The histone methyltransferase EZH2 mediates tumor progression on the chick chorioallantoic membrane assay, a novel model of head and neck squamous cell carcinoma

Translational Oncology

Volumn 6, Issue 3, 2013, Pages 273-281

  Liu, Min ^a   Scanlon, Christina Springstead ^a   Banerjee, Rajat ^a   Russo, Nickole ^a   Inglehart, Ronald C ^a   Willis, Amanda L ^b   Weiss, Stephen J ^b   D'Silva, Nisha J ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; TRANSCRIPTION FACTOR EZH2; UVOMORULIN; VIMENTIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICK; CHORIOALLANTOIS; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MICROSCOPY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR INVASION; TUMOR SEEDING; TUMOR VOLUME;

EID: 84878752709     PISSN: None     EISSN: 19365233     Source Type: Journal    
DOI: 10.1593/tlo.13175     Document Type: Article

References (37)

1. Leemans CR, Braakhuis BJ, and Brakenhoff RH (2011). The molecular biology of head and neck cancer. Nat Rev Cancer 11, 9-22.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, and Forman D (2011). Global cancer statistics. CA Cancer J Clin 61, 69-90.
3. Hanahan D and Weinberg RA (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
4. Rowe RG and Weiss SJ (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol 18, 560-574.
5. Van Tubergen EA, Banerjee R, Liu M, Vander Broek R, Light E, Shiuhyang K, Feinberg SE, Willis AL, Wolf G, Carey T, et al. (2013). Inactivation or loss of TTP promotes invasion in head and neck cancer via transcript stabilization and secretion of MMP9, MMP2, and IL-6. Clin Cancer Res 19, 1169-1179.
6. Stern CD (2005). The chick; a great model system becomes even greater. Dev Cell 8, 9-17.
7. Rous P (1911). A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J Exp Med 13, 397-411.
8. Stehelin D, Varmus HE, Bishop JM, and Vogt PK (1976). DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 260, 170-173.
9. Temin HM (1964). Homology between Rna from Rous sarcoma virous and DNA from Rous sarcoma virus-infected cells. Proc Natl Acad Sci USA 52, 323-329.
10. Levi-Montalcini R (1952). Effects of mouse tumor transplantation on the nervous system. Ann N Y Acad Sci 55, 330-344.
11. Murphy JB (1913). Transplantability of tissues to the embryo of foreign species: its bearing on questions of tissue specificity and tumor immunity. J Exp Med 17, 482-493.
12. Auerbach R, Arensman R, Kubai L, and Folkman J (1975). Tumor-induced angiogenesis: lack of inhibition by irradiation. Int J Cancer 15, 241-245.
13. Ossowski L and Reich E (1980). Experimental model for quantitative study of metastasis. Cancer Res 40, 2300-2309.
14. Rowe RG, Li XY, Hu Y, Saunders TL, Virtanen I, Garcia de Herreros A, Becker KF, Ingvarsen S, Engelholm LH, Bommer GT, et al. (2009). Mesenchymal cells reactivate Snail1 expression to drive three-dimensional invasion programs. J Cell Biol 184, 399-408.
15. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, et al. (2003). EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 100, 11606-11611.
16. Ota I, Li XY, Hu Y, and Weiss SJ (2009). Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci USA 106, 20318-20323.
17. Busch C, Krochmann J, and Drews U (2013). The chick embryo as an experimental system for melanoma cell invasion. PLoS One 8, e53970.
18. Banerjee R, Mani RS, Russo N, Scanlon CS, Tsodikov A, Jing X, Cao Q, Palanisamy N, Metwally T, Inglehart RC, et al. (2011). The tumor suppressor gene rap1GAP is silenced by miR-101-mediated EZH2 overexpression in invasive squamous cell carcinoma. Oncogene 30, 4339-4349.
19. Banerjee R, Russo N, Liu M, Van Tubergen E, and D'Silva NJ (2012). Rap1 and its regulatory proteins: the tumor suppressor, oncogene, tumor suppressor gene axis in head and neck cancer. Small GTPases 3, 192-197.
20. Mitra RS, Goto M, Lee JS, Maldonado D, Taylor JM, Pan Q, Carey TE, Bradford CR, Prince ME, Cordell KG, et al. (2008). Rap1GAP promotes invasion via induction of matrix metalloproteinase 9 secretion, which is associated with poor survival in low N-stage squamous cell carcinoma. Cancer Res 68, 3959-3969.
21. Mitra RS, Zhang Z, Henson BS, Kurnit DM, Carey TE, and D'Silva NJ (2003). Rap1A and rap1B ras-family proteins are prominently expressed in the nucleus of squamous carcinomas: nuclear translocation of GTP-bound active form. Oncogene 22, 6243-6256.
22. Goto M, Mitra RS, Liu M, Lee J, Henson BS, Carey T, Bradford C, Prince M, Wang CY, Fearon ER, et al. (2010). Rap1 stabilizes β-catenin and enhances β-catenin-dependent transcription and invasion in squamous cell carcinoma of the head and neck. Clin Cancer Res 16, 65-76.
23. Zhang Z, Mitra RS, Henson BS, Datta NS, McCauley LK, Kumar P, Lee JS, Carey TE, and D'Silva NJ (2006). Rap1GAP inhibits tumor growth in oropharyngeal squamous cell carcinoma. Am J Pathol 168, 585-596.
24. Zijlstra A, Mellor R, Panzarella G, Aimes RT, Hooper JD, Marchenko ND, and Quigley JP (2002). A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 62, 7083-7092.
25. van der Horst EH, Leupold JH, Schubbert R, Ullrich A, and Allgayer H (2004). TaqMan-based quantification of invasive cells in the chick embryo metastasis assay. Biotechniques 37, 940-942, 944, 946.
26. Zeidler M, Varambally S, Cao Q, Chinnaiyan AM, Ferguson DO, Merajver SD, and Kleer CG (2005). The polycomb group protein EZH2 impairs DNA repair in breast epithelial cells. Neoplasia 7, 1011-1019.
27. Raaphorst FM, Meijer CJ, Fieret E, Blokzijl T, Mommers E, Buerger H, Packeisen J, Sewalt RA, Otte AP, and van Diest PJ (2003). Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Neoplasia 5, 481-488.
28. Breuer RH, Snijders PJ, Smit EF, Sutedja TG, Sewalt RG, Otte AP, van Kemenade FJ, Postmus PE, Meijer CJ, and Raaphorst FM (2004). Increased expression of the EZH2 polycomb group gene in BMI-1-positive neoplastic cells during bronchial carcinogenesis. Neoplasia 6, 736-743.
29. Cao W, Ribeiro Rde O, Liu D, Saintigny P, Xia R, Xue Y, Lin R, Mao L, and Ren H (2012). EZH2 promotes malignant behaviors via cell cycle dysregulation and its mRNA level associates with prognosis of patient with non-small cell lung cancer. PLoS One 7, e52984.
30. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, Laxman B, Cao X, Jing X, Ramnarayanan K, et al. (2008). Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322, 1695-1699.
31. Sauvageau M and Sauvageau G (2010). Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 7, 299-313.
32. Crea F, Fornaro L, Bocci G, Sun L, Farrar WL, Falcone A, and Danesi R (2012). EZH2 inhibition: targeting the crossroad of tumor invasion and angiogenesis. Cancer Metastasis Rev 31, 753-761.
33. Lu C, Han HD, Mangala LS, Ali-Fehmi R, Newton CS, Ozbun L, Armaiz-Pena GN, Hu W, Stone RL, Munkarah A, et al. (2010). Regulation of tumor angiogenesis by EZH2. Cancer Cell 18, 185-197.
34. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH, Woodward WA, Hsu JM, Hortobagyi GN, and Hung MC (2011). EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-β-catenin signaling. Cancer Cell 19, 86-100.
35. Scanlon CS, Van Tubergen EA, Inglehart RC, and D'Silva NJ (2012). Biomarkers of epithelial-mesenchymal transition in squamous cell carcinoma. J Dent Res 92, 114-121.
36. Lokman NA, Elder AS, Ricciardelli C, and Oehler MK (2012). Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci 13, 9959-9970.
37. Zeisberg M and Neilson EG (2009). Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119, 1429-1437.