biol 1999;20:595-604.
31. Brown KJ, Formolo CA, Seol H, Marathi RL, Duguez S, An E, Pillai D, Nazarian J, Rood BR, Hathout Y. Advances in the proteomic investigation of the cell secretome. Expert Rev Proteomics 2012;9: 337-345.
32. Lizarbe MA, Barrasa JI, Olmo N, Gavilanes F, Turnay J. Annexinphospholipid interactions: functional implications. Int J Mol Sci 2013; 14:2652-2683.
33. Piljic A, Schultz C. Annexin A4 self-association modulates general membrane protein mobility in living cells. Mol Biol Cell 2006;17: 3318-3328.
34. Mayran N, Traverso V, Maroux S, Massey-Harroche D. Cellular and subcellular localizations of annexins I, IV, and VI in lung epithelia. Am J Physiol 1996;270:L863-L871.
35. Lin LL, Huang HC, Juan HF. Revealing the molecular mechanism of gastric cancer marker annexin A4 in cancer cell proliferation using exon arrays. PLoS ONE 2012;7:e44615.
36. Hein Z, Schmidt S, Zimmer KP, Naim HY. The dual role of annexin ii in targeting of brush border proteins and in intestinal cell polarity. Differentiation 2011;81:243-252.
37. Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, Yates Jr. Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res 2009;8:1304-1314.
38. Buschow SI, van Balkom BW, Aalberts M, Heck AJ, Wauben M, Stoorvogel W. MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol Cell Biol 2010;88:851-856.
39. Welton JL, Khanna S, Giles PJ, Brennan P, Brewis IA, Staffurth J, Mason MD, Clayton A. Proteomics analysis of bladder cancer exosomes. Mol Cell Proteomics 2010;9:1324-1338.
40. Choi DS, Lee JM, Park GW, Lim HW, Bang JY, Kim YK, Kwon KH, Kwon HJ, Kim KP, Gho YS. Proteomic analysis of microvesicles derived from human colorectal cancer cells. J Proteome Res 2007;6: 4646-4655.
41. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004;101: 13368-13373.
42. Gonzales PA, Pisitkun T, Hoffert JD, Tchapyjnikov D, Star RA, Kleta R, Wang NS, Knepper MA. Large-scale proteomics and phosphoproteomics of urinary exosomes. J Am Soc Nephrol 2009; 20:363-379.
43. Ali M, Lillehoj EP, Park Y, Kyo Y, Kim KC. Analysis of the proteome of human airway epithelial secretions. Proteome Sci 2011;9:4.
44. Cirillo N, Lanza M, De Rosa A, Cammarota M, La Gatta A, Gombos F, Lanza A. The most widespread desmosomal cadherin, desmoglein 2, is a novel target of caspase 3-mediated apoptotic machinery. J Cell Biochem 2008;103:598-606.
45. Schlegel N, Meir M, Heupel WM, Holthöfer B, Leube RE, Waschke J. Desmoglein 2-mediated adhesion is required for intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 2010;298: G774-G783.
46. Rizzo S, Lodder EM, Verkerk AO, Wolswinkel R, Beekman L, Pilichou K, Basso C, Remme CA, Thiene G, Bezzina CR. Intercalated disc abnormalities, reduced Na(1) current density, and conduction slowing in desmoglein-2 mutant mice prior to cardiomyopathic changes. Cardiovasc Res 2012;95:409-418.
47. Xiao C, Puddicombe SM, Field S, Haywood J, Broughton-Head V, Puxeddu I, Haitchi HM, Vernon-Wilson E, Sammut D, Bedke N, et al. Defective epithelial barrier function in asthma. J Allergy Clin Immunol 2011;128:549-556, e1-12.
48. Kirkham S, Sheehan JK, Knight D, Richardson PS, Thornton DJ. Heterogeneity of airways mucus: variations in the amounts and glycoforms of the major oligomeric mucins MUC5AC and MUC5B. Biochem J 2002;361:537-546.
49. Holmé n JM, Karlsson NG, Abdullah LH, Randell SH, Sheehan JK, Hansson GC, Davis CW. Mucins and their O-glycans from human bronchial epithelial cell cultures. Am J Physiol Lung Cell Mol Physiol 2004;287:L824-L834.
50. Preciado D, Goyal S, Rahimi M, Watson AM, Brown KJ, Hathout Y, Rose MC. MUC5B Is the predominant mucin glycoprotein in chronic otitis media fluid. Pediatr Res 2010;68:231-236.