Pivotal role of MUC1 glycosylation by cigarette smoke in modulating disruption of airway adherens junctions in vitro

Journal of Pathology

Volumn 234, Issue 1, 2014, Pages 60-73

  Zhang, Lili ^a   Gallup, Marianne ^a   Zlock, Lorna ^b   Chen, Yu Ting Feeling ^a   Finkbeiner, Walter E ^b   McNamara, Nancy A ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cigarette smoke; E cadherin; EGFR; epithelial mesenchymal transition; galectin 3; glycosylation; in vitro airway model; lung cancer; MUC1; p120 catenin

Indexed keywords

CADHERIN; CIGARETTE SMOKE; MUCIN 1; PROTEIN KINASE P60; PROTEIN P120; TUNICAMYCIN; CATENIN; DELTA CATENIN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; GALECTIN 3; GALECTIN-3, HUMAN; MUC1 PROTEIN, HUMAN; PASSIVE SMOKING;

ARTICLE; BRONCHUS MUCOSA; CELL ADHESION; CELL DISRUPTION; CELL JUNCTION; CONTROLLED STUDY; DEGLYCOSYLATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE LOSS; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ADHERENS JUNCTION; ADVERSE EFFECTS; BIOLOGICAL MODEL; CELL CULTURE; EPITHELIUM CELL; GENETICS; GLYCOSYLATION; LUNG; LUNG TUMOR; METABOLISM; PASSIVE SMOKING; PATHOLOGY; PHOSPHORYLATION; SMOKING;

ADHERENS JUNCTIONS; CADHERINS; CATENINS; CELLS, CULTURED; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GALECTIN 3; GLYCOSYLATION; HUMANS; LUNG; LUNG NEOPLASMS; MODELS, BIOLOGICAL; MUCIN-1; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SMOKING; TOBACCO SMOKE POLLUTION;

EID: 84905905058     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4375     Document Type: Article

References (41)

1. Society AC,. Cancer facts and figures, 2009 [internet]: http://www.cancer.org/acs/groups/content/@nho/documents/document/500809webpdf. pdf.
2. Gilpin EA, Pierce JP,. Demographic differences in patterns in the incidence of smoking cessation: United States 1950-1990. Ann Epidemiol 2002; 12: 141-150.
3. Polyak K, Weinberg RA,. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9: 265-273.
4. Mani SA, Guo W, Liao MJ, et al., The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
5. Thoreson MA, Reynolds AB,. Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation 2002; 70: 583-589.
6. Liu Y, Wang Y, Zhang Y, et al., Abnormal expression of p120-catenin, E-cadherin, and small GTPases is significantly associated with malignant phenotype of human lung cancer. Lung Cancer 2009; 63: 375-382.
7. Guddo F, Giatromanolaki A, Koukourakis MI, et al., MUC1 episialin; expression in non-small cell lung cancer is independent of EGFR and c-erbB-2 expression and correlates with poor survival in node positive patients. J Clin Pathol 1998; 51: 667-671.
8. Awaya H, Takeshima Y, Yamasaki M, et al., Expression of MUC1, MUC2, MUC5AC, and MUC6 in atypical adenomatous hyperplasia, bronchioloalveolar carcinoma, adenocarcinoma with mixed subtypes, and mucinous bronchioloalveolar carcinoma of the lung. Am J Clin Pathol 2004; 121: 644-653.
9. Situ D, Wang J, Ma Y, et al., Expression and prognostic relevance of MUC1 in stage IB non-small cell lung cancer. Med Oncol 2011; 28 (suppl 1): S596-604.
10. Dasari V, Gallup M, Lemjabbar H, et al., Epithelial-mesenchymal transition in lung cancer: is tobacco the 'smoking gun'? Am J Respir Cell Mol Biol 2006; 35: 3-9.
11. Chen YT, Gallup M, Nikulina K, et al., Cigarette smoke induces epidermal growth factor receptor-dependent redistribution of apical MUC1 and junctional β-catenin in polarized human airway epithelial cells. Am J Pathol 2010; 177: 1255-1264.
12. Zhang L, Gallup M, Zlock L, et al., Cigarette smoke disrupts the integrity of airway adherens junctions through the aberrant interaction of p120-catenin with the cytoplasmic tail of MUC1. J Pathol 2013; 229: 74-86.
13. Zhang L, Gallup M, Zlock L, et al., p120-catenin modulates airway epithelial cell migration induced by cigarette smoke. Biochem Biophys Res Commun 2012; 417: 49-55.
14. Zhang L, Gallup M, Zlock L, et al., Rac1 and Cdc42 differentially modulate cigarette smoke-induced airway cell migration through p120-catenin-dependent and -independent pathways. Am J Pathol 2013; 182: 1986-1995.
15. Shaykhiev R, Otaki F, Bonsu P, et al., Cigarette smoking reprograms apical junctional complex molecular architecture in the human airway epithelium in vivo. Cell Mol Life Sci 2011; 68: 877-892.
16. Kufe DW,. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 2009; 9: 874-885.
17. Kufe DW,. Functional targeting of the MUC1 oncogene in human cancers. Cancer Biol Ther 2009; 8: 1197-1203.
18. Hollingsworth MA, Swanson BJ,. Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 2004; 4: 45-60.
19. Pinto R, Carvalho AS, Conze T, et al., Identification of new cancer biomarkers based on aberrant mucin glycoforms by in situ proximity ligation. J Cell Mol Med 2012; 16: 1474-1484.
20. Metzgar RS, Rodriguez N, Finn OJ, et al., Detection of a pancreatic cancer-associated antigen, DU-PAN-2 antigen, in serum and ascites of patients with adenocarcinoma. Proc Natl Acad Sci USA 1984; 81: 5242-5246.
21. Scambia G, Benedetti Panici P, Baiocchi G, et al., CA 15-3 as a tumor marker in gynecological malignancies. Gynecol Oncol 1988; 30: 265-273.
22. Ramasamy S, Duraisamy S, Barbashov S, et al., The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop. Mol Cell 2007; 27: 992-1004.
23. Singh PK, Hollingsworth MA,. Cell surface-associated mucins in signal transduction. Trends Cell Biol 2006; 16: 467-476.
24. Senapati S, Das S, Batra SK,. Mucin-interacting proteins: from function to therapeutics. Trends Biochem Sci 2010; 35: 236-245.
25. Pezzulo AA, Starner TD, Scheetz TE, et al., The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol 2011; 300: L25-31.
26. Park JH, Nishidate T, Kijima K, et al., Critical roles of mucin 1 glycosylation by transactivated polypeptide N-acetylgalactosaminyltransferase 6 in mammary carcinogenesis. Cancer Res 2010; 70: 2759-2769.
27. Bennett EP, Mandel U, Clausen H, et al., Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 2012; 22: 736-756.
28. Gendler SJ, Spicer AP,. Epithelial mucin genes. Annu Rev Physiol 1995; 57: 607-634.
29. Pimental RA, Julian J, Gendler SJ, et al., Synthesis and intracellular trafficking of Muc-1 and mucins by polarized mouse uterine epithelial cells. J Biol Chem 1996; 271: 28128-28137.
30. Nutini S, Cappelli G, Benucci A, et al., Serum NSE, CEA, CT, CA 15-3 levels in human lung cancer. Int J Biol Markers 1990; 5: 198-202.
31. Lillehoj EP, Han F, Kim KC,. Mutagenesis of a Gly-Ser cleavage site in MUC1 inhibits ectodomain shedding. Biochem Biophys Res Commun 2003; 307: 743-749.
32. Thathiah A, Blobel CP, Carson DD,. Tumor necrosis factor-α- converting enzyme/ADAM 17 mediates MUC1 shedding. J Biol Chem 2003; 278: 3386-3394.
33. Altschuler Y, Kinlough CL, Poland PA, et al., Clathrin-mediated endocytosis of MUC1 is modulated by its glycosylation state. Mol Biol Cell 2000; 11: 819-831.
34. Szoke T, Kayser K, Trojan I, et al., The role of microvascularization and growth/adhesion-regulatory lectins in the prognosis of non-small cell lung cancer in stage II. Eur J Cardiothorac Surg 2007; 31: 783-787.
35. Li Y, Kuwahara H, Ren J, et al., The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3β and β-catenin. J Biol Chem 2001; 276: 6061-6064.
36. Xu X, Bai L, Chen W, et al., MUC1 contributes to BPDE-induced human bronchial epithelial cell transformation through facilitating EGFR activation. PLoS One 2012; 7: e33846.
37. Rajabi H, Alam M, Takahashi H, et al., MUC1-C oncoprotein activates the ZEB1-miR-200c regulatory loop and epithelial-mesenchymal transition. Oncogene 2014; 33: 1680-1689.
38. Roy LD, Sahraei M, Subramani DB, et al., MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 2011; 30: 1449-1459.
39. Gnemmi V, Bouillez A, Gaudelot K, et al., MUC1 drives epithelial-mesenchymal transition in renal carcinoma through Wnt/β-catenin pathway and interaction with SNAIL promoter. Cancer Lett 2014; 346: 225-236.
40. Rajabi H, Ahmad R, Jin C, et al., MUC1-C oncoprotein confers androgen-independent growth of human prostate cancer cells. Prostate 2012; 72: 1659-1668.
41. Park JH, Katagiri T, Chung S, et al., Polypeptide N- acetylgalactosaminyltransferase 6 disrupts mammary acinar morphogenesis through O-glycosylation of fibronectin. Neoplasia 2011; 13: 320-326.