Epithelial-to-mesenchymal transition in paired human primary and recurrent glioblastomas

International Journal of Oncology

Volumn 46, Issue 6, 2015, Pages 2515-2525

  Kubelt, Carolin ^a   Hattermann, Kirsten ^b   Sebens, Susanne ^a   Mehdorn, H Maximilian ^a   Held Feindt, Janka ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Epithelial to mesenchymal transition; Glial to mesenchymal transition; Glioblastomas; Mesenchymal to epithelial transition; Primary; Recurrent; Temozolomide

Indexed keywords

BETA CATENIN; BIGLYCAN; CD11B ANTIGEN; CD31 ANTIGEN; DESMOPLAKIN; FIBRONECTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IONIZED CALCIUM BINDING ADAPTER MOLECULE 1; MESSENGER RNA; NERVE CELL ADHESION MOLECULE L1; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MARKER; UNCLASSIFIED DRUG; VIMENTIN; VON WILLEBRAND FACTOR; DACARBAZINE;

ARTICLE; CANCER CHEMOTHERAPY; CANCER PATIENT; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; T98G CELL LINE; TUMOR RECURRENCE; UPREGULATION; ANALOGS AND DERIVATIVES; BRAIN TUMOR; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BIOMARKERS, TUMOR; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; NEOPLASM RECURRENCE, LOCAL;

EID: 84928533123     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2944     Document Type: Article

References (37)

1. Gao D, Vahdat LT, Wong S, Chang JC and Mittal V: Microenvironmental regulation of epithelial-mesenchymal transitions in cancer. Cancer Res 72: 4883-4889, 2012.
2. Scheel C and Weinberg RA: Cancer stem cells and epithelial-mesenchymal transition: Concepts and molecular links. Semin Cancer Biol 22: 396-403, 2012.
3. Thiery JP: Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454, 2002.
4. Tsuji T, Ibaragi S and Hu GF: Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 69: 7135-7139, 2009.
5. Zavadil J, Haley J, Kalluri R, Muthuswamy SK and Thompson E: Epithelial-mesenchymal transition. Cancer Res 68: 9574-9577, 2008.
6. Tarin D, Thompson EW and Newgreen DF: The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 65: 5996-6001, 2005.
7. Thompson EW, Newgreen DF and Tarin D: Carcinoma invasion and metastasis: A role for epithelial-mesenchymal transition? Cancer Res 65: 5991-5995, 2005.
8. Yates C: Prostate tumor cell plasticity: A consequence of the microenvironment. Adv Exp Med Biol 720: 81-90, 2011.
9. Ohgaki H and Kleihues P: Epidemiology and etiology of gliomas. Acta Neuropathol 109: 93-108, 2005.
10. Kahlert UD, Nikkhah G and Maciaczyk J: Epithelial-to-mesenchymal(-like) transition as a relevant molecular event in malignant gliomas. Cancer Lett 331: 131-138, 2013.
11. Mahabir R, Tanino M, Elmansuri A, Wang L, Kimura T, Itoh T, Ohba Y, Nishihara H, Shirato H, Tsuda M and Tanaka S: Sustained elevation of Snail promotes glial-mesenchymal transition after irradiation in malignant glioma. Neuro-oncol 16: 671-685, 2014.
12. Mikheeva SA, Mikheev AM, Petit A, Beyer R, Oxford RG, Khorasani L, Maxwell J-P, Glackin CA, Wakimoto H, González-Herrero I, et al: TWIST1 promotes invasion through mesenchymal change in human glioblastoma. Mol Cancer 9: 194-211, 2010.
13. Pala A, Karpel-Massler G, Kast RE, Wirtz CR and Halatsch M-E: Epidermal to mesenchymal transition and failure of EGFR-targeted therapy in glioblastoma. Cancers (Basel) 4: 523-530, 2012.
14. Zarkoob H, Taube JH, Singh SK, Mani SA and Kohandel M: Investigating the link between molecular subtypes of glioblastoma, epithelial-mesenchymal transition, and CD133 cell surface protein. PLoS One 8: e64169, 2013.
15. Kahlert UD, Maciaczyk D, Doostkam S, Orr BA, Simons B, Bogiel T, Reithmeier T, Prinz M, Schubert J, Niedermann G, et al: Activation of canonical WNT/β-catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and other activators of epithelial-to-mesenchymal transition. Cancer Lett 325: 42-53, 2012.
16. Brabletz T: To differentiate or not - routes towards metastasis. Nat Rev Cancer 12: 425-436, 2012.
17. Xu J, Lamouille S and Derynck R: TGF-β-induced epithelial to mesenchymal transition. Cell Res 19: 156-172, 2009.
18. Qiao B, Johnson NW and Gao J: Epithelial-mesenchymal transition in oral squamous cell carcinoma triggered by transforming growth factor-beta1 is Snail family-dependent and correlates with matrix metalloproteinase-2 and -9 expressions. Int J Oncol 37: 663-668, 2010.
19. Held-Feindt J, Schmelz S, Hattermann K, Mentlein R, Mehdorn HM and Sebens S: The neural adhesion molecule L1CAM confers chemoresistance in human glioblastomas. Neurochem Int 61: 1183-1191, 2012.
20. Elias MC, Tozer KR, Silber JR, Mikheeva S, Deng M, Morrison RS, Manning TC, Silbergeld DL, Glackin CA, Reh TA and Rostomily RC: TWIST is expressed in human gliomas and promotes invasion. Neoplasia 7: 824-837, 2005.
21. Han SP, Kim JH, Han ME, Sim HE, Kim KS, Yoon S, Baek SY, Kim BS and Oh SO: SNAI1 is involved in the proliferation and migration of glioblastoma cells. Cell Mol Neurobiol 31: 489-496, 2011.
22. Yang HW, Menon LG, Black PM, Carroll RS and Johnson MD: SNAI2/Slug promotes growth and invasion in human gliomas. BMC Cancer 10: 301, 2010.
23. De Wever O, Pauwels P, De Craene B, Sabbah M, Emami S, Redeuilh G, Gespach C, Bracke M and Berx G: Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front. Histochem Cell Biol 130: 481-494, 2008.
24. Kim H, Watkinson J, Varadan V and Anastassiou D: Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Med Genomics 3: 51, 2010.
25. Cheng WY, Kandel JJ, Yamashiro DJ, Canoll P and Anastassiou D: A multi-cancer mesenchymal transition gene expression signature is associated with prolonged time to recurrence in glioblastoma. PLoS One 7: e34705, 2012.
26. Kaufhold S and Bonavida B: Central role of Snail1 in the regulation of EMT and resistance in cancer: A target for therapeutic intervention. J Exp Clin Cancer Res 33: 62, 2014.
27. Tong Y, Mentlein R, Buhl R, Hugo H-H, Krause J, Mehdorn HM and Held-Feindt J: Overexpression of midkine contributes to anti-apoptotic effects in human meningiomas. J Neurochem 100: 1097-1107, 2007.
28. Mentlein R, Forstreuter F, Mehdorn HM and Held-Feindt J: Functional significance of vascular endothelial growth factor receptor expression on human glioma cells. J Neurooncol 67: 9-18, 2004.
29. Hattermann K, Held-Feindt J, Lucius R, Müerköster SS, Penfold MET, Schall TJ and Mentlein R: The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res 70: 3299-3308, 2010.
30. Held-Feindt J, Hattermann K, Müerköster SS, Wedderkopp H, Knerlich-Lukoschus F, Ungefroren H, Mehdorn HM and Mentlein R: CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs). Exp Cell Res 316: 1553-1566, 2010.
31. Mechtersheimer S, Gutwein P, Agmon-Levin N, Stoeck A, Oleszewski M, Riedle S, Postina R, Fahrenholz F, Fogel M, Lemmon V and Altevogt P: Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J Cell Biol 155: 661-673, 2001.
32. Thiery JP: Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 15: 740-746, 2003.
33. Friedl P and Wolf K: Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 3: 362-374, 2003.
34. Myung JK, Choi SA, Kim S-K, Wang K-C and Park S-H: Snail plays an oncogenic role in glioblastoma by promoting epithelial mesenchymal transition. Int J Clin Exp Pathol 7: 1977-1987, 2014.
35. Velpula KK, Dasari VR, Tsung AJ, Dinh DH and Rao JS: Cord blood stem cells revert glioma stem cell EMT by down regulating transcriptional activation of Sox2 and Twist1. Oncotarget 2: 1028-1042, 2011.
36. Tsuzuki T, Izumoto S, Ohnishi T, Hiraga S, Arita N and Hayakawa T: Neural cell adhesion molecule L1 in gliomas: Correlation with TGF-beta and p53. J Clin Pathol 51: 13-17, 1998.
37. Geismann C, Arlt A, Bauer I, Pfeifer M, Schirmer U, Altevogt P, Müerköster SS and Schäfer H: Binding of the transcription factor Slug to the L1CAM promoter is essential for transforming growth factor-β71 (TGF-β)-induced L1CAM expression in human pancreatic ductal adenocarcinoma cells. Int J Oncol 38: 257-266, 2011.