WNT/β-catenin signaling pathway and downstream modulators in low- and high-grade glioma

Cancer Genomics and Proteomics

Volumn 13, Issue 1, 2016, Pages 31-46

  Denysenko, Tetyana ^a,b   Annovazzi, Laura ^a   Cassoni, Paola ^c   Melcarne, Antonio ^b   Mellai, Marta ^a   Schiffer, Davide ^a  

^a Neuro bio oncology Center   (Italy)

^b CTO HOSPITAL   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Glioblastoma multiforme; Gliomas; Prognosis; TCF4; WNT3a; catenin

Indexed keywords

BETA CATENIN; CYCLIN D1; KI 67 ANTIGEN; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 4; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; TCF4 PROTEIN, HUMAN; WNT3A PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; BRAIN TUMOR CELL LINE; CANCER PATIENT; CANCER PROGNOSIS; CTNNB1 GENE; FEMALE; GENE; GENE MUTATION; GENE OVEREXPRESSION; GLIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; NUCLEAR LOCALIZATION SIGNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADOLESCENT; BRAIN TUMOR; CANCER GRADING; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; WNT SIGNALING PATHWAY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; BRAIN NEOPLASMS; FEMALE; GLIOMA; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; NEOPLASM GRADING; PROGNOSIS; RNA, MESSENGER; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY; WNT3A PROTEIN; YOUNG ADULT;

EID: 84959356679     PISSN: 11096535     EISSN: 17906245     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Logan CY and Nusse R: The WNT signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810, 2004.
2. Kobayashi M, Honma T, Matsuda Y, Suzuki Y, Narisawa R, Ajioka Y and Asakura H: Nuclear translocation of beta-catenin in colorectal cancer. Br J Cancer 82:1689-1693, 2000.
3. Koligs FT, Bommer G and Göke B: WNT/beta-catenin/tcf signaling: a critical pathway in gastrointestinal tumorigenesis. Digestion 66:131-144, 2002.
4. Iwai S, Katagiri W, Kong C, Amekawa S, Nakazawa M and Yura Y: Mutations of the APC, β-catenin, and axin 1 genes and cytoplasmic accumulation of beta-catenin in oral squamous cell carcinoma. J Cancer Res Clin Oncol 131:773-782, 2005.
5. De Panfilis G, Ferrari D, Santoro S, Ricci R, Lombardi M, Pedrazzi G, Pepe C, Cortelazzi C and Santini M: Cytoplasmic β-catenin is lacking in a subset of melanoma-associated naevi, but is detectable in naevus-associated melanomas: Potential implications for melanoma tumorigenesis? Br J Dermatol 160:600-608, 2009.
6. Heiser PW, Cano DA, Landsman L, Kim GE, Kench JG, Klimstra DS, Taketo MM, Biankin AV and Hebrok M: Stabilization of β-catenin induces pancreas tumor formation. Gastroenterology 135:1288-1300, 2008.
7. Clevers H: WNT/β-catenin signaling in development and disease. Cell 127:469-480, 2006.
8. Barker N: The canonical WNT/β-catenin signaling pathway. Methods Mol Biol 468:5-15, 2008.
9. MacDonald BT, Tamai K and He X: WNT/β-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26, 2009.
10. Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S and Fujii K: Relationship between the expression of E-, N-cadherins and β-catenin and tumor grade in astrocytomas. J Neurooncol 57:187-192, 2002.
11. Sareddy GR, Panigrahi M, Chala S, Mahadevan A and Babu PP: Activation of WNT/β-catenin/TCF signaling pathway in human astrocytomas. Neurochem Int 55:307-317, 2009.
12. Liu X, Wang L, Zhao S, Ji X, Luo Y and Ling F: β-Catenin overexpression in malignant glioma and its role in proliferation and apoptosis in glioblastoma cells. Med Oncol 28:608-614, 2011.
13. Zhang J, Huang K, Shi Z, Zou J, Wang Y, Jia Z, Zhang A, Han L, Yue X, Liu N, Jiang T, You Y, Pu P and Kang C: High β-catenin/TCF4 activity confers glioma progression via direct regulation of AKT2 gene expression. Neuro Oncol 13:600-609, 2011.
14. Schüle R, Dictus C, Campos B, Wan F, Felsberg J, Ahmadi R, Centner FS, Grabe N, Reifenberger G, Bermejo JL, Unterberg A and Herold-Mende C: Potential canonical WNT pathway activation in high-grade astrocytomas. Sci World J 2012:697313, 2012.
15. Yang C, Iyer RR, Yu AC, Yong RL, Park DM, Weil RJ, Ikejiri B, Brady RO, Lonser RR and Zhuang Z: β-Catenin signaling initiates the activation of astrocytes and its dysregulation contributes to the pathogenesis of astrocytomas. Proc Natl Acad Sci USA 109:6963-6968, 2012.
16. Kahlert UD, Maciaczyk D, Doostkam S, Orr BA, Simons B, Bogiel T, Reithmeier T, Prinz M, Schubert J, Niedermann G, Brabletz T, Eberhart CG, Nikkhah G and Maciaczyk J: 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.
17. Rossi M, Magnoni L, Miracco C, Mori E, Tosi P, Pirtoli L, Tini P, Oliveri G, Cosci E and Bakker A: β-Catenin and GLI1 are prognostic markers in glioblastoma. Cancer Biol Ther 11:753-761, 2011.
18. Liu C, Tu Y, Sun X, Jiang J, Jin X, Bo X, Li Z, Bian A, Wang X, Liu D, Wang Z and Ding L: WNT/β-catenin pathway in human glioma: expression pattern and clinical/prognostic correlations. Clin Exp Med 11:105-112, 2011.
19. Shi Z, Qian X, Li L, Zhang J, Zhu S, Zhu J, Chen L, Zhang K, Han L, Yu S, Pu P, Jiang T and Kang C: Nuclear translocation of β-catenin is essential for glioma cell survival. J Neuroimmune Pharmacol 7:892-903, 2012.
20. Yu JM, Kim JH, Song GS and Jung JS: Increase in proliferation and differentiation of neural progenitor cells isolated from postnatal and adult mice brain by WNT-3a and WNT-5a. Mol Cell Biochem 288:17-28, 2006.
21. David MD, Cantí C and Herreros J: WNT-3a and WNT-3 differently stimulate proliferation and neurogenesis of spinal neural precursors and promote neurite outgrowth by canonical signaling. J Neurosci Res 88:3011-3023, 2010.
22. Lee SM, Tole S, Grove E and McMahon AP: A local WNT-3a signal is required for development of the mammalian hippocampus. Development 127:457-467, 2000.
23. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y, Sawaya R, Xie K, Yung WK, Medema RH, He X and Huang S: FoxM1 promotes β-catenin nuclear localization and controls WNT target-gene expression and glioma tumorigenesis. Cancer Cell 20:427-442, 2011.
24. Riganti C, Salaroglio IC, Caldera V, Campia I, Kopecka J, Melai M, Annovazzi L, Bosia A, Ghigo D and Schiffer D: Temozolomide down-regulates P-glycoprotein expression in glioblastoma stem cells by interfering with the WNT3a/glycogen synthase-3 kinase/β-catenin pathway. Neuro Oncol 15:1502-1517, 2013.
25. Kaur N, Chettiar S, Rathod S, Rath P, Muzumdar D, Shaikh ML and Shiras A: WNT3a mediated activation of WNT/β-catenin signaling promotes tumor progression in glioblastoma. Mol Cell Neurosci 54:44-57, 2013.
26. Chen L, Huang K, Han L, Shi Z, Zhang K, Pu P, Jiang C and Kang C: β-catenin/TCF4 complex transcriptionally regulates AKT1 in glioma. Int J Oncol 39:883-890, 2011.
27. Pu P, Zhang Z, Kang C, Jiang R, Jia Z, Wang G and Jiang H: Down-regulation of WNT2 and β-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther 16:351-361, 2009.
28. Zhang ZQ, Chen HQ, Chen YH and Cheng XF: Significance of β-catenin and cyclin D1 express in glioma. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 25:1010-1012, 2009.
29. Klaus A and Birchmeier W: WNT signaling and its impact on development and cancer. Nat Rev Cancer 8:387-398, 2008.
30. Polakis P: WNT signaling and cancer. Genes Dev 14:1837-1851, 2000.
31. Eberhart CG, Tihan T and Burger PC: Nuclear localization and mutation of β-catenin in medulloblastomas. sJ Neuropathol Exp Neurol 59:333-337, 2000.
32. Johnson V, Volikos E, Halford SE, Eftekhar Sadat ET, Popat S, Talbot I, Truninger K, Martin J, Jass J, Houlston R, Atkin W, Tomlinson IP and Silver AR: Exon 3 β-catenin mutations are specifically associated with colorectal carcinomas in hereditary non-polyposis colorectal cancer syndrome. Gut 54:264-267, 2005.
33. Anastas JN and Moon RT: WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 13:11-26, 2013.
34. Gong A and Huang S: FOXM1 and WNT/β-catenin signaling in glioma stem cells. Cancer Res 72:5658-5662, 2012.
35. Nager M, Bhardwaj D, Cantí C, Medina L, Nogués P and Herreros J: β-Catenin signalling in glioblastoma multiforme and glioma-initiating cells. Chemother Res Pract 2012:192362, 2012.
36. Zheng H, Ying H, Wiedemeyer R, Yan H, Quayle SN, Ivanova EV, Paik JH, Zhang H, Xiao Y, Perry SR, Hu J, Vinjamoori A, Gan B, Sahin E, Chheda MG, Brennan C, Wang YA, Hahn WC, Chin L and DePinho RA: PLAGL2 regulates WNT signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 17:497-509, 2010.
37. Kim Y, Kim KH, Lee J, Lee YA, Kim M, Lee SJ, Park K, Yang H, Jin J, Joo KM, Lee J and Nam DH: WNT activation is implicated in glioblastoma radioresistance. Lab Invest 92:466-473, 2012.
38. Rheinbay E, Suvà ML, Gillespie SM, Wakimoto H, Patel AP, Shahid M, Oksuz O, Rabkin SD, Martuza RL, Rivera MN, Louis DN, Kasif S, Chi AS and Bernstein BE: An aberrant transcription factor network essential for WNT signaling and stem cell maintenance in glioblastoma. Cell Rep 3:1567-1579, 2013.
39. Shi L, Fei X, Wang Z and You Y: PI3K inhibitor combined with miR-125b inhibitor sensitize TMZ-induced anti-glioma stem cancer effects through inactivation of WNT/β-catenin signaling pathway. in vitro Cell Dev Biol Anim, Jul. 14, 2015 DOI: 10.1007/s11626-015-9931-x.
40. Lan F, Pan Q, Yu H and Yue X: Sulforaphane enhances temozolomide-induced apoptosis because of down-regulation of miR-21 via WNT/β-catenin signaling in glioblastoma. J Neurochem 134:811-818, 2015.
41. Louis DN, Ohgaki H, Wiestler OD, and Cavenee WK: WHO Classification of Tumours of the Central Nervous System. International Agency for Research on Cancer (IARC), Lyon, France, 4th edition, 2007.
42. Caldera V, Mellai M, Annovazzi L, Piazzi A, Lanotte M, Cassoni P and Schiffer D: Antigenic and genotypic similarity between primary glioblastomas and their derived neurospheres. J Oncol 2011:314962, 2011.
43. Galli R: The neurosphere assay applied to neural stem cells and cancer stem cells. Methods Mol Biol 986:267-277, 2013.
44. Melai M, Piazzi A, Caldera V, Monzeglio O, Cassoni P, Valente G and Schiffer D: IDH1 and IDH2 mutations, immunohistochemistry and associations in a series of brain tumors. J Neurooncol 105:345-357, 2011.
45. Mellai M, Monzeglio O, Piazzi A, Caldera V, Annovazzi L, Cassoni P, Valente G, Cordera S, Mocellini C and Schiffer D: MGMT promoter hypermethylation and its associations with genetic alterations in a series of 350 brain tumors. J Neurooncol 107:617-631, 2012.
46. Fodde R and Brabletz T: WNT/β-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19:150-158, 2007.
47. Kim KH, Seol HJ, Kim EH, Rheey J, Jin HJ, Lee Y, Joo KM, Lee J and Nam DH: WNT/β-catenin signaling is a key downstream mediator of MET signaling in glioblastoma stem cells. Neuro Oncol 15:161-171, 2013.
48. Holand JD, Klaus A, Garratt AN and Birchmeier W: WNT signaling in stem and cancer stem cells. Curr Opin Cell Biol 25:254-264, 2013.
49. Krieghoff E, Behrens J and Mayr B: Nucleo-cytoplasmic distribution of β-catenin is regulated by retention. J Cell Sci 119:1453-1463, 2006.
50. Götze S, Wolter M, Reifenberger G, Müler O and Sievers S: Frequent promoter hypermethylation of WNT pathway inhibitor genes in malignant astrocytic gliomas. Int J Cancer 126:2584-2593, 2010.
51. Yang Z, Wang Y, Fang J, Chen F, Liu J, Wu J, Wang Y, Song T, Zeng F and Rao Y: Downregulation of WIF1 by hypermethylation in astrocytomas. Acta Biochim Biophys Sin 42:418-425, 2010.
52. Lambiv WL, Vassalo I, Delorenzi M, Shay T, Diserens AC, Misra A, Feuerstein B, Murat A, Migliavacca E, Hamou MF, Sciuscio D, Burger R, Domany E Stupp R and Hegi ME: The WNT inhibitory factor 1 (WIF1) is targeted in glioblastoma and has a tumor-suppressing function potentially by induction of senescence. Neuro Oncol 13:736-747, 2011.
53. Wu J, Fang J, Yang Z, Chen F, Liu J and Wang Y: WNT-inhibitory factor-1 regulates glioblastoma cell cycle and proliferation. J Clin Neurosci 19:1428-1432, 2012.
54. Kim SA, Kwak J, Nam HY, Chun SM, Lee BW, Lee HJ, Khang SK and Kim SW: Promoter methylation of WNT inhibitory factor-1 and expression pattern of WNT/β-catenin pathway in human astrocytoma: pathologic and prognostic correlations. Mod Pathol 26:626-639, 2013.
55. Salaroli R, Di Tomaso T, Ronchi A, Ceccarelli C, Cammelli S, Cappellini A, Martinelli GN, Barbieri E, Giangaspero F and Cenacchi G: Radiobiologic response of medulloblastoma cell lines: involvement of β-catenin? J Neurooncol 90:243-251, 2008.
56. Yano H, Hara A, Takenaka K, Nakatani K, Shinoda J, Shimokawa K, Yoshimi N, Mori H and Sakai N: Differential expression of β-catenin in human glioblastoma multiforme and normal brain tissue. Neurol Res 22:650-656, 2000.
57. Jin X, Jeon HY, Joo KM, Kim JK, Jin J, Kim SH, Kang BG, Beck S, Lee SJ, Kim JK, Park AK, Park WY, Choi YJ, Nam DH and Kim H: Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res 71:3066-3075, 2011.
58. Reya T and Clevers H: WNT signaling in stem cells and cancer. Nature 434:843-850, 2005.
59. Toledo EM, Colombres M and Inestrosa NC: Signaling in neuroprotection and stem cell differentiation. Prog Neurobiol 86:281-296, 2008.
60. Wend P, Holand JD, Ziebold U and Birchmeier W: WNT signaling in stem and cancer stem cells. Semin Cell Dev Biol 21:855-863, 2010.
61. Pereira L, Yi F and Merrill BJ: Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 26:7479-7491, 2006.
62. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A and Weinberg RA: An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40:499-507, 2008.
63. Jiang X, Yu Y, Yang HW, Agar NY, Frado L and Johnson MD: The imprinted gene PEG3 inhibits WNT signaling and regulates glioma growth. J Biol Chem 285:8472-8480, 2010.
64. Flahaut M, Meier R, Coulon A, Nardou KA, Niggli FK, Martinet D, Beckmann JS, Joseph JM, Mühlethaler-Mottet A and Gross N: The WNT receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the WNT/β-catenin pathway. Oncogene 28:2245-2256, 2009.
65. Dandekar S, Romanos-Sirakis E, Pais F, Bhatla T, Jones C, Bourgeois W, Hunger SP, Raetz EA, Hermiston ML, Dasgupta R, Morrison DJ and Carrol WL: WNT inhibition leads to improved chemosensitivity in paediatric acute lymphoblastic leukaemia. Br J Haematol 167:87-99, 2014.
66. Elzagheid A, Buhmeida A, Korkeila E, Colan Y, Syrjanen K and Pyrhonen S: Nuclear β-catenin expression as a prognostic factor in advanced colorectal carcinoma. World J Gastroenterol 14:3866-3871, 2008.
67. Huang CL, Liu D, Ishikawa S, Nakashima T, Nakashima N, Yokomise H, Kadota K and Ueno M: WNT1 overexpression promotes tumour progression in non-small cell lung cancer. Eur J Cancer 44:2680-2688, 2008.