Pancreatic cancer counterattack: MUC4 mediates Fas-independent apoptosis of antigen-specific cytotoxic T lymphocyte

Oncology Reports

Volumn 31, Issue 4, 2014, Pages 1768-1776

  Zhu, Yi ^a,b   Zhang, Jing Jing ^a,b   Liang, Wen Biao ^b   Zhu, Rong ^c   Wang, Bin ^d   Miao, Yi ^a,b   Xu, Ze Kuan ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Jiangsu Province Academy of Clinical Medicine Institute of Tumor Biology ^*  (China)

^c FUDAN UNIVERSITY   (China)

^d THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

Apoptosis; Cytotoxic; MUC4; Pancreatic neoplasms; T lymphocytes

Indexed keywords

CD14 ANTIGEN; CD86 ANTIGEN; FAS ANTIGEN; FAS LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HLA DR ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 4; MUCIN 4; T6 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ADULT; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL SELECTION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE AMPLIFICATION; GENE INDUCTION; GENE SILENCING; HUMAN; HUMAN CELL; INCUBATION TIME; MALE; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; ANTIGENS, CD95; ANTIGENS, NEOPLASM; APOPTOSIS; BLOTTING, WESTERN; CANCER VACCINES; COCULTURE TECHNIQUES; FLOW CYTOMETRY; HUMANS; MALE; MUCIN-4; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, CYTOTOXIC; YOUNG ADULT;

EID: 84908128916     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2014.3016     Document Type: Article

References (48)

1. Wong HH and Lemoine NR: Biological approaches to therapy of pancreatic cancer. Pancreatology 8: 431-461, 2008.
2. Li J, Merl MY, Chabot J and Saif MW: Updates of adjuvant therapy in pancreatic cancer: where are we and where are we going? Highlights from the '2010 ASCO Annual Meeting'. Chicago, IL, USA. June 4-8, 2010. JOP 11: 310-312, 2010.
3. Porchet N, Nguyen VC, Dufosse J, et al: Molecular cloning and chromosomal localization of a novel human tracheo-bronchial mucin cDNA containing tandemly repeated sequences of 48 base pairs. Biochem Biophys Res Commun 175: 414-422, 1991.
4. Moniaux N, Nollet S, Porchet N, Degand P, Laine A and Aubert JP: Complete sequence of the human mucin MUC4: a putative cell membrane-associated mucin. Biochem J 338: 325-333, 1999.
5. Rachagani S, Torres MP, Moniaux N and Batra SK: Current status of mucins in the diagnosis and therapy of cancer. Biofactors 35: 509-527, 2009.
6. Torres MP, Chakraborty S, Souchek J and Batra SK: Mucin-based targeted pancreatic cancer therapy. Curr Pharm Des 18: 2472-2481, 2012.
7. Andrianifahanana M, Moniaux N, Schmied BM, et al: 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, 2001.
8. Jhala N, Jhala D, Vickers SM, et al: Biomarkers in diagnosis of pancreatic carcinoma in fine-needle aspirates. Am J Clin Pathol 126: 572-579, 2006.
9. Zhu Y, Zhang JJ, Zhu R, et al: The increase in the expression and hypomethylation of MUC4 gene with the progression of pancreatic ductal adenocarcinoma. Med Oncol 28 (Suppl 1): S175-S184, 2011.
10. Saitou M, Goto M, Horinouchi M, et al: MUC4 expression is a novel prognostic factor in patients with invasive ductal carcinoma of the pancreas. J Clin Pathol 58: 845-852, 2005.
11. Bafna S, Kaur S, Momi N and Batra SK: Pancreatic cancer cells resistance to gemcitabine: the role of MUC4 mucin. Br J Cancer 101: 1155-1161, 2009.
12. Chaturvedi P, Singh AP, Moniaux N, et al: 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, 2007.
13. Singh AP, Moniaux N, Chauhan SC, Meza JL and Batra SK: Inhibition of MUC4 expression suppresses pancreatic tumor cell growth and metastasis. Cancer Res 64: 622-630, 2004.
14. Rachagani S, Macha MA, Ponnusamy MP, et al: MUC4 potentiates invasion and metastasis of pancreatic cancer cells through stabilization of fibroblast growth factor receptor 1. Carcinogenesis 33: 1953-1964, 2012.
15. Wei J, Gao W, Wu J, et al: Dendritic cells expressing a combined PADRE/MUC4-derived polyepitope DNA vaccine induce multiple cytotoxic T-cell responses. Cancer Biother Radiopharm 23: 121-128, 2008.
16. Wu J, Wei J, Meng K, et al: Identification of an HLA-A*0201- restrictive CTL epitope from MUC4 for applicable vaccine therapy. Immunopharmacol Immunotoxicol 31: 468-476, 2009.
17. Gao WT, Zhang JJ, Zhu Y, et al: Pentamer guided HLA-restricted epitope identification for mucoprotein 4 antigen of pancreatic ductal adenocarcinoma. Zhonghua Wai Ke Za Zhi 48: 1416-1424, 2010 (In Chinese).
18. Singh AP, Chaturvedi P and Batra SK: Emerging roles of MUC4 in cancer: a novel target for diagnosis and therapy. Cancer Res 67: 433-436, 2007.
19. Hollingsworth MA and Swanson BJ: Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4: 45-60, 2004.
20. Qin Qin P, Su F, Xiao Yan W, et al: Distribution of human leucocyte antigen-A, -B and -DR alleles and haplotypes at high resolution in the population from Jiangsu province of China. Int J Immunogenet 38: 475-481, 2011.
21. Nagy P, Friedlander E, Tanner M, et al: Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 65: 473-482, 2005.
22. Workman HC, Sweeney C and Carraway KL III: The membrane mucin Muc4 inhibits apoptosis induced by multiple insults via ErbB2-dependent and ErbB2-independent mechanisms. Cancer Res 69: 2845-2852, 2009.
23. Moffat J, Grueneberg DA, Yang X, et al: A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124: 1283-1298, 2006.
24. Ma C, Zhang J, Durrin LK, et al: The BCL2 major breakpoint region (mbr) regulates gene expression. Oncogene 26: 2649-2657, 2007.
25. Kim GG, Donnenberg VS, Donnenberg AD, Gooding W and Whiteside TL: A novel multiparametric flow cytometry-based cytotoxicity assay simultaneously immunophenotypes effector cells: comparisons to a 4 h 51Cr-release assay. J Immunol Methods 325: 51-66, 2007.
26. Sedgwick JD, Riminton DS, Cyster JG and Korner H: Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol Today 21: 110-113, 2000.
27. Moss ML, Jin SL, Milla ME, et al: Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-α. Nature 385: 733-736, 1997.
28. Wiley SR, Schooley K, Smolak PJ, et al: Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682, 1995.
29. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A and Ashkenazi A: Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271: 12687-12690, 1996.
30. Komatsu M, Yee L and Carraway KL: Overexpression of sialomucin complex, a rat homologue of MUC4, inhibits tumor killing by lymphokine-activated killer cells. Cancer Res 59: 2229-2236, 1999.
31. Nagata S: Apoptosis by death factor. Cell 88: 355-365, 1997.
32. Krammer PH, Arnold R and Lavrik IN: Life and death in peripheral T cells. Nat Rev Immunol 7: 532-542, 2007.
33. Maher S, Toomey D, Condron C and Bouchier-Hayes D: Activation-induced cell death: the controversial role of Fas and Fas ligand in immune privilege and tumour counterattack. Immunol Cell Biol 80: 131-137, 2002.
34. Rivoltini L, Carrabba M, Huber V, et al: Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev 188: 97-113, 2002.
35. Igney FH, Behrens CK and Krammer PH: CD95L mediates tumor counterattack in vitro but induces neutrophil-independent tumor rejection in vivo. Int J Cancer 113: 78-87, 2005.
36. Derby MA, Snyder JT, Tse R, Alexander-Miller MA and Berzofsky JA: An abrupt and concordant initiation of apoptosis: antigen-dependent death of CD8+ CTL. Eur J Immunol 31: 2951-2959, 2001.
37. Khazaie K and von Boehmer H: The impact of CD4+CD25 + Treg on tumor specific CD8+ T cell cytotoxicity and cancer. Semin Cancer Biol 16: 124-136, 2006.
38. Miyara M and Sakaguchi S: Natural regulatory T cells: mechanisms of suppression. Trends Mol Med 13: 108-116, 2007.
39. Carraway KL, Perez A, Idris N, et al: 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, 2002.
40. Jepson S, Komatsu M, Haq B, et al: Muc4/sialomucin complex, the intramembrane ErbB2 ligand, induces specific phosphorylation of ErbB2 and enhances expression of p27kip, but does not activate mitogen-activated kinase or protein kinaseB/Akt pathways. Oncogene 21: 7524-7532, 2002.
41. Chaturvedi P, Singh AP, Chakraborty S, et al: MUC4 mucin interacts with and stabilizes the HER2 oncoprotein in human pancreatic cancer cells. Cancer Res 68: 2065-2070, 2008.
42. Carraway KL, Ramsauer VP, Haq B and Carothers Carraway CA: Cell signaling through membrane mucins. Bioessays 25: 66-71, 2003.
43. Carraway CA and Carraway KL: Sequestration and segregation of receptor kinases in epithelial cells: implications for ErbB2 oncogenesis. Sci STKE 2007: re3, 2007.
44. Desseyn JL, Tetaert D and Gouyer V: Architecture of the large membrane-bound mucins. Gene 410: 215-222, 2008.
45. Timpl R: Structure and biological activity of basement membrane proteins. Eur J Biochem 180: 487-502, 1989.
46. Mayer U, Kohfeldt E and Timpl R: Structural and genetic analysis of laminin-nidogen interaction. Ann NY Acad Sci 857: 130-142, 1998.
47. Ciccarelli FD, Doerks T and Bork P: AMOP, a protein module alternatively spliced in cancer cells. Trends Biochem Sci 27: 113-115, 2002.
48. Chaturvedi P, Singh AP and Batra SK: Structure, evolution, and biology of the MUC4 mucin. FASEB J 22: 966-981, 2008.