1,956
Views
46
CrossRef citations to date
0
Altmetric
Original Research

MUC1 upregulation promotes immune resistance in tumor cells undergoing brachyury-mediated epithelial-mesenchymal transition

, &
Article: e1117738 | Received 28 Aug 2015, Accepted 02 Nov 2015, Published online: 08 Apr 2016

References

  • Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006; 127:679-95; PMID:17110329; http://dx.doi.org/10.1016/j.cell.2006.11.001
  • Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013; 19:1438-49; PMID:24202396; http://dx.doi.org/10.1038/nm.3336
  • Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006; 66:8319-26; PMID:16951136; http://dx.doi.org/10.1158/0008-5472.CAN-06-0410
  • Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138:645-59; PMID:19682730; http://dx.doi.org/10.1016/j.cell.2009.06.034
  • Thomson S, Petti F, Sujka-Kwok I, Epstein D, Haley JD. Kinase switching in mesenchymal-like non-small cell lung cancer lines contributes to EGFR inhibitor resistance through pathway redundancy. Clin Exp Metastasis 2008; 25:843-54; PMID:18696232; http://dx.doi.org/10.1007/s10585-008-9200-4
  • Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A 2009; 106:13820-5; PMID:19666588; http://dx.doi.org/10.1073/pnas.0905718106
  • Showell C, Binder O, Conlon FL. T-box genes in early embryogenesis. Dev Dyn 2004; 229:201-18; PMID:14699590; http://dx.doi.org/10.1002/dvdy.10480
  • Fernando RI, Castillo MD, Litzinger M, Hamilton DH, Palena C. IL-8 signaling plays a critical role in the epithelial-mesenchymal transition of human carcinoma cells. Cancer Res 2011; 71:5296-306; PMID:21653678; http://dx.doi.org/10.1158/0008-5472.CAN-11-0156
  • Fernando RI, Litzinger M, Trono P, Hamilton DH, Schlom J, Palena C. The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. J Clin Invest 2010; 120:533-44; PMID:20071775; http://dx.doi.org/10.1172/JCI38379
  • Palena C, Polev DE, Tsang KY, Fernando RI, Litzinger M, Krukovskaya LL, Baranova AV, Kozlov AP, Schlom J. The human T-box mesodermal transcription factor Brachyury is a candidate target for T-cell-mediated cancer immunotherapy. Clin Cancer Res 2007; 13:2471-8; PMID:17438107; http://dx.doi.org/10.1158/1078-0432.CCR-06-2353
  • Palena C, Roselli M, Litzinger MT, Ferroni P, Costarelli L, Spila A, Cavaliere F, Huang B, Fernando RI, Hamilton DH et al. Overexpression of the EMT driver brachyury in breast carcinomas: association with poor prognosis. J Natl Cancer Inst 2014; 106(5); pii:dju054; PMID:24815864; http://dx.doi.org/10.1093/jnci/dju054
  • Roselli M, Fernando RI, Guadagni F, Spila A, Alessandroni J, Palmirotta R, Costarelli L, Litzinger M, Hamilton D, Huang B et al. Brachyury, a driver of the epithelial-mesenchymal transition, is overexpressed in human lung tumors: an opportunity for novel interventions against lung cancer. Clin Cancer Res 2012; 18:3868-79; PMID:22611028; http://dx.doi.org/10.1158/1078-0432.CCR-11-3211
  • Pinto F, Pertega-Gomes N, Pereira MS, Vizcaino JR, Monteiro P, Henrique RM, Baltazar F, Andrade RP, Reis RM. T-box transcription factor brachyury is associated with prostate cancer progression and aggressiveness. Clin Cancer Res 2014; 20:4949-61; PMID:25009296; http://dx.doi.org/10.1158/1078-0432.CCR-14-0421
  • Haro A, Yano T, Kohno M, Yoshida T, Koga T, Okamoto T, Takenoyama M, Maehara Y. Expression of Brachyury gene is a significant prognostic factor for primary lung carcinoma. Ann Surg Oncol 2013; 20(Suppl 3):S509-16; PMID:23456319; http://dx.doi.org/10.1245/s10434-013-2914-9
  • Tirabosco R, Mangham DC, Rosenberg AE, Vujovic S, Bousdras K, Pizzolitto S, De Maglio G, den Bakker MA, Di Francesco L, Kalil RK et al. Brachyury expression in extra-axial skeletal and soft tissue chordomas: a marker that distinguishes chordoma from mixed tumor/myoepithelioma/parachordoma in soft tissue. Am J Surg Pathol 2008; 32:572-80; PMID:18301055; http://dx.doi.org/10.1097/PAS.0b013e31815b693a
  • Vujovic S, Henderson S, Presneau N, Odell E, Jacques TS, Tirabosco R, Boshoff C, Flanagan AM. Brachyury, a crucial regulator of notochordal development, is a novel biomarker for chordomas. J Pathol 2006; 209:157-65; PMID:16538613; http://dx.doi.org/10.1002/path.1969
  • Kelley MJ, Shi J, Ballew B, Hyland PL, Li WQ, Rotunno M, Alcorta DA, Liebsch NJ, Mitchell J, Bass S et al. Characterization of T gene sequence variants and germline duplications in familial and sporadic chordoma. Hum Genet 2014; 133:1289-97; PMID:24990759; http://dx.doi.org/10.1007/s00439-014-1463-z
  • Yang XR, Ng D, Alcorta DA, Liebsch NJ, Sheridan E, Li S, Goldstein AM, Parry DM, Kelley MJ. T (brachyury) gene duplication confers major susceptibility to familial chordoma. Nat Genet 2009; 41:1176-8; PMID:19801981; http://dx.doi.org/10.1038/ng.454
  • Barresi V, Ieni A, Branca G, Tuccari G. Brachyury: a diagnostic marker for the differential diagnosis of chordoma and hemangioblastoma vs. neoplastic histological mimickers. Dis Markers 2014; 2014:514753; PMID:24591762; http://dx.doi.org/10.1155/2014/514753
  • Barresi V, Vitarelli E, Branca G, Antonelli M, Giangaspero F, Barresi G. Expression of brachyury in hemangioblastoma: potential use in differential diagnosis. Am J Surg Pathol 2012; 36:1052-7; PMID:22446946; http://dx.doi.org/10.1097/PAS.0b013e31824f4ce3
  • Huang B, Cohen JR, Fernando RI, Hamilton DH, Litzinger MT, Hodge JW, Palena C. The embryonic transcription factor Brachyury blocks cell cycle progression and mediates tumor resistance to conventional antitumor therapies. Cell Death Dis 2013; 4:e682; PMID:23788039; http://dx.doi.org/10.1038/cddis.2013.208
  • Larocca C, Cohen JR, Fernando RI, Huang B, Hamilton DH, Palena C. An autocrine loop between TGF-beta1 and the transcription factor brachyury controls the transition of human carcinoma cells into a mesenchymal phenotype. Mol Cancer Ther 2013; 12:1805-15; PMID:23783250; http://dx.doi.org/10.1158/1535-7163.MCT-12-1007
  • Kilic N, Feldhaus S, Kilic E, Tennstedt P, Wicklein D, Wasielewski R, Viebahn C, Kreipe H, Schumacher U. Brachyury expression predicts poor prognosis at early stages of colorectal cancer. Eur J Cancer 2011; 47:1080-5; PMID:21220197; http://dx.doi.org/10.1016/j.ejca.2010.11.015
  • Heery CR, Singh BH, Rauckhorst M, Marte JL, Donahue RN, Grenga I, Rodell TC, Dahut W, Arlen PM, Madan R et al. Phase I trial of a yeast-based therapeutic cancer vaccine (GI-6301) targeting the transcription factor brachyury. Cancer Immunol Res 2015; 3(11):1248-56; PMID:26130065; http://dx.doi.org/10.1158/2326-6066.CIR-15-0119
  • Safety and Tolerability of a Modified Vaccinia Ankara (MVA)-Based Vaccine Modified to Express Brachyury and T-cell Costimulatory Molecules (MVA-Brachyury-TRICOM). http://www.clinicaltrials.gov/, 2015
  • Hamilton DH, Huang B, Fernando RI, Tsang KY, Palena C. WEE1 inhibition alleviates resistance to immune attack of tumor cells undergoing epithelial-mesenchymal transition. Cancer Res 2014; 74:2510-9; PMID:24626094; http://dx.doi.org/10.1158/0008-5472.CAN-13-1894
  • Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 2009; 9:874-85; PMID:19935676; http://dx.doi.org/10.1038/nrc2761
  • Kufe DW. MUC1-C oncoprotein as a target in breast cancer: activation of signaling pathways and therapeutic approaches. Oncogene 2013; 32:1073-81; PMID:22580612; http://dx.doi.org/10.1038/onc.2012.158
  • Raina D, Kosugi M, Ahmad R, Panchamoorthy G, Rajabi H, Alam M, Shimamura T, Shapiro GI, Supko J, Kharbanda S et al. Dependence on the MUC1-C oncoprotein in non-small cell lung cancer cells. Mol Cancer Ther 2011; 10:806-16; PMID:21421804; http://dx.doi.org/10.1158/1535-7163.MCT-10-1050
  • Rajabi H, Alam M, Takahashi H, Kharbanda A, Guha M, Ahmad R, Kufe D. MUC1-C oncoprotein activates the ZEB1/miR-200c regulatory loop and epithelial-mesenchymal transition. Oncogene 2014; 33:1680-9; PMID:23584475; http://dx.doi.org/10.1038/onc.2013.114
  • Kharbanda A, Rajabi H, Jin C, Alam M, Wong KK, Kufe D. MUC1-C confers EMT and KRAS independence in mutant KRAS lung cancer cells. Oncotarget 2014; 5:8893-905; PMID:25245423; http://dx.doi.org/10.18632/oncotarget.2360
  • Takahashi H, Jin C, Rajabi H, Pitroda S, Alam M, Ahmad R, Raina D, Hasegawa M, Suzuki Y, Tagde A et al. MUC1-C activates the TAK1 inflammatory pathway in colon cancer. Oncogene 2015; 34(40):5187-97; PMID:25659581; http://dx.doi.org/10.1038/onc.2014.442
  • Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL, Bajaj E, Shanmugam K, Lee YY, Hwang SI et al. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 2011; 30:1449-59; PMID:21102519; http://dx.doi.org/10.1038/onc.2010.526
  • Alam M, Rajabi H, Ahmad R, Jin C, Kufe D. Targeting the MUC1-C oncoprotein inhibits self-renewal capacity of breast cancer cells. Oncotarget 2014; 5:2622-34; PMID:24770886; http://dx.doi.org/10.18632/oncotarget.1848
  • Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 2004; 5:163-75; PMID:14998492; http://dx.doi.org/10.1016/S1535-6108(04)00020-0
  • Ahmad R, Alam M, Rajabi H, Kufe D. The MUC1-C oncoprotein binds to the BH3 domain of the pro-apoptotic BAX protein and blocks BAX function. J Biol Chem 2012; 287:20866-75; PMID:22544745; http://dx.doi.org/10.1074/jbc.M112.357293
  • Kimura T, Finn OJ. MUC1 immunotherapy is here to stay. Expert Opin Biol Ther 2013; 13:35-49; PMID:22998452; http://dx.doi.org/10.1517/14712598.2012.725719
  • Leibovitz A, Stinson JC, McCombs WB, 3rd, McCoy CE, Mazur KC, Mabry ND. Classification of human colorectal adenocarcinoma cell lines. Cancer Res 1976; 36:4562-9; PMID:1000501
  • Buck E, Eyzaguirre A, Barr S, Thompson S, Sennello R, Young D, Iwata KK, Gibson NW, Cagnoni P, Haley JD. Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition. Mol Cancer Ther 2007; 6:532-41; PMID:17308052; http://dx.doi.org/10.1158/1535-7163.MCT-06-0462
  • Huang RY, Wong MK, Tan TZ, Kuay KT, Ng AH, Chung VY, Chu YS, Matsumura N, Lai HC, Lee YF et al. An EMT spectrum defines an anoikis-resistant and spheroidogenic intermediate mesenchymal state that is sensitive to e-cadherin restoration by a src-kinase inhibitor, saracatinib (AZD0530). Cell Death Dis 2013; 4:e915; PMID:24201814; http://dx.doi.org/10.1038/cddis.2013.442
  • Schliekelman MJ, Taguchi A, Zhu J, Dai X, Rodriguez J, Celiktas M, Zhang Q, Chin A, Wong CH, Wang H et al. Molecular portraits of epithelial, mesenchymal, and hybrid States in lung adenocarcinoma and their relevance to survival. Cancer Res 2015; 75:1789-800; PMID:25744723; http://dx.doi.org/10.1158/0008-5472.CAN-14-2535
  • Rajabi H, Jin C, Ahmad R, McClary C, Joshi MD, Kufe D. Mucin 1 oncoprotein expression is suppressed by the miR-125b oncomir. Genes Cancer 2010; 1:62-8; PMID:20729973; http://dx.doi.org/10.1177/1947601909357933
  • Sachdeva M, Mo YY. MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res 2010; 70:378-87; PMID:19996288; http://dx.doi.org/10.1158/0008-5472.CAN-09-2021
  • Jin C, Rajabi H, Kufe D. miR-1226 targets expression of the mucin 1 oncoprotein and induces cell death. Int J Oncol 2010; 37:61-9; PMID:20514397; http://dx.doi.org/10.3892/ijo_00000653
  • Agata N, Ahmad R, Kawano T, Raina D, Kharbanda S, Kufe D. MUC1 oncoprotein blocks death receptor-mediated apoptosis by inhibiting recruitment of caspase-8. Cancer Res 2008; 68:6136-44; PMID:18676836; http://dx.doi.org/10.1158/0008-5472.CAN-08-0464
  • Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007; 35:495-516; PMID:17562483; http://dx.doi.org/10.1080/01926230701320337
  • Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993; 197:40-5; PMID:8250945; http://dx.doi.org/10.1006/bbrc.1993.2438
  • Kataoka T, Shinohara N, Takayama H, Takaku K, Kondo S, Yonehara S, Nagai K. Concanamycin A, a powerful tool for characterization and estimation of contribution of perforin- and Fas-based lytic pathways in cell-mediated cytotoxicity. J Immunol 1996; 156:3678-86; PMID:8621902
  • Guaita S, Puig I, Franci C, Garrido M, Dominguez D, Batlle E, Sancho E, Dedhar S, De Herreros AG, Baulida J. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J Biol Chem 2002; 277:39209-16; PMID:12161443; http://dx.doi.org/10.1074/jbc.M206400200
  • Gnemmi V, Bouillez A, Gaudelot K, Hemon B, Ringot B, Pottier N, Glowacki F, Villers A, Vindrieux D, Cauffiez C et al. MUC1 drives epithelial-mesenchymal transition in renal carcinoma through Wnt/β-catenin pathway and interaction with SNAIL promoter. Cancer Lett 2014; 346:225-36; PMID:24384091; http://dx.doi.org/10.1016/j.canlet.2013.12.029
  • Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001; 412:95-9; PMID:11452314; http://dx.doi.org/10.1038/35083620
  • Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397:441-6; PMID:9989411; http://dx.doi.org/10.1038/17135
  • Beatty PL, Narayanan S, Gariepy J, Ranganathan S, Finn OJ. Vaccine against MUC1 antigen expressed in inflammatory bowel disease and cancer lessens colonic inflammation and prevents progression to colitis-associated colon cancer. Cancer Prevention Res (Philadelphia, Pa) 2010; 3:438-46; PMID:20332301; http://dx.doi.org/10.1158/1940-6207.CAPR-09-0194
  • Butts C, Maksymiuk A, Goss G, Soulieres D, Marshall E, Cormier Y, Ellis PM, Price A, Sawhney R, Beier F et al. Updated survival analysis in patients with stage IIIB or IV non-small-cell lung cancer receiving BLP25 liposome vaccine (L-BLP25): phase IIB randomized, multicenter, open-label trial. J Cancer Res Clin Oncol 2011; 137:1337-42; PMID:21744082; http://dx.doi.org/10.1007/s00432-011-1003-3
  • Mohebtash M, Tsang KY, Madan RA, Huen NY, Poole DJ, Jochems C, Jones J, Ferrara T, Heery CR, Arlen PM et al. A pilot study of MUC-1/CEA/TRICOM poxviral-based vaccine in patients with metastatic breast and ovarian cancer. Clin Cancer Res 2011; 17:7164-73; PMID:22068656; http://dx.doi.org/10.1158/1078-0432.CCR-11-0649
  • Morse MA, Niedzwiecki D, Marshall JL, Garrett C, Chang DZ, Aklilu M, Crocenzi TS, Cole DJ, Dessureault S, Hobeika AC et al. A randomized phase II study of immunization with dendritic cells modified with poxvectors encoding CEA and MUC1 compared with the same poxvectors plus GM-CSF for resected metastatic colorectal cancer. Annals Surg 2013; 258:879-86; PMID:23657083; http://dx.doi.org/10.1097/SLA.0b013e318292919e
  • Jochems C, Tucker JA, Vergati M, Boyerinas B, Gulley JL, Schlom J, Tsang KY. Identification and characterization of agonist epitopes of the MUC1-C oncoprotein. Cancer Immunol Immunotherapy 2014; 63:161-74; PMID:24233342; http://dx.doi.org/10.1007/s00262-013-1494-7
  • Hamilton DH, Litzinger MT, Jales A, Huang B, Fernando RI, Hodge JW, Ardiani A, Apelian D, Schlom J, Palena C. Immunological targeting of tumor cells undergoing an epithelial-mesenchymal transition via a recombinant brachyury-yeast vaccine. Oncotarget 2013; 4:1777-90; PMID:24125763; http://dx.doi.org/10.18632/oncotarget.1295
  • Kudo-Saito C, Shirako H, Ohike M, Tsukamoto N, Kawakami Y. CCL2 is critical for immunosuppression to promote cancer metastasis. Clin Exp Metastasis 2013; 30:393-405; PMID:23143679; http://dx.doi.org/10.1007/s10585-012-9545-6
  • Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 2009; 15:195-206; PMID:19249678; http://dx.doi.org/10.1016/j.ccr.2009.01.023
  • Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P, Bertheau P, Badoual C, Vielh P, Larsen AK et al. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res 2013; 73:2418-27; PMID:23436798; http://dx.doi.org/10.1158/0008-5472.CAN-12-2432
  • Raina D, Ahmad R, Joshi MD, Yin L, Wu Z, Kawano T, Vasir B, Avigan D, Kharbanda S, Kufe D. Direct targeting of the mucin 1 oncoprotein blocks survival and tumorigenicity of human breast carcinoma cells. Cancer Res 2009; 69:5133-41; PMID:19491255; http://dx.doi.org/10.1158/0008-5472.CAN-09-0854
  • Joshi MD, Ahmad R, Yin L, Raina D, Rajabi H, Bubley G, Kharbanda S, Kufe D. MUC1 oncoprotein is a druggable target in human prostate cancer cells. Mol Cancer Ther 2009; 8:3056-65; PMID:19887552; http://dx.doi.org/10.1158/1535-7163.MCT-09-0646
  • Hasegawa M, Sinha RK, Kumar M, Alam M, Yin L, Raina D, Kharbanda A, Panchamoorthy G, Gupta D, Singh H et al. Intracellular Targeting of the Oncogenic MUC1-C Protein with a Novel GO-203 Nanoparticle Formulation. Clin Cancer Res 2015; 21:2338-47; PMID:25712682; http://dx.doi.org/10.1158/1078-0432.CCR-14-3000
  • Hamilton DH, Fernando RI, Schlom J, Palena C. Aberrant expression of the embryonic transcription factor brachyury in human tumors detected with a novel rabbit monoclonal antibody. Oncotarget 2015; 6:4853-62; PMID:25605015; http://dx.doi.org/10.18632/oncotarget.3086