Membrane-bound mucins: The mechanistic basis for alterations in the growth and survival of cancer cells

Oncogene

Volumn 29, Issue 20, 2010, Pages 2893-2904

  Bafna, S ^a   Kaur, S ^a   Batra, S K ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Cancer; Cell survival; MUC1; MUC16 (CA125); MUC4

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; MUCIN; MUCIN 1; MUCIN 16; MUCIN 4; MUCIN 6; UNCLASSIFIED DRUG;

ASTHMA; AUTOPHAGY; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL DEATH; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CYSTIC FIBROSIS; CYTOPLASM; HUMAN; NEOPLASM; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; TUMOR GROWTH;

ANIMALS; APOPTOSIS; CELL SURVIVAL; HUMANS; MEMBRANE PROTEINS; MUCINS; NEOPLASMS;

EID: 77952668655     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.87     Document Type: Review

References (105)

1. Agata N, Ahmad R, Kawano T, Raina D, Kharbanda S, Kufe D. (2008). MUC1 oncoprotein blocks death receptor-mediated apoptosis by inhibiting recruitment of caspase-8. Cancer Res 68: 6136-6144.
2. Ahmad R, Raina D, Trivedi V, Ren J, Rajabi H, Kharbanda S et al. (2007). MUC1 oncoprotein activates the IkappaB kinase beta complex and constitutive NF-kappaB signalling. Nat Cell Biol 9: 1419-1427. (Pubitemid 350201755)
3. Andrianifahanana M, Moniaux N, Schmied BM, Ringel J, Friess H, Hollingsworth MA et al. (2001). Mucin (MUC) gene expression in human pancreatic adenocarcinoma and chronic pancreatitis: a potential role of MUC4 as a tumor marker of diagnostic significance. Clin Cancer Res 7: 4033-4040. (Pubitemid 34044624)
4. Arango ME, Li P, Komatsu M, Montes C, Carraway CA, Carraway KL. (2001). Production and localization of Muc4/sialomucin complex and its receptor tyrosine kinase ErbB2 in the rat lacrimal gland. Invest Ophthalmol Vis Sci 42: 2749-2756. (Pubitemid 33035266)
5. Argueso P, Spurr-Michaud S, Russo CL, Tisdale A, Gipson IK. (2003). MUC16 mucin is expressed by the human ocular surface epithelia and carries the H185 carbohydrate epitope. Invest Ophthalmol Vis Sci 44: 2487-2495. (Pubitemid 36618405)
6. Aubert S, Fauquette V, Hemon B, Lepoivre R, Briez N, Bernard D et al. (2009). MUC1, a new hypoxia inducible factor target gene, is an actor in clear renal cell carcinoma tumor progression. Cancer Res 69: 5707-5715.
7. Bafna S, Kaur S, Momi N, Batra SK. (2009). Pancreatic cancer cells resistance to gemcitabine: the role of MUC4 mucin. Br J Cancer 101: 1155-1161.
8. Bafna S, Singh AP, Moniaux N, Eudy JD, Meza JL, Batra SK. (2008). MUC4, a multifunctional transmembrane glycoprotein, induces oncogenic transformation of NIH3T3 mouse fibroblast cells. Cancer Res 68: 9231-9238.
9. Bast Jr RC, Xu FJ, Yu YH, Barnhill S, Zhang Z, Mills GB. (1998). CA 125: the past and the future. Int J Biol Markers 13: 179-187. (Pubitemid 29178546)
10. Bitler BG, Menzl I, Huerta CL, Sands B, Knowlton W, Chang A et al. (2009). Intracellular MUC1 peptides inhibit cancer progression. Clin Cancer Res 15: 100-109.
11. Blalock TD, Spurr-Michaud SJ, Tisdale AS, Heimer SR, Gilmore MS, Ramesh V et al. (2007). Functions of MUC16 in corneal epithelial cells. Invest Ophthalmol Vis Sci 48: 4509-4518. (Pubitemid 351260966)
12. Boivin M, Lane D, Piche A, Rancourt C. (2009). CA125 (MUC16) tumor antigen selectively modulates the sensitivity of ovarian cancer cells to genotoxic drug-induced apoptosis. Gynecol Oncol 115: 407-413.
13. Buisine MP, Desreumaux P, Leteurtre E, Copin MC, Colombel JF, Porchet N et al. (2001). Mucin gene expression in intestinal epithelial cells in Crohn's disease. Gut 49: 544-551. (Pubitemid 32896986)
14. Capstick V, Maclean GD, Suresh MR, Bodnar D, Lloyd S, Shepert L et al. (1991). Clinical evaluation of a new two-site assay for CA125 antigen. Int J Biol Markers 6: 129-135.
15. Carraway III KL, Funes M, Workman HC, Sweeney C. (2007). Contribution of membrane mucins to tumor progression through modulation of cellular growth signaling pathways. Curr Top Dev Biol 78: 1-22.
16. Carraway KL, Perez A, Idris N, Jepson S, Arango M, Komatsu M et al. (2002). Muc4/sialomucin complex, the intramembrane ErbB2 ligand, in cancer and epithelia: to protect and to survive. Prog Nucleic Acid Res Mol Biol 71: 149-185.
17. Chao C, Saito S, Kang J, Anderson CW, Appella E, Xu Y. (2000). p53 transcriptional activity is essential for p53-dependent apoptosis following DNA damage. EMBO J 19: 4967-4975.
18. Chaturvedi P, Singh AP, Batra SK. (2008a). Structure, evolution, and biology of the MUC4 mucin. FASEB J 22: 966-981. (Pubitemid 351519954)
19. Chaturvedi P, Singh AP, Chakraborty S, Chauhan SC, Bafna S, Meza JL et al. (2008b). MUC4 mucin interacts with and stabilizes the HER2 oncoprotein in human pancreatic cancer cells. Cancer Res 68: 2065-2070. (Pubitemid 351521776)
20. Chaturvedi P, Singh AP, Moniaux N, Senapati S, Chakraborty S, Meza JL et al. (2007). MUC4 mucin potentiates pancreatic tumor cell proliferation, survival, and invasive properties and interferes with its interaction to extracellular matrix proteins. Mol Cancer Res 5: 309-320. (Pubitemid 46706993)
21. Chauhan SC, Vannatta K, Ebeling MC, Vinayek N, Watanabe A, Pandey KK et al. (2009). Expression and functions of transmem-brane mucin MUC13 in ovarian cancer. Cancer Res 69: 765-774.
22. Copin MC, Buisine MP, Leteurtre E, Marquette CH, Porte H, Aubert JP et al. (2001). Mucinous bronchioloalveolar carcinomas display a specific pattern of mucin gene expression among primary lung adenocarcinomas. Hum Pathol 32: 274-281. (Pubitemid 32246800)
23. Corfield AP, Carroll D, Myerscough N, Probert CS. (2001). Mucins in the gastrointestinal tract in health and disease. Front Biosci 6: D1321-D1357.
24. Croce CM. (2008). Oncogenes and cancer. N Engl J Med 358: 502-511.
25. Davidson B, Baekelandt M, Shih I. (2007). MUC4 is upregulated in ovarian carcinoma effusions and differentiates carcinoma cells from mesothelial cells. Diagn Cytopathol 35: 756-760. (Pubitemid 350250759)
26. Gendler SJ. (2001). MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia 6: 339-353. (Pubitemid 39600492)
27. Gipson IK. (2005). Human endocervical mucins. Ernst Schering Res Found Workshop 52: 219-244.
28. Gubbels JA, Belisle J, Onda M, Rancourt C, Migneault M, Ho M et al. (2006). Mesothelin-MUC16 binding is a high affinity, N-glycan dependent interaction that facilitates peritoneal metastasis of ovarian tumors. Mol Cancer 5: 50. (Pubitemid 44742657)
29. Gubbels JA, Felder M, Horibata S, Belisle JA, Kapur A, Holden H et al. (2010). MUC16 provides immune protection by inhibiting synapse formation between NK and ovarian tumor cells. Mol Cancer 9: 11.
30. Hait WN, Jin S, Yang JM. (2006). A matter of life or death (or both): understanding autophagy in cancer. Clin Cancer Res 12: 1961-1965.
31. Hanaoka J, Kontani K, Sawai S, Ichinose M, Tezuka N, Inoue S et al. (2001). Analysis of MUC4 mucin expression in lung carcinoma cells and its immunogenicity. Cancer 92: 2148-2157. (Pubitemid 32973326)
32. Hattrup CL, Gendler SJ. (2006). MUC1 alters oncogenic events and transcription in human breast cancer cells. Breast Cancer Res 8: R37.
33. Hattrup CL, Gendler SJ. (2008). Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 70: 431-457. (Pubitemid 351738187)
34. Higuchi T, Orita T, Katsuya K, Yamasaki Y, Akiyama K, Li H et al. (2004a). MUC20 suppresses the hepatocyte growth factor-induced Grb2-Ras pathway by binding to a multifunctional docking site of met. Mol Cell Biol 24: 7456-7468. (Pubitemid 39121474)
35. Higuchi T, Orita T, Nakanishi S, Katsuya K, Watanabe H, Yamasaki Y et al. (2004b). Molecular cloning, genomic structure, and expression analysis of MUC20, a novel mucin protein, up-regulated in injured kidney. J Biol Chem 279: 1968-1979. (Pubitemid 38084468)
36. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas III CF, Hynes NE. (2003). The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA 100: 8933-8938. (Pubitemid 36899201)
37. Holbro T, Hynes NE. (2004). ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 44: 195-217. (Pubitemid 38263839)
38. Hollingsworth MA, Swanson BJ. (2004). Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4: 45-60.
39. Horowitz JC, Lee DY, Waghray M, Keshamouni VG, Thomas PE, Zhang H et al. (2004). Activation of the pro-survival phosphatidy-linositol 3-kinase/AKT pathway by transforming growth factor-beta1 in mesenchymal cells is mediated by p38 MAPK-dependent induction of an autocrine growth factor. J Biol Chem 279: 1359-1367. (Pubitemid 38082662)
40. Hu YP, Haq B, Carraway KL, Savaraj N, Lampidis TJ. (2003). Multidrug resistance correlates with overexpression of Muc4 but inversely with P-glycoprotein and multidrug resistance related protein in transfected human melanoma cells. Biochem Pharmacol 65: 1419-1425. (Pubitemid 36555829)
41. Huang L, Chen D, Liu D, Yin L, Kharbanda S, Kufe D. (2005). MUC1 oncoprotein blocks glycogen synthase kinase 3beta-mediated phosphorylation and degradation of beta-catenin. Cancer Res 65: 10413-10422. (Pubitemid 41743735)
42. Hynes NE, Lane HA. (2005). ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 5: 341-354.
43. Itoh Y, Kamata-Sakurai M, da-Nagai K, Nagai S, Tsuiji M, Ishii-Schrade K et al. (2008). Identification and expression of human epiglycanin/MUC21: a novel transmembrane mucin. Glycobiology 18: 74-83.
44. Jepson S, Komatsu M, Haq B, Arango ME, Huang D, Carraway CA et al. (2002). Muc4/sialomucin complex, the intramembrane ErbB2 ligand, induces specific phosphorylation of ErbB2 and enhances expression of p27(kip), but does not activate mitogen-activated kinase or protein kinaseB/Akt pathways. Oncogene 21: 7524-7532. (Pubitemid 35305580)
45. Kawano T, Ahmad R, Nogi H, Agata N, Anderson K, Kufe D. (2008). MUC1 oncoprotein promotes growth and survival of human multiple myeloma cells. Int J Oncol 33: 153-159.
46. Kharbanda S, Pandey P, Ren R, Mayer B, Zon L, Kufe D. (1995a). c-Abl activation regulates induction of the SEK1/stress-activated protein kinase pathway in the cellular response to 1-beta-D-arabinofuranosylcytosine. J Biol Chem 270: 30278-30281. (Pubitemid 3022820)
47. Kharbanda S, Ren R, Pandey P, Shafman TD, Feller SM, Weichselbaum RR et al. (1995b). Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 376: 785-788.
48. Komatsu M, Jepson S, Arango ME, Carothers Carraway CA, Carraway KL. (2001). Muc4/sialomucin complex, an intramem-brane modulator of ErbB2/HER2/Neu, potentiates primary tumor growth and suppresses apoptosis in a xenotransplanted tumor. Oncogene 20: 461-470. (Pubitemid 32158226)
49. Kui WN, Easton RL, Panico M, Sutton-Smith M, Morrison JC, Lattanzio FA et al. (2003). Characterization of the oligosaccharides associated with the human ovarian tumor marker CA125. J Biol Chem 278: 28619-28634. (Pubitemid 36935768)
50. Lan MS, Batra SK, Qi WN, Metzgar RS, Hollingsworth MA. (1990). Cloning and sequencing of a human pancreatic tumor mucin cDNA. J Biol Chem 265: 15294-15299. (Pubitemid 20296237)
51. Levine AJ. (1997). p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
52. Li GS, Zhang H, Lu JC, Hou P, Zhou Y, Ma XZ et al. (2005). Variable number of tandem repeats polymorphism of MUC20 is associated with the progression of IgA nephropathy. Zhonghua Yi Xue Za Zhi 85: 1333-1338. (Pubitemid 40852085)
53. Li Y, Liu D, Chen D, Kharbanda S, Kufe D. (2003). Human DF3/MUC1 carcinoma-associated protein functions as an oncogene. Oncogene 22: 6107-6110. (Pubitemid 37175889)
54. Li Y, Ren J, Yu W, Li Q, Kuwahara H, Yin L et al. (2001). The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and beta-catenin. J Biol Chem 276: 35239-35242. (Pubitemid 37384312)
55. Mall AS. (2008). Analysis of mucins: role in laboratory diagnosis. J Clin Pathol 61: 1018-1024.
56. Malmberg EK, Pelaseyed T, Petersson AC, Seidler UE, De JH, Riordan JR et al. (2008). The C-terminus of the transmembrane mucin MUC17 binds to the scaffold protein PDZK1 that stably localizes it to the enterocyte apical membrane in the small intestine. Biochem J 410: 283-289. (Pubitemid 351346186)
57. Matsuoka Y, Endo K, Kawamura Y, Yoshida T, Saga T, Watanabe Y et al. (1990). Normal bronchial mucus contains high levels of cancer-associated antigens, CA125, CA19-9, and carcinoembryonic antigen. Cancer 65: 506-510. (Pubitemid 20058368)
58. Meerzaman D, Shapiro PS, Kim KC. (2001). Involvement of the MAP kinase ERK2 in MUC1 mucin signaling. Am J Physiol Lung Cell Mol Physiol 281: L86-L91. (Pubitemid 32927361)
59. Moniaux N, Chaturvedi P, Varshney GC, Meza JL, Rodriguez-Sierra JF, Aubert JP et al. (2007). Human MUC4 mucin induces ultra-structural changes and tumorigenicity in pancreatic cancer cells. Br J Cancer 97: 345-357. (Pubitemid 47196741)
60. Moniaux N, Escande F, Porchet N, Aubert JP, Batra SK. (2001). Structural organization and classification of the human mucin genes. Front Biosci 6: D1192-D1206.
61. Moniaux N, Junker WM, Singh AP, Jones AM, Batra SK. (2006). Characterization of human mucin MUC17. Complete coding sequence and organization. J Biol Chem 281: 23676-23685. (Pubitemid 44274143)
62. Moniaux N, Nollet S, Porchet N, Degand P, Laine A, Aubert JP. (1999). Complete sequence of the human mucin MUC4: a putative cell membrane-associated mucin. Biochem J 338: 325-333. (Pubitemid 129512255)
63. Nakamura T, Kuwai T, Kitadai Y, Sasaki T, Fan D, Coombes KR et al. (2007). Zonal heterogeneity for gene expression in human pancreatic carcinoma. Cancer Res 67: 7597-7604. (Pubitemid 47281351)
64. Nemoto S, Finkel T. (2002). Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295: 2450-2452. (Pubitemid 34270258)
65. O'Brien TJ, Beard JB, Underwood LJ, Dennis RA, Santin AD, York L. (2001). The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 22: 348-366. (Pubitemid 34062947)
66. O'Brien TJ, Beard JB, Underwood LJ, Shigemasa K. (2002). The CA 125 gene: a newly discovered extension of the glycosylated N-terminal domain doubles the size of this extracellular superstructure. Tumour Biol 23: 154-169. (Pubitemid 44858307)
67. Pallesen LT, Berglund L, Rasmussen LK, Petersen TE, Rasmussen JT. (2002). Isolation and characterization of MUC15, a novel cell membrane-associated mucin. Eur J Biochem 269: 2755-2763. (Pubitemid 34595643)
68. Park HU, Kim JW, Kim GE, Bae HI, Crawley SC, Yang SC et al. (2003). Aberrant expression of MUC3 and MUC4 membrane-associated mucins and sialyl Le(x) antigen in pancreatic intrae-pithelial neoplasia. Pancreas 26: e48-e54.
69. Patton S, Gendler SJ, Spicer AP. (1995). The epithelial mucin, MUC1, of milk, mammary gland and other tissues. Biochim Biophys Acta 1241: 407-423. (Pubitemid 26021828)
70. Pochampalli MR, el Bejjani RM, Schroeder JA. (2007). MUC1 is a novel regulator of ErbB1 receptor trafficking. Oncogene 26: 1693-1701.
71. Price-Schiavi SA, Andrechek E, Idris N, Li P, Rong M, Zhang J et al. (2005). Expression, location, and interactions of ErbB2 and its intramembrane ligand Muc4 (sialomucin complex) in rat mammary gland during pregnancy. J Cell Physiol 203: 44-53. (Pubitemid 40328171)
72. Raina D, Ahmad R, Kumar S, Ren J, Yoshida K, Kharbanda S et al. (2006). MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J 25: 3774-3783. (Pubitemid 44300263)
73. Raina D, Kharbanda S, Kufe D. (2004). The MUC1 oncoprotein activates the anti-apoptotic phosphoinositide 3-kinase/Akt and Bcl-xL pathways in rat 3Y1 fibroblasts. J Biol Chem 279: 20607-20612. (Pubitemid 38656454)
74. Ramsauer VP, Pino V, Farooq A, Carothers Carraway CA, Salas PJ, Carraway KL. (2006). Muc4-ErbB2 complex formation and signaling in polarized CACO-2 epithelial cells indicate that Muc4 acts as an unorthodox ligand for ErbB2. Mol Biol Cell 17: 2931-2941. (Pubitemid 43993498)
75. Ren J, Raina D, Chen W, Li G, Huang L, Kufe D. (2006). MUC1 oncoprotein functions in activation of fibroblast growth factor receptor signaling. Mol Cancer Res 4: 873-883. (Pubitemid 44877017)
76. Riese DJ, Stern DF. (1998). Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20: 41-48.
77. Roepstorff K, Grovdal L, Grandal M, Lerdrup M, van DB. (2008). Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem Cell Biol 129: 563-578.
78. Rump A, Morikawa Y, Tanaka M, Minami S, Umesaki N, Takeuchi M et al. (2004). Binding of ovarian cancer antigen CA125/MUC16 to mesothelin mediates cell adhesion. J Biol Chem 279: 9190-9198. (Pubitemid 38295982)
79. Saitou M, Goto M, Horinouchi M, Tamada S, Nagata K, Hamada T et al. (2005). MUC4 expression is a novel prognostic factor in patients with invasive ductal carcinoma of the pancreas. J Clin Pathol 58: 845-852. (Pubitemid 41113392)
80. Schlessinger J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
81. Scholler N, Garvik B, Hayden-Ledbetter M, Kline T, Urban N. (2007). Development of a CA125-mesothelin cell adhesion assay as a screening tool for biologics discovery. Cancer Lett 247: 130-136. (Pubitemid 44959415)
82. Schroeder JA, Masri AA, Adriance MC, Tessier JC, Kotlarczyk KL, Thompson MC et al. (2004). MUC1 overexpression results in mammary gland tumorigenesis and prolonged alveolar differentiation. Oncogene 23: 5739-5747.
83. Schroeder JA, Thompson MC, Gardner MM, Gendler SJ. (2001). Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J Biol Chem 276: 13057-13064. (Pubitemid 37385232)
84. Seelenmeyer C, Wegehingel S, Lechner J, Nickel W. (2003). The cancer antigen CA125 represents a novel counter receptor for galectin-1. J Cell Sci 116: 1305-1318. (Pubitemid 36410668)
85. Shibahara H, Tamada S, Higashi M, Goto M, Batra SK, Hollings-worth MA et al. (2004). MUC4 is a novel prognostic factor of intrahepatic cholangiocarcinoma-mass forming type. Hepatology 39: 220-229. (Pubitemid 38461485)
86. Shyu MK, Lin MC, Shih JC, Lee CN, Huang J, Liao CH et al. (2007). Mucin 15 is expressed in human placenta and suppresses invasion of trophoblast-like cells in vitro. Hum Reprod 22: 2723-2732. (Pubitemid 47434219)
87. Singh AP, Chauhan SC, Bafna S, Johansson SL, Smith LM, Moniaux N et al. (2006). Aberrant expression of transmembrane mucins, MUC1 and MUC4, in human prostate carcinomas. Prostate 66: 421-429. (Pubitemid 43348735)
88. Singh AP, Moniaux N, Chauhan SC, Meza JL, Batra SK. (2004). Inhibition of MUC4 expression suppresses pancreatic tumor cell growth and metastasis. Cancer Res 64: 622-630. (Pubitemid 38120902)
89. Singh PK, Hollingsworth MA. (2006). Cell surface-associated mucins in signal transduction. Trends Cell Biol 16: 467-476. (Pubitemid 44293402)
90. Singh PK, Wen Y, Swanson BJ, Shanmugam K, Kazlauskas A, Cerny RL et al. (2007). Platelet-derived growth factor receptor beta-mediated phosphorylation of MUC1 enhances invasiveness in pancreatic adenocarcinoma cells. Cancer Res 67: 5201-5210. (Pubitemid 46997258)
91. Swartz MJ, Batra SK, Varshney GC, Hollingsworth MA, Yeo CJ, Cameron JL et al. (2002). MUC4 expression increases progressively in pancreatic intraepithelial neoplasia. Am J Clin Pathol 117: 791-796.
92. Tamada S, Shibahara H, Higashi M, Goto M, Batra SK, Imai K et al. (2006). MUC4 is a novel prognostic factor of extrahepatic bile duct carcinoma. Clin Cancer Res 12: 4257-4264.
93. Taylor-Papadimitriou J, Burchell J, Miles DW, Dalziel M. (1999). MUC1 and cancer. Biochim Biophys Acta 1455: 301-313. (Pubitemid 29435996)
94. Tsutsumida H, Goto M, Kitajima S, Kubota I, Hirotsu Y, Wakimoto J et al. (2007). MUC4 expression correlates with poor prognosis in small-sized lung adenocarcinoma. Lung Cancer 55: 195-203. (Pubitemid 46074231)
95. Walsh MD, Young JP, Leggett BA, Williams SH, Jass JR, McGuckin MA. (2007). The MUC13 cell surface mucin is highly expressed by human colorectal carcinomas. Hum Pathol 38: 883-892.
96. Wei X, Xu H, Kufe D. (2005). Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer Cell 7: 167-178. (Pubitemid 40248342)
97. Wei X, Xu H, Kufe D. (2006). MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell 21: 295-305. (Pubitemid 43099944)
98. Williams SJ, Wreschner DH, Tran M, Eyre HJ, Sutherland GR, McGuckin MA. (2001). Muc13, a novel human cell surface mucin expressed by epithelial and hemopoietic cells. J Biol Chem 276: 18327-18336. (Pubitemid 37411406)
99. Workman HC, Sweeney C, Carraway III KL. (2009). The membrane mucin Muc4 inhibits apoptosis induced by multiple insults via ErbB2-dependent and ErbB2-independent mechanisms. Cancer Res 69: 2845-2852.
100. Yin L, Huang L, Kufe D. (2004). MUC1 oncoprotein activates the FOXO3a transcription factor in a survival response to oxidative stress. J Biol Chem 279: 45721-45727. (Pubitemid 39491562)
101. Yin L, Kharbanda S, Kufe D. (2009). MUC1 oncoprotein promotes autophagy in a survival response to glucose deprivation. Int J Oncol 34: 1691-1699.
102. Yin L, Li Y, Ren J, Kuwahara H, Kufe D. (2003). Human MUC1 carcinoma antigen regulates intracellular oxidant levels and the apoptotic response to oxidative stress. J Biol Chem 278: 35458-35464. (Pubitemid 37102316)
103. Yu D, Hung MC. (2000). Role of erbB2 in breast cancer chemosensi-tivity. Bioessays 22: 673-680. (Pubitemid 30457959)
104. Zeimet AG, Offner FA, Muller-Holzner E, Widschwendter M, Abendstein B, Fuith LC et al. (1998). Peritoneum and tissues of the female reproductive tract as physiological sources of CA-125. Tumour Biol 19: 275-282. (Pubitemid 28318438)
105. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, Rhodes JM et al. (2009). Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69: 6799-6806.