Wnt/β-catenin signaling is a key downstream mediator of MET signaling in glioblastoma stem cells

Neuro-Oncology

Volumn 15, Issue 2, 2013, Pages 161-171

  Kim, Kang Ho ^a   Seol, Ho Jun ^a   Kim, Eun Hee ^b   Rheey, Jinguen ^c   Jin, Hyun Jin ^a   Lee, Yeri ^a   Joo, Kyeung Min ^a,d,e   Lee, Jeongwu ^b   Nam, Do Hyun ^a,e  

^a Samsung Medical Center   (South Korea)

^b LERNER RESEARCH INSTITUTE   (United States)

^c SAMSUNG Electronics   (South Korea)

^d Sungkyunkwan University School of Medicine   (South Korea)

^e Sungkyunkwan University   (South Korea)

Author keywords

Glioblastoma; Glioblastoma stem cell; Hepatocyte growth factor; MET protooncogene; Wnt bcatenin signaling

Indexed keywords

BETA CATENIN; SCATTER FACTOR RECEPTOR; SHORT HAIRPIN RNA; WNT PROTEIN;

ARTICLE; CELL SUBPOPULATION; CLONOGENESIS; DOWNSTREAM PROCESSING; FLOW CYTOMETRY; GLIOBLASTOMA; HUMAN; IMMUNOHISTOCHEMISTRY; MOLECULAR INTERACTION; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; TUMOR CELL; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HUMANS; IMMUNOENZYME TECHNIQUES; LUCIFERASES; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-MET; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; TUMOR STEM CELL ASSAY; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84875723571     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nos299     Document Type: Article

References (76)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996. (Pubitemid 40349501)
2. Liu G, Yuan X, Zeng Z, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.
3. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756-760. (Pubitemid 44949604)
4. Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488(7412):522-526.
5. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396-401. (Pubitemid 39551674)
6. Son MJ, Woolard K, Nam DH, Lee J, Fine HA. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell. 2009;4(5):440-452.
7. Lathia JD, Gallagher J, Heddleston JM, et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell. 2010;6(5):421-432.
8. He J, Liu Y, Xie X, et al. Identification of cell surface glycoprotein markers for glioblastoma-derived stem-like cells using a lectin microarray and LC-MS/MS approach. J Proteome Res. 2010;9(5):2565-2572.
9. Li Y, Li A, Glas M, et al. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci U S A. 2011;108(24):9951-9956.
10. Joo KM, Jin J, Kim E, et al. MET signaling regulates glioblastoma stem cells. Cancer Res. 2012;72(15):3828-3838.
11. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63(18):5821-5828. (Pubitemid 37187480)
12. Cooper CS, Park M, Blair DG, et al. Molecular cloning of a new transforming gene from a chemically transformed human cell line. Nature. 1984;311(5981):29-33. (Pubitemid 14065275)
13. Park M, Dean M, Cooper CS, et al. Mechanism of met oncogene activation. Cell. 1986;45(6):895-904. (Pubitemid 16083694)
14. Bottaro DP, Rubin JS, Faletto DL, et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science. 1991;251(4995):802-804. (Pubitemid 21926175)
15. Buchanan SG, Hendle J, Lee PS, et al. SGX523 is an exquisitely selective, ATP-competitive inhibitor of the MET receptor tyrosine kinase with antitumor activity in vivo.Mol Cancer Ther. 2009;8(12):3181-3190.
16. Lesko E,MajkaM.The biological role ofHGF-METaxis in tumor growth and development of metastasis. Front Biosci. 2008;13:1271-1280. (Pubitemid 351594710)
17. Lopez-Gines C, Cerda-Nicolas M, Gil-Benso R, et al. Association of chromosome 7, chromosome 10 and EGFR gene amplification in glioblastoma multiforme. Clin Neuropathol. 2005;24(5):209-218. (Pubitemid 41277337)
18. Fischer U, Wullich B, Sattler HP, Gottert E, Zang KD, Meese E. Coamplification on chromosomes 7p12-13 and 9q12-13 identified by reverse chromosome painting in a glioblastoma multiforme. Hum Genet. 1994;93(3):331-334. (Pubitemid 24066938)
19. Network CGAR. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216): 1061-1068.
20. Snuderl M, Fazlollahi L, Le LP, et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell. 2011;20(6): 810-817.
21. Koochekpour S, Jeffers M, Rulong S, et al. Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res. 1997;57(23):5391-5398. (Pubitemid 27516379)
22. Kong DS, Song SY, Kim DH, et al. Prognostic significance of c-Met expression in glioblastomas. Cancer. 2009;115(1):140-148.
23. Nabeshima K, Shimao Y, Sato S, et al. Expression of c-Met correlates with grade of malignancy in human astrocytic tumours: An immunohistochemical study. Histopathology. 1997;31(5):436-443. (Pubitemid 27505360)
24. Lal B, Xia S, Abounader R, Laterra J. Targeting the c-Met pathway potentiates glioblastoma responses to gamma-radiation. Clin Cancer Res. 2005;11(12):4479-4486. (Pubitemid 40825638)
25. Wen PY. American Society of Clinical Oncology 2010: Report of selected studies from the CNS tumors section. Expert Rev Anticancer Ther. 2010;10(9):1367-1369.
26. Zhang Y, Guessous F, Kofman A, Schiff D, Abounader R. XL-184, a MET, VEGFR-2 and RET kinase inhibitor for the treatment of thyroid cancer, glioblastoma multiforme and NSCLC. IDrugs. 2010;13(2): 112-121.
27. De Bacco F, Casanova E, Medico E, et al. The MET oncogene is a functional marker of a glioblastoma stem cell subtype. Cancer Res. 2012;72(17):4537-4550.
28. Bar EE, Chaudhry A, Lin A, et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells. 2007;25(10):2524-2533. (Pubitemid 47582744)
29. Fan X, Matsui W, Khaki L, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 2006;66(15):7445-7452. (Pubitemid 44289197)
30. Kim Y, Kim KH, Lee J, et al. Wnt activation is implicated in glioblastoma radioresistance. Lab Invest. 2012;92(3):466-473.
31. Piccirillo SG, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444(7120):761-765. (Pubitemid 44949605)
32. Joo KM, Nam DH. Prospective identification of cancer stem cells with the surface antigen CD133. Methods Mol Biol. 2009;568:57-71.
33. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403. (Pubitemid 43668737)
34. Joo KM, Kim SY, Jin X, et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest. 2008;88(8):808-815.
35. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003;100(25):15178-15183. (Pubitemid 37518036)
36. Hu Y, Smyth GK. ELDA: Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347(1-2):70-78.
37. Sattler M, Pride YB, Ma P, et al. A novel small molecule met inhibitor induces apoptosis in cells transformed by the oncogenic TPR-MET tyrosine kinase. Cancer Res. 2003;63(17):5462-5469. (Pubitemid 37139865)
38. Christensen JG, Schreck R, Burrows J, et al. A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res. 2003;63(21):7345-7355. (Pubitemid 37413476)
39. Wang W, Pan H, Murray K, Jefferson BS, Li Y. Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol. 2009;174(2):541-549.
40. Schenkel JM, Zloza A, Li W, Narasipura SD, Al-Harthi L. Beta-catenin signaling mediates CD4 expression on mature CD8+ T cells. J Immunol. 2010;185(4):2013-2019.
41. Zhang J, Huang K, Shi Z, et al. High beta-catenin/Tcf-4 activity confers glioma progression via direct regulation of AKT2 gene expression. Neuro Oncol. 2011;13(6):600-609.
42. van Noort M, Meeldijk J, van der Zee R, Destree O, Clevers H. Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem. 2002;277(20):17901-17905. (Pubitemid 34967600)
43. Conley SJ, Gheordunescu E, Kakarala P, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A. 2012;109(8):2784-2789.
44. Easwaran V, Song V, Polakis P, Byers S. The ubiquitin-proteasome pathway and serine kinase activity modulate adenomatous polyposis coli protein-mediated regulation of beta-catenin-lymphocyte enhancer-binding factor signaling. J Biol Chem. 1999;274(23): 16641-16645.
45. Porfiri E, Rubinfeld B, Albert I, Hovanes K, Waterman M, Polakis P. Induction of a beta-catenin-LEF-1 complex by wnt-1 and transforming mutants of beta-catenin. Oncogene. 1997;15(23):2833-2839. (Pubitemid 28004572)
46. Vermeulen L, De Sousa EMF, van der Heijden M, et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 2010;12(5):468-476.
47. King TD, Suto MJ, Li Y. The Wnt/beta-catenin signaling pathway: A potential therapeutic target in the treatment of triple negative breast cancer. J Cell Biochem. 2012;113(1):13-18.
48. Teng Y, Wang X, Wang Y, Ma D. Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun. 2010;392(3):373-379.
49. Yamashita T, Ji J, Budhu A, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136(3):1012-1024.
50. 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(2):608-614.
51. Liu C, Tu Y, Sun X, et al. Wnt/beta-Catenin pathway in human glioma: Expression pattern and clinical/prognostic correlations. Clin Exp Med. 2011;11(2):105-112.
52. Rossi M, Magnoni L, Miracco C, et al. beta-catenin and Gli1 are prognostic markers in glioblastoma. Cancer Biol Ther. 2011;11(8):753-761.
53. Zheng H, Ying H, Wiedemeyer R, et al. PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell. 2010;17(5):497-509.
54. Jin X, Jeon HY, Joo KM, et al. Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res. 2011;71(8):3066-3075.
55. Ponzo MG, Lesurf R, Petkiewicz S, et al. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc Natl Acad Sci U S A. 2009;106(31): 12903-12908.
56. Previdi S, Maroni P, Matteucci E, Broggini M, Bendinelli P, Desiderio MA. Interaction between human-breast cancer metastasis and bone microenvironment through activated hepatocyte growth factor/Met and beta-catenin/Wnt pathways. Eur J Cancer. 2010;46(9):1679-1691.
57. Pan FY, Zhang SZ, Xu N, et al. Beta-catenin signaling involves HGF-enhanced HepG2 scattering through activating MMP-7 transcription. Histochem Cell Biol. 2010;134(3):285-295.
58. Boon EM, Kovarikova M, Derksen PW, van der Neut R. MET signalling in primary colon epithelial cells leads to increased transformation irrespective of aberrant Wnt signalling. Br J Cancer. 2005;92(6):1078-1083. (Pubitemid 40546672)
59. Apte U, Zeng G, Muller P, et al. Activation of Wnt/beta-catenin pathway during hepatocyte growth factor-induced hepatomegaly in mice. Hepatology. 2006;44(4):992-1002. (Pubitemid 46499261)
60. Herynk MH, Tsan R, Radinsky R, Gallick GE. Activation of c-Met in colorectal carcinoma cells leads to constitutive association of tyrosinephosphorylated beta-catenin. Clin Exp Metastasis. 2003;20(4):291-300. (Pubitemid 36745657)
61. Monga SP, Mars WM, Pediaditakis P, et al. Hepatocyte growth factor induces Wnt-independent nuclear translocation of beta-catenin after Met-beta-catenin dissociation in hepatocytes. Cancer Res. 2002; 62(7):2064-2071. (Pubitemid 34408453)
62. Tamai K, Semenov M, Kato Y, et al. LDL-receptor-related proteins in Wnt signal transduction. Nature. 2000;407(6803):530-535.
63. Bilic J, Huang YL, Davidson G, et al. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science. 2007;316(5831):1619-1622. (Pubitemid 46982035)
64. Huang FI, Chen YL, Chang CL, Yuan RH, Jeng YM. Hepatocyte growth factor activates Wnt pathway by transcriptional activation of LEF1 to facilitate tumor invasion. Carcinogenesis. 2012;33(6): 1142-1148.
65. Liu Y, Chattopadhyay N, Qin S, et al. Coordinate integrin and c-Met signaling regulate Wnt gene expression during epithelial morphogenesis. Development. 2009;136(5):843-853.
66. Bertotti A, Bracco C, Girolami F, et al. Inhibition of Src impairs the growth of met-addicted gastric tumors. Clin Cancer Res. 2010; 16(15):3933-3943.
67. Papkoff J, Aikawa M. WNT-1 and HGF regulate GSK3 beta activity and beta-catenin signaling in mammary epithelial cells. Biochem Biophys Res Commun. 1998;247(3):851-858. (Pubitemid 28418480)
68. Ji H, Wang J, Nika H, et al. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-Catenin from beta-Catenin and transactivation of beta-Catenin. Mol Cell. 2009;36(4):547-559.
69. Yang W, Xia Y, Ji H, et al. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature. 2011;480(7375): 118-122.
70. Krejci P, Aklian A, Kaucka M, et al. Receptor tyrosine kinases activate canonical WNT/beta-catenin signaling via MAP kinase/LRP6 pathway and direct beta-catenin phosphorylation. PLoS One. 2012;7(4):e35826.
71. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell. 2003;4(6):499-515. (Pubitemid 38050046)
72. Jo M,Stolz DB, Esplen JE,Dorko K,MichalopoulosGK, StromSC. Cross-talk between epidermal growth factor receptor and c-Met signal pathways in transformed cells. J Biol Chem. 2000;275(12):8806-8811. (Pubitemid 30180235)
73. Karamouzis MV, Konstantinopoulos PA, Papavassiliou AG. Targeting MET as a strategy to overcome crosstalk-related resistance to EGFR inhibitors. Lancet Oncol. 2009;10(7):709-717.
74. Kawaguchi K, Murakami H, Taniguchi T, et al. Combined inhibition of MET and EGFR suppresses proliferation of malignant mesothelioma cells. Carcinogenesis. 2009;30(7):1097-1105.
75. Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science. 2007;318(5848):287-290. (Pubitemid 47574858)
76. Gupta PB, Kuperwasser C, Brunet JP, et al. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet. 2005;37(10):1047-1054. (Pubitemid 41486656)