MUC13 protects colorectal cancer cells from death by activating the NF-κB pathway and is a potential therapeutic target

Oncogene

Volumn 36, Issue 5, 2017, Pages 700-713

  Sheng, Y H ^a   He, Y ^a   Hasnain, S Z ^a   Wang, R ^a   Tong, H ^a   Clarke, D T ^b   Lourie, R ^a   Oancea, I ^a   Wong, K Y ^a   Lumley, J W ^c   Florin, T H ^a   Sutton, P ^d,e,f   Hooper, J D ^a   McMillan, N A ^b   McGuckin, M A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c WESLEY HOSPITAL   (Australia)

^d MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; CYCLOHEXIMIDE; CYTOCHROME C; DOXORUBICIN; ETOPOSIDE; FLUOROURACIL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MUCIN; MUCIN 1; MUCIN 13; OXALIPLATIN; PROTEIN BCL 2; PROTEIN BCL XL; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VINCRISTINE; ANTINEOPLASTIC ANTIMETABOLITE; BCL2L1 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR; LY64 PROTEIN, MOUSE; MEMBRANE ANTIGEN; MEMBRANE PROTEIN; MIC13 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PROTEIN BCL X;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER REGRESSION; CARCINOMA CELL; CELL DEATH; CELL SURFACE; CELL SURVIVAL; COLORECTAL CANCER; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE RESPONSE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED PERIODIC SYNDROME; UPREGULATION; ANIMAL; BIOSYNTHESIS; COLORECTAL NEOPLASMS; GENETICS; HT-29 CELL LINE; METABOLISM; MOLECULARLY TARGETED THERAPY; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIGENS, SURFACE; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; BCL-X PROTEIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; EPIDERMAL GROWTH FACTOR; FLUOROURACIL; HETEROGRAFTS; HT29 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; MITOCHONDRIAL PROTEINS; MOLECULAR TARGETED THERAPY; NF-KAPPA B; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84978139065     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.241     Document Type: Article

References (44)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
2. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore Vdel G et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 2011; 334: 1129-1133.
3. McAuley JL, Linden SK, Png CW, King RM, Pennington HL, Gendler SJ et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007; 117: 2313-2324.
4. Sheng YH, Hasnain SZ, Florin TH, McGuckin MA. Mucins in Ibd and colorectal cancer. J Gastroenterol Hepatol 2011; 27: 28-30.
5. McGuckin MA, Linden SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011; 9: 265-278.
6. Jonckheere N, Skrypek N, Van Seuningen I. Mucins and tumor resistance to chemotherapeutic drugs. Biochim Biophys Acta 2014; 1846: 142-151.
7. Nath S, Mukherjee P. MUC1: A multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med 2014; 20: 332-342.
8. Andrianifahanana M, Moniaux N, Schmied BM, Ringel J, Friess H, Hollingsworth MA 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 2001; 7: 4033-4040.
9. Hollingsworth MA, Strawhecker JM, Caffrey TC, Mack DR. Expression of MUC1, MUC2, MUC3 and MUC4 mucin mRNAs in human pancreatic and intestinal tumor cell lines. Int J Cancer 1994; 57: 198-203.
10. McDermott KM, Crocker PR, Harris A, Burdick MD, Hinoda Y, Hayashi T et al. Overexpression of MUC1 reconfigures the binding properties of tumor cells. Int J Cancer 2001; 94: 783-791.
11. Swartz MJ, Batra SK, Varshney GC, Hollingsworth MA, Yeo CJ, Cameron JL et al. MUC4 expression increases progressively in pancreatic intraepithelial neoplasia. Am J Clin Pathol 2002; 117: 791-796.
12. Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 2009; 9: 874-885.
13. Kufe DW. MUC1-C oncoprotein as a target in breast cancer: Activation of signaling pathways and therapeutic approaches. Oncogene 2013; 32: 1073-1081.
14. Hollingsworth MA, Swanson BJ. Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 2004; 4: 45-60.
15. Nishii Y, Yamaguchi M, Kimura Y, Hasegawa T, Aburatani H, Uchida H et al. A newly developed anti-Mucin 13 monoclonal antibody targets pancreatic ductal adenocarcinoma cells. Int J Oncol 2015; 46: 1781-1787.
16. Shimamura T, Ito H, Shibahara J, Watanabe A, Hippo Y, Taniguchi H et al. Overexpression of MUC13 is associated with intestinal-type gastric cancer. Cancer Sci 2005; 96: 265-273.
17. Walsh MD, Young JP, Leggett BA, Williams SH, Jass JR, McGuckin MA. The MUC13 cell surface mucin is highly expressed by human colorectal carcinomas. Hum Pathol 2007; 38: 883-892.
18. Gupta BK, Maher DM, Ebeling MC, Stephenson PD, Puumala SE, Koch MR et al. Functions and regulation of MUC13 mucin in colon cancer cells. J Gastroenterol 2014; 49: 1378-1391.
19. Gupta BK, Maher DM, Ebeling MC, Sundram V, Koch MD, Lynch DW et al. Increased expression and aberrant localization of mucin 13 in metastatic colon cancer. J Histochem Cytochem 2012; 60: 822-831.
20. Khan S, Ebeling MC, Zaman MS, Sikander M, Yallapu MM, Chauhan N et al. MicroRNA-145 targets MUC13 and suppresses growth and invasion of pancreatic cancer. Oncotarget 2014; 5: 7599-7609.
21. Chauhan SC, Ebeling MC, Maher DM, Koch MD, Watanabe A, Aburatani H et al. MUC13 mucin augments pancreatic tumorigenesis. Mol Cancer Ther 2012; 11: 24-33.
22. Chauhan SC, Vannatta K, Ebeling MC, Vinayek N, Watanabe A, Pandey KK et al. Expression and functions of transmembrane mucin MUC13 in ovarian cancer. Cancer Res 2009; 69: 765-774.
23. Williams SJ, Wreschner DH, Tran M, Eyre HJ, Sutherland GR, McGuckin MA. Muc13, a novel human cell surface mucin expressed by epithelial and hemopoietic cells. J Biol Chem 2001; 276: 18327-18336.
24. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal Immunol 2008; 1: 183-197.
25. Sheng YH, Lourie R, Linden SK, Jeffery PL, Roche D, Tran TV et al. The MUC13 cell-surface mucin protects against intestinal inflammation by inhibiting epithelial cell apoptosis. Gut 2011; 60: 1661-1670.
26. Meier P, Vousden KH. Lucifer's labyrinth-ten years of path finding in cell death. Mol cell 2007; 28: 746-754.
27. Dolcet X, Llobet D, Pallares J, Matias-Guiu X. NF-kB in development and progression of human cancer. Virchows Arch 2005; 446: 475-482.
28. Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 2001; 107: 241-246.
29. Janssens S, Tinel A, Lippens S, Tschopp J. PIDD mediates NF-kappaB activation in response to DNA damage. Cell 2005; 123: 1079-1092.
30. Tsujimoto Y. Role of Bcl-2 family proteins in apoptosis: Apoptosomes or mitochondria. Genes Cells 1998; 3: 697-707.
31. Lin A, Karin M. NF-kappaB in cancer: A marked target. Semin Cancer biology 2003; 13: 107-114.
32. Sheng YH, Triyana S, Wang R, Das I, Gerloff K, Florin TH et al. MUC1 and MUC13 differentially regulate epithelial inflammation in response to inflammatory and infectious stimuli. Mucosal Immunol 2013; 6: 557-568.
33. Ahmad R, Raina D, Joshi MD, Kawano T, Ren J, Kharbanda S, Kufe D. MUC1-C oncoprotein functions as a direct activator of the nuclear factor-kappaB p65 transcription factor. Cancer Res 2009; 69: 7013-7021.
34. Ahmad R, Raina D, Trivedi V, Ren J, Rajabi H, Kharbanda S et al. MUC1 oncoprotein activates the IkappaB kinase beta complex and constitutive NF-kappaB signalling. Nat Cell Biol 2007; 9: 1419-1427.
35. Silke J, Vaux D. IAPs and Necroptotic Cell Death. Humana Press Inc: New York, NY, USA, 2014, pp 57-77.
36. Iwai K. Diverse ubiquitin signaling in NF-kappaB activation. Trends Cell Biol 2012; 22: 355-364.
37. Li N, Banin S, Ouyang H, Li GC, Courtois G, Shiloh Y et al. ATM is required for IkappaB kinase (IKKk) activation in response to DNA double strand breaks. J Biol Chem 2001; 276: 8898-8903.
38. Wu SY, Putral LN, Liang M, Chang HI, Davies NM, McMillan NA. Development of a novel method for formulating stable siRNA-loaded lipid particles for in vivo use. Pharm Res 2009; 26: 512-522.
39. Li F, Sethi G. Targeting transcription factor NF-kappaB to overcome chemoresistance and radioresistance in cancer therapy. Biochim Biophys Acta 2010; 1805: 167-180.
40. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006; 355: 1253-1261.
41. McCool KW, Miyamoto S. DNA damage-dependent NF-kappaB activation: NEMO turns nuclear signaling inside out. Immunol Rev 2012; 246: 311-326.
42. Breccia M, Alimena G. NF-kappaB as a potential therapeutic target in myelodysplastic syndromes and acute myeloid leukemia. Expert Opin Ther Targets 2010; 14: 1157-1176.
43. DiDonato JA, Mercurio F, Karin M. NF-kappaB and the link between inflammation and cancer. Immunol Rev 2012; 246: 379-400.
44. Deng M, Jing DD, Meng XJ. Effect of MUC1 siRNA on drug resistance of gastric cancer cells to trastuzumab. Asian Pac J Cancer Prev 2013; 14: 127-131.