MAGEC2, an epithelial-mesenchymal transition inducer, is associated with breast cancer metastasis

Breast Cancer Research and Treatment

Volumn 145, Issue 1, 2014, Pages 23-32

  Yang, Fan ^a   Zhou, Xingchun ^b   Miao, Xia ^b   Zhang, Tao ^a   Hang, Xiaojun ^b   Tie, Ru ^b   Liu, Nan ^b   Tian, Fei ^b   Wang, Fuli ^a   Yuan, Jianlin ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer; Clinical outcome; Epithelial to mesenchymal transition; MAGEC2; Metastasis

Indexed keywords

MELANOMA ANTIGEN; MELANOMA ANTIGEN C2 PROTEIN; UNCLASSIFIED DRUG; MAGEC2 PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST METASTASIS; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SURVIVAL RATE; ADULT; BREAST TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; PAGET NIPPLE DISEASE; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; RISK FACTOR; TISSUE MICROARRAY; TUMOR INVASION; WESTERN BLOTTING;

ADULT; ANTIGENS, NEOPLASM; BLOTTING, WESTERN; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PROGNOSIS; RISK FACTORS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84900489528     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-014-2915-9     Document Type: Article

References (48)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69-90. doi: 10.3322/caac.20107
2. Gupta GP, Massague J (2006) Cancer metastasis: building a framework. Cell 127(4):679-695. doi: 10.1016/j.cell.2006.11.001
3. Savagner P (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23(10):912-923. doi: 10.1002/bies.1132
4. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2(6):442-454. doi: 10.1038/nrc822
5. Thompson EW, Newgreen DF, Tarin D (2005) Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer res 65(14):5991-5995. doi: 10.1158/0008-5472.CAN-05-0616
6. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131-142. doi: 10.1038/nrm1835
7. Peinado H, Olmeda D, Cano A (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7(6):415-428. doi: 10.1038/nrc2131
8. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871-890. doi: 10.1016/j.cell.2009.11.007
9. Peinado H, Portillo F, Cano A (2004) Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 48(5-6):365-375. doi: 10.1387/ijdb.041794hp
10. De Craene B, Gilbert B, Stove C, Bruyneel E, van Roy F, Berx G (2005) The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res 65(14):6237-6244. doi: 10.1158/0008-5472.CAN-04-3545
11. Moreno-Bueno G, Cubillo E, Sarrio D, Peinado H, Rodriguez-Pinilla SM, Villa S, Bolos V, Jorda M, Fabra A, Portillo F, Palacios J, Cano A (2006) Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial-mesenchymal transition. Cancer Res 66(19):9543-9556. doi: 10.1158/0008-5472.CAN-06-0479
12. Qiao B, Johnson NW, Chen X, Li R, Tao Q, Gao J (2011) Disclosure of a stem cell phenotype in an oral squamous cell carcinoma cell line induced by BMP-4 via an epithelial-mesenchymal transition. Oncol Rep 26(2):455-461. doi: 10.3892/or.2011.1299
13. Coradini D, Fornili M, Ambrogi F, Boracchi P, Biganzoli E (2012) TP53 mutation, epithelial-mesenchymal transition, and stemlike features in breast cancer subtypes. J Biomed Biotechnol 2012:254085. doi: 10.1155/2012/254085
14. Costa FF, Le Blanc K, Brodin B (2007) Concise review: cancer/testis antigens, stem cells, and cancer. Stem Cells 25(3):707-711. doi: 10.1634/stemcells.2006-0469
15. Cronwright G, Le Blanc K, Gotherstrom C, Darcy P, Ehnman M, Brodin B (2005) Cancer/testis antigen expression in human mesenchymal stem cells: down-regulation of SSX impairs cell migration and matrix metalloproteinase 2 expression. Cancer Res 65(6):2207-2215. doi: 10.1158/0008-5472.CAN-04-1882
16. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T (1991) A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254(5038):1643-1647
17. Kasuga C, Nakahara Y, Ueda S, Hawkins C, Taylor MD, Smith CA, Rutka JT (2008) Expression of MAGE and GAGE genes in medulloblastoma and modulation of resistance to chemotherapy Laboratory investigation. J Neurosurg Pediatr 1(4):305-313. doi: 10.3171/PED/2008/1/4/305
18. Bolli M, Kocher T, Adamina M, Guller U, Dalquen P, Haas P, Mirlacher M, Gambazzi F, Harder F, Heberer M, Sauter G, Spagnoli GC (2002) Tissue microarray evaluation of Melanoma antigen E (MAGE) tumor-associated antigen expression: potential indications for specific immunotherapy and prognostic relevance in squamous cell lung carcinoma. Ann Surg 236(6):785-793. doi: 10.1097/01.SLA. 0000036266.09823.6C
19. Brasseur F, Rimoldi D, Lienard D, Lethe B, Carrel S, Arienti F, Suter L, Vanwijck R, Bourlond A, Humblet Y et al (1995) Expression of MAGE genes in primary and metastatic cutaneous melanoma. Int J Cancer 63(3):375-380
20. Brichard VG, Lejeune D (2007) GSK's antigen-specific cancer immunotherapy programme: pilot results leading to Phase III clinical development. Vaccine 25(Suppl 2):B61-B71. doi: 10.1016/j.vaccine.2007.06.038
21. Liu W, Cheng S, Asa SL, Ezzat S (2008) The melanoma-associated antigen A3 mediates fibronectin-controlled cancer progression and metastasis. Cancer Res 68(19):8104-8112. doi: 10.1158/0008-5472.CAN-08-2132
22. Gure AO, Chua R, Williamson B, Gonen M, Ferrera CA, Gnjatic S, Ritter G, Simpson AJ, Chen YT, Old LJ, Altorki NK (2005) Cancer-testis genes are coordinately expressed and are markers of poor outcome in non-small cell lung cancer. Clin Cancer Res 11(22):8055-8062. doi: 10.1158/1078-0432.CCR-05-1203
23. Miranda EI (2010) MAGE, biological functions and potential clinical applications. Leuk Res 34(9):1121-1122. doi: 10.1016/j.leukres.2010.03.045
24. Gure AO, Stockert E, Arden KC, Boyer AD, Viars CS, Scanlan MJ, Old LJ, Chen YT (2000) CT10: a new cancer-testis (CT) antigen homologous to CT7 and the MAGE family, identified by representational-difference analysis. Int J Cancer 85(5):726-732
25. Zhou X, Yang F, Zhang T, Zhuang R, Sun Y, Fang L, Zhang C, Ma Y, Huang G, Ma F, Song C, Jin B (2013) Heterogeneous expression of CT10, CT45 and GAGE7 antigens and their prognostic significance in human breast carcinoma. Jpn J Clin Oncol 43(3):243-250. doi: 10.1093/jjco/hys236
26. Bode PK, Barghorn A, Fritzsche FR, Riener MO, Kristiansen G, Knuth A, Moch H (2011) MAGEC2 is a sensitive and novel marker for seminoma: a tissue microarray analysis of 325 testicular germ cell tumors. Mod Pathol 24(6):829-835
27. von Boehmer L, Keller L, Mortezavi A, Provenzano M, Sais G, Hermanns T, Sulser T, Jungbluth AA, Old LJ, Kristiansen G, van den Broek M, Moch H, Knuth A, Wild PJ (2011) MAGE-C2/CT10 protein expression is an independent predictor of recurrence in prostate cancer. PLoS One 6(7):e21366. doi: 10.1371/journal.pone. 0021366
28. Pabst C, Zustin J, Jacobsen F, Luetkens T, Kroger N, Schilling G, Bokemeyer C, Sauter G, Atanackovic D, Marx A (2010) Expression and prognostic relevance of MAGE-C1/CT7 and MAGE-C2/CT10 in osteolytic lesions of patients with multiple myeloma. Exp Mol Pathol 89(2):175-181. doi: 10.1016/j.yexmp.2010.06. 011
29. Chen YT, Ross DS, Chiu R, Zhou XK, Chen YY, Lee P, Hoda SA, Simpson AJ, Old LJ, Caballero O, Neville AM (2011) Multiple cancer/testis antigens are preferentially expressed in hormone-receptor negative and high-grade breast cancers. PLoS One 6(3):e17876. doi: 10.1371/journal.pone.0017876
30. Adams S, Greeder L, Reich E, Shao Y, Fosina D, Hanson N, Tassello J, Singh B, Spagnoli GC, Demaria S, Jungbluth AA (2011) Expression of cancer testis antigens in human BRCA-associated breast cancers: potential targets for immunoprevention? Cancer Immunol Immunother 60(7):999-1007. doi: 10.1007/s00262-011-1005-7
31. Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP (1998) Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 4(7):844-847
32. Zhuang R, Zhu Y, Fang L, Liu XS, Tian Y, Chen LH, Ouyang WM, Xu XG, Jian JL, Gure AO, Fortunato S, Ritter G, Old LJ, Simpson AJ, Chen YT, Jin B, Jungbluth AA (2006) Generation of monoclonal antibodies to cancer/testis (CT) antigen CT10/MAGE-C2. Cancer immun 6:7
33. Sakaguchi H, Fujimoto J, Hong BL, Tamaya T (2007) Clinical implications of osteopontin in metastatic lesions of uterine cervical cancers. Cancer Lett 247(1):98-102. doi: 10.1016/j.canlet.2006.03.026
34. Zhou YC, Liu JY, Li J, Zhang J, Xu YQ, Zhang HW, Qiu LB, Ding GR, Su XM, Mei S, Guo GZ (2011) Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition. Int J Radiat Oncol Biol Phys 81(5):1530-1537. doi: 10.1016/j.ijrobp.2011.06.1956
35. Tang HR, Luo XQ, Xu G, Wang Y, Feng ZJ, Xu H, Shi YW, Zhang Q, Wu LG, Xue CQ, Wang CW, Wu CY (2012) High mobility group-box 3 overexpression is associated with poor prognosis of resected gastric adenocarcinoma. World J Gastroenterol 18(48):7319-7326. doi: 10.3748/wjg.v18.i48.7319
36. Curioni-Fontecedro A, Nuber N, Mihic-Probst D, Seifert B, Soldini D, Dummer R, Knuth A, van den Broek M, Moch H (2011) Expression of MAGE-C1/CT7 and MAGE-C2/CT10 predicts lymph node metastasis in melanoma patients. PLoS One 6(6):e21418. doi: 10.1371/journal.pone.0021418
37. Dunnwald LK, Rossing MA, Li CI (2007) Hormone receptor status, tumor characteristics, and prognosis: a prospective cohort of breast cancer patients. Breast Cancer Res 9(1):R6. doi: 10.1186/bcr1639
38. Germeau C, Ma W, Schiavetti F, Lurquin C, Henry E, Vigneron N, Brasseur F, Lethe B, De Plaen E, Velu T, Boon T, Coulie PG (2005) High frequency of antitumor T cells in the blood of melanoma patients before and after vaccination with tumor antigens. J Exp Med 201(2):241-248. doi: 10.1084/jem.20041379
39. Straetemans T, van Brakel M, van Steenbergen S, Broertjes M, Drexhage J, Hegmans J, Lambrecht BN, Lamers C, van Der Bruggen P, Coulie PG, Debets R (2012) TCR gene transfer: MAGE-C2/HLA-A2 and MAGE-A3/HLA-DP4 epitopes as melanoma-specific immune targets. Clin Dev Immunol 2012:586314. doi: 10.1155/2012/586314
40. Xiao TZ, Bhatia N, Urrutia R, Lomberk GA, Simpson A, Longley BJ (2011) MAGE I transcription factors regulate KAP1 and KRAB domain zinc finger transcription factor mediated gene repression. PLoS One 6(8):e23747. doi: 10.1371/journal.pone.0023747
41. Yang B, O'Herrin SM, Wu J, Reagan-Shaw S, Ma Y, Bhat KM, Gravekamp C, Setaluri V, Peters N, Hoffmann FM, Peng H, Ivanov AV, Simpson AJ, Longley BJ (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67(20):9954-9962. doi: 10.1158/0008-5472.CAN-07-1478
42. Cheung PY, Yip YL, Tsao SW, Ching YP, Cheung AL (2011) Id-1 induces cell invasiveness in immortalized epithelial cells by regulating cadherin switching and Rho GTPases. J Cell Biochem 112(1):157-168. doi: 10.1002/jcb.22911
43. Cubillo E, Diaz-Lopez A, Cuevas EP, Moreno-Bueno G, Peinado H, Montes A, Santos V, Portillo F, Cano A (2013) E47 and Id1 interplay in epithelial-mesenchymal transition. PLoS One 8(3):e59948. doi: 10.1371/journal.pone.0059948
44. Tobin NP, Sims AH, Lundgren KL, Lehn S, Landberg G (2011) Cyclin D1, Id1 and EMT in breast cancer. BMC Cancer 11:417. doi: 10.1186/1471-2407-11-417
45. Venkov CD, Link AJ, Jennings JL, Plieth D, Inoue T, Nagai K, Xu C, Dimitrova YN, Rauscher FJ, Neilson EG (2007) A proximal activator of transcription in epithelial-mesenchymal transition. J Clin Investig 117(2):482-491. doi: 10.1172/JCI29544
46. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133(4):704-715. doi: 10.1016/j.cell.2008.03.027
47. Ohman Forslund K, Nordqvist K (2001) The melanoma antigen genes-any clues to their functions in normal tissues? Exp Cell Res 265(2):185-194. doi: 10.1006/excr.2001.5173
48. Chen YT, Chiu R, Lee P, Beneck D, Jin B, Old LJ (2011) Chromosome X-encoded cancer/testis antigens show distinctive expression patterns in developing gonads and in testicular seminoma. Hum Reprod 26(12):3232-3243. doi: 10.1093/humrep/der330