Wnt3a mediated activation of Wnt/β-catenin signaling promotes tumor progression in glioblastoma

Molecular and Cellular Neuroscience

Volumn 54, Issue , 2013, Pages 44-57

  Kaur, Navjot ^a   Chettiar, Sivarajan ^a   Rathod, Sachin ^a   Rath, Phalguni ^a   Muzumdar, Dattatraya ^b   Shaikh, M L ^a   Shiras, Anjali ^a  

^a NATIONAL CENTRE FOR CELL SCIENCE   (India)

^b KEM HOSPITAL   (India)

Author keywords

Cancer stem cells; CD133; Malignant transformation; Side population (SP); Temozolomide; Vascularization

Indexed keywords

BETA CATENIN; WNT PROTEIN; WNT3A PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CARCINOGENESIS; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLIOBLASTOMA; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; TRANSCRIPTION, GENETIC; WNT SIGNALING PATHWAY; WNT1 PROTEIN; WNT3A PROTEIN;

EID: 84873649097     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.01.001     Document Type: Article

References (69)

1. Abla A.A., Turner J.D., Sanai N. FoxM1 is vital in the Wnt/beta-catenin signaling pathogenesis of gliomas. World Neurosurg. 2012, 77:594-596.
2. Alexson T.O., Hitoshi S., Coles B.L., Bernstein A., van der Kooy D. Notch signaling is required to maintain all neural stem cell populations - irrespective of spatial or temporal niche. Dev Neurosci. 2006, 28:34-48.
3. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10:468-477.
4. Anzano M.A., Roberts A.B., Smith J.M., Sporn M.B., De larcot J.E. Sarcoma growth factor from conditioned medium of virally transformed cells is composed of both type a and type f8 transforming growth factors. Proc. Natl. Acad. Sci. USA. 1983, 80:6264-6268.
5. Augustin I., Goidts V., Bongers A., Kerr G., Vollert G., Radlwimmer B., Hartmann C., Herold-Mende C., Reifenberger G., von D.A., Boutros M. The Wnt secretion protein Evi/Gpr177 promotes glioma tumourigenesis. EMBO Mol. Med. 2012, 4:38-51.
6. Bachoo R.M., Maher E.A., Ligon K.L., Sharpless N.E., Chan S.S., You M.J., Tang Y., DeFrances J., Stover E., Weissleder R., Rowitch D.H., Louis D.N., dePinho R.A. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 2002, 1:269-277.
7. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
8. Beier D., Schulz J.B., Beier C.P. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol. Cancer 2011, 10:128.
9. Bowman A., Nusse R. Location, location, location: FoxM1 mediates beta-catenin nuclear translocation and promotes glioma tumorigenesis. Cancer Cell 2011, 20:415-416.
10. Burgess A.W., Faux M.C., Layton M.J., Ramsay R.G. Wnt signaling and colon tumorigenesis-a view from the periphery. Exp. Cell Res. 2011, 317:2748-2758.
11. Cadigan K.M. Wnt-beta-catenin signaling. Curr. Biol. 2008, 18:R943-R947.
12. Cadigan K.M. Wnt/beta-catenin signaling: turning the switch. Dev. Cell 2008, 14:322-323.
13. Carmo A., Carvalheiro H., Crespo I., Nunes I., Lopes M.C. Effect of temozolomide on the U-118 glioma cell line. Oncol. Lett. 2011, 2:1165-1170.
14. Chen Y.Y., Li B.A., Wang H.D., Liu X.Y., Tan G.W., Ma Y.H., Shen S.H., Zhu H.W., Wang Z.X. The role of Pygopus 2 in rat glioma cell growth. Med. Oncol. 2011, 28:631-640.
15. Chow M.L., Brambati S.M., Gorno-Tempini M.L., Miller B.L., Johnson J.K. Sound naming in neurodegenerative disease. Brain Cogn. 2010, 72:423-429.
16. Clark G.J., Cox A.D., Graham S.M., Der C.J. Biological assays for Ras transformation. Methods Enzymol. 1995, 255:395-412.
17. Clevers H., Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012, 149:1192-1205.
18. Dai C., Holland E.C. Glioma models. Biochim. Biophys. Acta 2001, 1551:M19-M27.
19. Dai C., Celestino J.C., Okada Y., Louis D.N., Fuller G.N., Holland E.C. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 2001, 15:1913-1925.
20. Daneman R., Agalliu D., Zhou L., Kuhnert F., Kuo C.J., Barres B.A. Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:641-646.
21. Faigle R., Song H. Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim. Biophys. Acta (BBA) 2013, 2435-2448.
22. Friel A.M., Sergent P.A., Patnaude C., Szotek P.P., Oliva E., Scadden D.T., Seiden M.V., Foster R., Rueda B.R. Functional analyses of the cancer stem cell-like properties of human endometrial tumor initiating cells. Cell Cycle 2008, 7:242-249.
23. Goodell M.A., Rosenzweig M., Kim H., Marks D.F., DeMaria M., Paradis G., Grupp S.A., Sieff C.A., Mulligan R.C., Johnson R.P. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med. 1997, 3:1337-1345.
24. Gopisetty G., Xu J., Sampath D., Colman H., Puduvalli V.K. Epigenetic regulation of CD133/PROM1 expression in glioma stem cells by Sp1/myc and promoter methylation. Oncogene 2012, 331:1-11.
25. Gotze S., Wolter M., Reifenberger G., Muller O., Sievers S. Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas. Int. J. Cancer 2010, 126:2584-2593.
26. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481:306-313.
27. Hadjipanayis C.G., Van Meir E.G. Brain cancer propagating cells: biology, genetics and targeted therapies. Trends Mol. Med. 2009, 15:519-530.
28. Howard B., Ashworth A. Signalling pathways implicated in early mammary gland morphogenesis and breast cancer. PLoS Genet. 2006, 2:e112.
29. Hu J., Dong A., Fernandez-Ruiz V., Shan J., Kawa M., Martinez-Anso E., Prieto J., Qian C. Blockade of Wnt signaling inhibits angiogenesis and tumor growth in hepatocellular carcinoma. Cancer Res. 2009, 69:6951-6959.
30. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
31. Jiang X., Yu Y., Yang H.W., Agar N.Y., Frado L., Johnson M.D. The imprinted gene PEG3 inhibits Wnt signaling and regulates glioma growth. J. Biol. Chem. 2010, 285:8472-8480.
32. Kamino M., Kishida M., Kibe T., Ikoma K., Iijima M., Hirano H., Tokudome M., Chen L., Koriyama C., Yamada K., Arita K., Kishida S. Wnt-5a signaling is correlated with infiltrative activity in human glioma by inducing cellular migration and MMP-2. Cancer Sci. 2011, 102:540-548.
33. Kanwar S.S., Yu Y., Nautiyal J., Patel B.B., Majumdar A.P. The Wnt/beta-catenin pathway regulates growth and maintenance of colonospheres. Mol. Cancer 2010, 9:212.
34. Kim Y., Kim K.H., Lee J., Lee Y.A., Kim M., Lee S.J., Park K., Yang H., Jin J., Joo K.M., Lee J., Nam D.H. Wnt activation is implicated in glioblastoma radioresistance. Lab. Invest. 2012, 92:466-473.
35. Le C.B., Rynkowski M., Le M.M., Bruyere C., Lonez C., Gras T., Haibe-Kains B., Bontempi G., Decaestecker C., Ruysschaert J.M., Kiss R., Lefranc F. Long-term in vitro treatment of human glioblastoma cells with temozolomide increases resistance in vivo through up-regulation of GLUT transporter and aldo-keto reductase enzyme AKR1C expression. Neoplasia 2010, 12:727-739.
36. Liang C.C., Park A.Y., Guan J.L. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2007, 2:329-333.
37. Liao D.J., Thakur A., Wu J., Biliran H., Sarkar F.H. Perspectives on c-Myc, Cyclin D1, and their interaction in cancer formation, progression, and response to chemotherapy. Crit. Rev. Oncog. 2007, 13:93-158.
38. Liebner S., Plate K.H. Differentiation of the brain vasculature: the answer came blowing by the Wnt. J. Angiogenes. Res. 2010, 2:1.
39. Liu X., Wang L., Zhao S., Ji X., Luo Y., Ling F. beta-Catenin overexpression in malignant glioma and its role in proliferation and apoptosis in glioblastma cells. Med. Oncol. 2011, 28:608-614.
40. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
41. Martinez R. Beyond genetics in glioma pathways: the ever-increasing crosstalk between epigenomic and genomic events. J. Signal Transduct. 2012, 2012:519807.
42. Minde D.P., Anvarian Z., Rudiger S.G., Maurice M.M. Messing up disorder: how do missense mutations in the tumor suppressor protein APC lead to cancer?. Mol. Cancer 2011, 10:101.
43. Morin P.J. beta-Catenin signaling and cancer. Bioessays 1999, 21:1021-1030.
44. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
45. Nakazato Y. Revised WHO classification of brain tumours. Brain Nerve 2008, 60:59-77.
46. Nusse R., Varmus H. Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J. 2012, 31:2670-2684.
47. Ozawa T., James C.D. Establishing intracranial brain tumor xenografts with subsequent analysis of tumor growth and response to therapy using bioluminescence imaging. J. Vis. Exp. 2010, 41:e1986. (1-5).
48. Pu P., Zhang Z., Kang C., Jiang R., Jia Z., Wang G., Jiang H. Downregulation of Wnt2 and beta-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther. 2009, 16:351-361.
49. Reddy E.M., Chettiar S.T., Kaur N., Ganeshkumar R., Shepal V., Shanbhag N.C., Shiras A. Dlxin-1, a member of MAGE family, inhibits cell proliferation, invasion and tumorigenicity of glioma stem cells. Cancer Gene Ther. 2011, 18(3):206-218.
50. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia V.J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
51. Sanson M. Editorial review: targets for glioma treatment: from bench to bedside. Curr. Opin. Oncol. 2008, 20:650-651.
52. Sciuscio D., Diserens A.C., van Dommelen K., Martinet D., Jones G., Janzer R.C., Pollo C., Hamou M.F., Kaina B., Stupp R., Levivier M., Hegi M.E. Extent and patterns of MGMT promoter methylation in glioblastoma- and respective glioblastoma-derived spheres. Clin. Cancer Res. 2011, 17:255-266.
53. Shi Z., Qian X., Li L., Zhang J., Zhu S., Zhu J., Chen L., Zhang K., Han L., Yu S., Pu P., Jiang T., Kang C. Nuclear translocation of beta-catenin is essential for glioma cell survival. J. Neuroimmune Pharmacol. 2012, 4:892-903.
54. Shiras A., Bhosale A., Shepal V., Shukla R., Baburao V.S., Prabhakara K., Shastry P. A unique model system for tumor progression in GBM comprising two developed human neuro-epithelial cell lines with differential transforming potential and coexpressing neuronal and glial markers. Neoplasia 2003, 5:520-532.
55. Shiras A., Chettiar S.T., Shepal V., Rajendran G., Prasad G.R., Shastry P. Spontaneous transformation of human adult nontumorigenic stem cells to cancer stem cells is driven by genomic instability in a human model of glioblastoma. Stem Cells 2007, 25:1478-1489.
56. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
57. Stiles C.D., Rowitch D.H. Glioma stem cells: a midterm exam. Neuron 2008, 58:832-846.
58. Su Y., Fu C., Ishikawa S., Stella A., Kojima M., Shitoh K., Schreiber E.M., Day B.W., Liu B. APC is essential for targeting phosphorylated beta-catenin to the SCFbeta-TrCP ubiquitin ligase. Mol. Cell 2008, 32:652-661.
59. Tanaka K., Kitagawa Y., Kadowaki T. Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J. Biol. Chem. 2002, 277:12816-12823.
60. Tang X.N., Berman A.E., Swanson R.A., Yenari M.A. Digitally quantifying cerebral hemorrhage using Photoshop and Image J. J. Neurosci. Methods 2010, 190:240-243.
61. Thon N., Eigenbrod S., Grasbon-Frodl E.M., Lutz J., Kreth S., Popperl G., Belka C., Kretzschmar H.A., Tonn J.C., Kreth F.W. Predominant influence of MGMT methylation in non-resectable glioblastoma after radiotherapy plus temozolomide. J. Neurol. Neurosurg. Psychiatry 2011, 82:441-446.
62. Utsuki S., Sato Y., Oka H., Tsuchiya B., Suzuki S., Fujii K. Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J. Neurooncol. 2002, 57:187-192.
63. Vermeulen L., De Sousa E., Melo F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., Sprick M.R., Kemper K., Richel D.J., Stassi G., Medema J.P. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 468-476.
64. Wang J., Guo L.P., Chen L.Z., Zeng Y.X., Lu S.H. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res. 2007, 67:3716-3724.
65. Yamamoto H., Oue N., Sato A., Hasegawa Y., Yamamoto H., Matsubara A., Yasui W., Kikuchi A. Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 2010, 29:2036-2046.
66. Yang C., Iyer R.R., Yu A.C., Yong R.L., Park D.M., Weil R.J., Ikejiri B., Brady R.O., Lonser R.R., Zhuang Z. beta-Catenin signaling initiates the activation of astrocytes and its dysregulation contributes to the pathogenesis of astrocytomas. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6963-6968.
67. Zhang N., Wei P., Gong A., Chiu W.T., Lee H.T., Colman H., Huang H., Xue J., Liu M., Wang Y., Sawaya R., Xie K., Yung W.K., Medema R.H., He X., Huang S. FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011, 20:427-442.
68. Zheng H., Ying H., Yan H., Kimmelman A.C., Hiller D.J., Chen A.J., Perry S.R., Tonon G., Chu G.C., Ding Z., Stommel J.M., Dunn K.L., Wiedemeyer R., You M.J., Brennan C., Wang Y.A., Ligon K.L., Wong W.H., Chin L., DePinho R.A. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455:1129-1133.
69. Zheng H., Ying H., Wiedemeyer R., Yan H., Quayle S.N., Ivanova E.V., Paik J.H., Zhang H., Xiao Y., Perry S.R., Hu J., Vinjamoori A., Gan B., Sahin E., Chheda M.G., Brennan C., Wang Y.A., Hahn W.C., Chin L., dePinho R.A. PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 2010, 17:497-509.