Misregulated E-Cadherin expression associated with an aggressive brain tumor phenotype

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Lewis Tuffin, Laura J ^a   Rodriguez, Fausto ^b   Giannini, Caterina ^b   Scheithauer, Bernd ^b   Necela, Brian M ^a   Sarkaria, Jann N ^b   Anastasiadis, Panos Z ^a  

^a MAYO CLINIC   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UVOMORULIN; CADHERIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN TUMOR; CANCER INVASION; CELL CONTACT; CELL DIFFERENTIATION; CELL GROWTH; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GLIOBLASTOMA; GLIOMA; GLIOMA CELL; HUMAN; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PROGNOSIS; PROTEIN EXPRESSION; ANIMAL; CELL DIVISION; IMMUNOHISTOCHEMISTRY; METABOLISM; NUDE MOUSE; PATHOLOGY; RETROSPECTIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

MUS MUSCULUS;

ANIMALS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CADHERINS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE, TUMOR; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; RETROSPECTIVE STUDIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 78149423441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013665     Document Type: Article

References (60)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO Classification of tumours of the central nervous system; Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, eds. Lyon: IARC.
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, et al. (2007) The 2007 WHO classification of tumours of the central nervous system.[erratum appears in Acta Neuropathol. 2007 Nov;114(5):547]. Acta Neuropathol 114: 97-109.
3. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21: 1624-1636.
4. Takeichi M (1993) Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 5: 806-811.
5. Takeichi M (1995) Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7: 619-627.
6. Cavallaro U, Christofori G (2004) Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 4: 118-132.
7. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634.
8. Gumbiner BM (2000) Regulation of cadherin adhesive activity. J Cell Biol 148: 399-404.
9. Steinberg MS, McNutt PM (1999) Cadherins and their connections: adhesion junctions have broader functions. Curr Opin Cell Biol 11: 554-560.
10. Troyanovsky SM (1999) Mechanism of cell-cell adhesion complex assembly. Curr Opin Cell Biol 11: 561-566.
11. Anastasiadis PZ (2007) p120-ctn: A nexus for contextual signaling via Rho GTPases. Biochim Biophys Acta 1773: 34-46.
12. Nelson WJ, Nusse R (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483-1487.
13. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR (2008) Cadherin switching. J Cell Sci 121: 727-735.
14. Takeichi M, Nakagawa S, Aono S, Usui T, Uemura T (2000) Patterning of cell assemblies regulated by adhesion receptors of the cadherin superfamily. Philos Trans R Soc Lond B Biol Sci 355: 885-890.
15. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
16. Suzuki SC, Takeichi M (2008) Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50: S119-S130.
17. Takeichi M (2007) The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 8: 11-20.
18. Redies C (2000) Cadherins in the central nervous system. Prog Neurobiol 61: 611-648.
19. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
20. Schwechheimer K, Zhou L, Birchmeier W (1998) E-Cadherin in human brain tumours: loss of immunoreactivity in malignant meningiomas. Virchows Arch 432: 163-167.
21. Tohma Y, Yamashima T, Yamashita J (1992) Immunohistochemical localization of cell adhesion molecule epithelial cadherin in human arachnoid villi and meningiomas. Cancer Res 52: 1981-1987.
22. Howng SL, Wu CH, Cheng TS, Sy WD, Lin PC, et al. (2002) Differential expression of Wnt genes, beta-catenin and E-cadherin in human brain tumors. Cancer Lett 183: 95-101.
23. Asano K, Kubo O, Tajika Y, Huang MC, Takakura K, et al. (1997) Expression and role of cadherins in astrocytic tumors. Brain Tumor Pathol 14: 27-33.
24. Asano K, Kubo O, Tajika Y, Takakura K, Suzuki S (2000) Expression of cadherin and CSF dissemination in malignant astrocytic tumors. Neurosurg Rev 23: 39-44.
25. Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S, et al. (2002) Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J Neurooncol 57: 187-192.
26. Karpowicz P, Willaime-Morawek S, Balenci L, DeVeale B, Inoue T, et al. (2009) E-Cadherin regulates neural stem cell self-renewal. J Neurosci 29: 3885-3896.
27. Motta FJ, Valera ET, Lucio-Eterovic AK, Queiroz RG, Neder L, et al. (2008) Differential expression of E-cadherin gene in human neuroepithelial tumors. Genet Mol Res 7: 295-304.
28. Shinoura N, Paradies NE, Warnick RE, Chen H, Larson JJ, et al. (1995) Expression of N-cadherin and alpha-catenin in astrocytomas and glioblastomas. Br J Cancer 72: 627-633.
29. Asano K, Duntsch CD, Zhou Q, Weimar JD, Bordelon D, et al. (2004) Correlation of N-cadherin expression in high grade gliomas with tissue invasion. J Neurooncol 70: 3-15.
30. Barami K, Lewis-Tuffin L, Anastasiadis PZ (2006) The role of cadherins and catenins in gliomagenesis. Neurosurg Focus 21: e13.
31. Perego C, Vanoni C, Massari S, Raimondi A, Pola S, et al. (2002) Invasive behaviour of glioblastoma cell lines is associated with altered organisation of the cadherin-catenin adhesion system. J Cell Sci 115: 3331-3340.
32. Xia M, Hu M, Wang J, Xu Y, Chen X, et al. (2010) Identification of the role of Smad interacting protein 1 (SIP1) in glioma. J Neurooncol 97: 225-232.
33. Rodriguez FJ, Scheithauer BW, Giannini C, Bryant SC, Jenkins RB (2008) Epithelial and pseudoepithelial differentiation in glioblastoma and gliosarcoma: a comparative morphologic and molecular genetic study. Cancer 113: 2779-2789.
34. Kislin KL, McDonough WS, Eschbacher JM, Armstrong BA, Berens ME (2009) NHERF-1: modulator of glioblastoma cell migration and invasion. Neoplasia 11: 377-387.
35. Ordonez NG (2003) Value of E-cadherin and N-cadherin immunostaining in the diagnosis of mesothelioma. Hum Pathol 34: 749-755.
36. Ohgaki H, Kleihues P (2007) Genetic pathways to primary and secondary glioblastoma. Am J Pathol 170: 1445-1453.
37. De Leeuw WJ, Berx G, Vos CB, Peterse JL, Van de Vijver MJ, et al. (1997) Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situ. J Pathol 183: 404-411.
38. Giannini C, Sarkaria JN, Saito A, Uhm JH, Galanis E, et al. (2005) Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 7: 164-176.
39. Leuraud P, Taillandier L, Aguirre-Cruz L, Medioni J, Criniere E, et al. (2003) Correlation between genetic alterations and growth of human malignant glioma xenografted in nude mice. Br J Cancer 89: 2327-2332.
40. Pandita A, Aldape KD, Zadeh G, Guha A, James CD (2004) Contrasting in vivo and in vitro fates of glioblastoma cell subpopulations with amplified EGFR. Genes Chromosomes Cancer 39: 29-36.
41. Ozawa T, Wang J, Hu LJ, Lamborn KR, Bollen AW, et al. (1998) Characterization of human glioblastoma xenograft growth in athymic mice. In Vivo 12: 369-374.
42. Demuth T, Rennert JL, Hoelzinger DB, Reavie LB, Nakada M, et al. (2008) Glioma cells on the run - the migratory transcriptome of 10 human glioma cell lines. BMC Genomics 9: 54.
43. Christofori G, Semb H (1999) The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci 24: 73-76.
44. Wijnhoven BP, Dinjens WN, Pignatelli M (2000) E-cadherin-catenin cell-cell adhesion complex and human cancer. Br J Surg 87: 992-1005.
45. Soto E, Yanagisawa M, Marlow LA, Copland JA, Perez EA, et al. (2008) p120 catenin induces opposing effects on tumor cell growth depending on E-cadherin expression. J Cell Biol 183: 737-749.
46. Yanagisawa M, Anastasiadis PZ (2006) p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J Cell Biol 174: 1087-1096.
47. Reddy P, Liu L, Ren C, Lindgren P, Boman K, et al. (2005) Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 19: 2564-2578.
48. Sundfeldt K (2003) Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol Cell Endocrinol 202: 89-96.
49. Figarella-Branger D, Pellissier JF, Bouillot P, Bianco N, Mayan M, et al. (1994) Expression of neural cell-adhesion molecule isoforms and epithelial cadherin adhesion molecules in 47 human meningiomas: correlation with clinical and morphological data. Mod Pathol 7: 752-761.
50. du Plessis DG, Rutherfoord GS, Joyce KA, Walker C (2004) Phenotypic and genotypic characterization of glioblastoma multiforme with epithelial differentiation and adenoid formations. Clin Neuropathol 23: 141-148.
51. Ozolek JA, Finkelstein SD, Couce ME (2004) Gliosarcoma with epithelial differentiation: immunohistochemical and molecular characterization. A case report and review of the literature. Mod Pathol 17: 739-745.
52. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, et al. (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173.
53. Perez TD, Tamada M, Sheetz MP, Nelson WJ (2008) Immediate-early signaling induced by E-cadherin engagement and adhesion. J Biol Chem 283: 5014-5022.
54. Yamada S, Nelson WJ (2007) Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 178: 517-527.
55. Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
56. Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, et al. (2006) Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 12: 2264-2271.
57. Sarkaria JN, Yang L, Grogan PT, Kitange GJ, Carlson BL, et al. (2007) Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol Cancer Ther 6: 1167-1174.
58. Yang L, Clarke MJ, Carlson BL, Mladek AC, Schroeder MA, et al. (2008) PTEN loss does not predict for response to RAD001 (Everolimus) in a glioblastoma orthotopic xenograft test panel. Clin Cancer Res 14: 3993-4001.
59. Bible KC, Boerner SA, Kaufmann SH (1999) A one-step method for protein estimation in biological samples: nitration of tyrosine in nitric acid. Anal Biochem 267: 217-221.
60. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.