Modulation of the Wnt/beta-catenin pathway in human oligodendroglioma cells by Sox17 regulates proliferation and differentiation

Cancer Letters

Volumn 335, Issue 2, 2013, Pages 361-371

  Chen, Hui Ling ^a   Chew, Li Jin ^a   Packer, Roger J ^a   Gallo, Vittorio ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Cell cycle; Oligodendrocyte progenitor; Sonic hedgehog; Sox17; Wnt

Indexed keywords

BETA CATENIN; CYCLOPAMINE; MEMBRANE PROTEIN; MYELIN; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 3; SECRETED FRIZZLED RELATED PROTEIN 7; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ADULT; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; OLIGODENDROGLIOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WNT SIGNALING PATHWAY;

APOPTOSIS; BETA CATENIN; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETAL PROTEINS; FRIZZLED RECEPTORS; HEDGEHOG PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MYELIN PROTEINS; OLIGODENDROGLIA; OLIGODENDROGLIOMA; PHOSPHORYLATION; RECOMBINANT PROTEINS; RNA, MESSENGER; SOXF TRANSCRIPTION FACTORS; STEM CELLS; VERATRUM ALKALOIDS; WNT PROTEINS; WNT SIGNALING PATHWAY;

ERINACEIDAE;

EID: 84878248430     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.02.058     Document Type: Article

References (54)

1. A. Alentorn, M. Sanson, A. Adbaih, Oligodendrogliomas: new insights from the genetics and perspectives, Curr. Opin. Oncol., 2012.
2. Ayyanan A., Civenni G., Ciarloni L., Morel C., Mueller N., Lefort K., Mandinova A., Raffoul W., Fiche M., Dotto G.P., Brisken C. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc. Natl. Acad. Sci. (USA) 2006, 103:3799-3804.
3. Bar E.E., Chaudhry A., Lin A., Fan X., Schreck K., Matsui W., Piccirillo S., Vescovi A.L., DiMeco F., Olivi A., Eberhart C.G. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007, 25:2524-2533.
4. Bettegowda C., Agrawal N., Jiao Y., Sausen M., Wood L.D., Hruban R.H., Rodriguez F.J., Cahill D.P., McLendon R., Riggins G., Velculescu V.E., Oba-Shinjo S.M., Marie S.K.M., Vogelstei B., Bigner D., Yan H., Papadopoulos N., Kinzler K.W. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 2011, 333:1453-1455.
5. Bultje R.S., Castaneda-Castellanos D.R., Jan L.Y., Jan Y.N., Kriegstein A.R., Shi S.H. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing cortex. Neuron 2009, 63:189-202.
6. Buntinx M., Vanderlocht J., Hellings N., Vandenabeele F., Lambrichts I., Raus J., Ameloot M., Stinissen P., Steels P. Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocyte-specific gene expression. J. Neurocytol. 2003, 32:25-38.
7. Caraglia M., De Rosa G., Salzano G., Santini D., Lamberti, Sperlongano P., Lombardi A., Abbruzzese A., Addeo R. Nanotech revolution for the anti-cancer drug delivery through blood-brain barrier. Curr. Cancer Drug Targets 2012, 12:186-196.
8. Chew L.J., Shen W., Ming X., Senatorov V.V.J., Chen H.-L., Cheng Y., Hong E., Knoblach S., Gallo V. SRY-box containing gene 17 regulates the Wnt/beta-catenin signaling pathway in oligodendrocyte progenitor cells. J. Neurosci. 2011, 31:13921-13935.
9. Chimonidou M., Strati A., Tzitzira A., Sotiropoulou G., Malamos N., Georgoulias V., Lianidou E.S. DNA methylation of tumor suppressor and metastasis suppressor genes in circulating tumor cells. Clin. Chem. 2011, 57:1169-1177.
10. Clement V., Sanchez P., de Tribolet N., Radovanovic I., Ruizi Altaba A. Hedgehog-Gli1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 2007, 17:165-172.
11. Danesin C., Agius E., Escalas N., Ai X., Emerson C., Cochard P., Soula C. Ventral neural progenitors switch toward an oligodendroglial fate in response to increased sonic hedgehog (Shh) activity: involvement of sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J. Neurosci. 2006, 26:5037-5048.
12. Dissanayake K., Toth R., Blakey J., Olsson O., Campbell D.G., Prescott A.R., MacKintosh C. ERK/p90(RSK)/14-3-3 signalling has an impact on expressio of PEA3 Ets transcription factors via the transcirptional repressor capicua. Biochem. J. 2011, 433:515-525.
13. Du Y.C., Oshima H., Oguma K., Kitamura T., Itadani H., Fujimura T., Piao Y.S., Yoshimoto T., Minamoto T., Kotani H., Taketo M.M., Oshima M. Induction and down-regulation of Sox17 and its possible roles during the course of gastrointestinal tumorigenesis. Gastroenterology 2009, 137:1346-1357.
14. Ehtesham M., Sarangi A., Valadez J.G., Chanthaphaychith S., Becher M.W., Abel T.W., Thompson R.C., Cooper M.K. Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells. Oncogene 2007, 26:5752-5761.
15. Ellison D.W., Dalton J., Kocak M., Nicholson S.L., Fraga C., Neale G., Kenney A.M., Brat D.J., Perry A., Yong W.H., Taylor R.E., Bailey S., Clifford S.C., Gilbertson R.J. Medulloblastoma: clinicopathological correlates of SHH, WNT and non-SHH/WNT molecular subgroups. Acta Neuropathol. 2011, 121:381-396.
16. Fancy S.P.J., Baranzini S.E., Zhao C., Yuk D.-I., Irvine K.-A., Kaing S., Sanai N., Franklin R.J.M., Rowitch D.H. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 2009, 23:1571-1585.
17. Feigenson K., Reid M., See J., Crenshaw E.B.r., Grinspan J.B. Wnt signaling is sufficient to perturb oligodendrocyte maturation. Mol. Cell Neurosci. 2009, 42:255-265.
18. Flahaut M., Meier R., Coulon A., Nardou K.A., Niggli F.K., Martinel D., Beckmann J.S., Joseph J.M., Muhlethaler-Mottet A., Gross N. The Wnt receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the Wnt/beta-catenin pathway. Oncogene 2009, 28:2245-2256.
19. D.-Y. Fu, Z.-M. Wang, L. Chen, B.-L. Wang, Z.-Z. Shen, W. Huang, Z.-M. Shao, Sox17, the canonical Wnt antagonist, is epigenetically inactivated by promoter methylation in human breast cancer, Breast Cancer, 2010.
20. Givogri M.I., Bongarzone E.R., Schonmann V., Campagnoni A.T. Expression and regulation of golli products of myelin basic protein gene during in vitro development of oligodendrocytes. J. Neurosci. Res. 2001, 66:679-690.
21. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., Munsterberg A., Vivian N., Goodfellow P., Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 1990, 346:245-250.
22. He S., Kim I., Lim M.S., Morrison S.J. Sox17 expression confers self-renewal potential and fetal stem cell characteristics upon adult hematopoietic progenitors. Genes Dev. 2011, 25:1613-1627.
23. Hudson C., Clements D., Friday R.V., Stott D., Woddland H.R. XSox17alpha and -beta mediate endoderm formation in Xenopus. Cell 1997, 91:397-405.
24. Jia Y., Yang Y., Liu S., Herman J.G., Lu F., Guo M. Sox17 antagonizes WNT/beta-catenin signaling pathway in hepatocellular carcinoma. Epigenetics 2010, 5:743-749.
25. Kanai-Azuma M., Kanai Y., Gad J.M., Tajima Y., Taya C., Kurohmaru M., Sanai Y., Yonekawa H., Yazaki K., Tam P.P.L., Hayashi Y. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 2002, 129:2367-2379.
26. Katoh Y., Katoh M. WNT antagonist, SFRP1, is Hedgehog signaling target. Int. J. Mol. Med. 2006, 17:171-175.
27. Kelly J.J., Blough M.D., Stechishin O.D., Chan J.A., Beauchamp D., Perizzolo M., Demetrick D.J., Steele L., Auer R.N., Hader W.J., Westgate M., Parney I.F., Jenkins R., Cairncross J.G., Weiss S. Oligodendroglioma cell lines containing t(1;19)(q10;p10). Neuro. Oncol. 2010, 12:745-755.
28. Kim I., Saunders T.L., Morrison S.J. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 2007, 130:470-483.
29. Matsui T., Kanai-Azuma M., Hara K., Matoba S., Hiramatsu R., Kawakami H., Kurohmaru M., Koopman P., Kanai Y. Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice. J. Cell Sci. 2006, 119:3513-3526.
30. Milovanovic T., Planutis K., Nguyen A., Marsh J.L., Lin F., Hope C., Holcombe R.F. Expression of Wnt genes and frizzled 1 and 2 receptors in normal breast epithelium and infiltrating breast carcinoma. Int. J. Oncol. 2004, 25:1337-1342.
31. Niakan K.K., Ji K., Maehr R., Vokes S.A., Rodolfa K.T., Sherwood R.I., Yamaki M., Dimos J.T., Chen A.E., Melton D.A., McMahon A.P., Eggan K. Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes Dev. 2010, 24:312-326.
32. Pannone G., Bufo P., Santoro A., Franco R., Aquino G., Longo F., Botti G., Serpico R., Cafarelli B., Abbruzzese A., Caraglia M., Papagerakis S., Lo Muzio L. WNT pathway in oral cancer: epigenetic inactivation of WNT-inhibitors. Oncol. Rep. 2010, 24:1035-1041.
33. Persson A.I., Petritsch C., Swartling F.J., Itsara M., Sim F.J., Auvergne R., Goldenberg D.D., Vandenberg S.R., Nguyen K.N., Yakovenko S., Ayers-Ringler J., Nishiiyama A., Stallcup W.B., Berger M.S., Bergers G., McKnight T.R., Goldman S.A., Weiss W.A. Non-stem cell origin for oligodendroglioma. Cancer Cell 2010, 18:669-682.
34. Post G.R., Dawson G. Characterization of a cell line derived from a human oligodendroglioma. Mol. Chem. Neuropathol. 1992, 16:303-317.
35. Post G.R., Dawson G. Regulation of carbachol- and histamine-induced inositol phospholipid hydrolysis in a human oligodendroglioma. Glia 1992, 5:122-130.
36. Reis-Filho J.S., Faoro L.N., Carrilho C., Bleggi-Torres L.F., Schmitt F.C. Evaluation of cell proliferation, epidermal growth factor receptor, and bcl-2 immunoexpression as prognostic factors for patients with World Health Organization grade 2 oligodendroglioma. Cancer 2000, 88:862-869.
37. Schepers G.E., Teasdale R.D., Koopman P. Twenty pairs of Sox: extent, homology, and nomenclature of the mouse and human Sox transcription factor gene families. Dev. Cell 2002, 3:167-170.
38. Schwalbe E.C., Lindsey J.C., Straughton D., Hogg T.L., Cole M., Megahed H., Ryan S.L., Lusher M.E., Taylor M.D., Gilbertson R.J., Ellison D.W., Bailey S., Clifford S.C. Rapid diagnosis of medulloblastoma molecular subgroups. Clin. Cancer Res. 2011, 17:1883-1894.
39. Sinner D., Kordich J.J., Spence J.R., Opoka R., Rankin S., Lin S.-C.J., Jonatan D., Zorn A.M., Wells J.M. Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol. Cell. Biol. 2007, 27:7802-7815.
40. Sinner D., Rankin S., Lee M., Zorn A.M. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 2004, 131:3069-3080.
41. Sohn J., Natale J.E., Chew L.J., Belachew S., Cheng Y., Aguirre A.A., Lytle J., Nait-Oumesmar B., Kerninon C., Kanai-Azuma M., Kanai Y., Gallo V. Identification of Sox17 as a transcription factor that regulates oligodendrocyte development. J. Neurosci. 2006, 26:9722-9735.
42. Sugiarto S., Persson A.I., Munoz E.G., Waldhuber M., Lamagna C., Andor N., Hanecker P., Ayers-Ringler J., Phillips J., Siu J., Lim D.A., Vandenberg S., Stallcup W., Berger M.S., Bergers G., Weiss W.A., Petritsch C. Asymmetry-defective oligodendrocyte progentiros are glioma precursors. Cancer Cell 2011, 20:328-340.
43. Takezaki T., Hide T., Takanaga H., Nakamura H., Kuratsu J., Kondo T. Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci. 2011, 102:1306-1312.
44. Taylor M.D., Northcott P.A., Korshunov A., Remke M., Cho Y.J., Clifford S.C., Eberhart C.G., Parsons D.W., Rutkowski S., Gajjar A., Ellison D.W., Lichter P., Gilbertson R.J., Pomeroy S.L., Kool M., Pfister S.M. Molecular subgroups of medulloglastoma: the current consensus. Acta Neuropathol. 2012, 123:465-472.
45. Ueno K., Hazama S., Mitomori S., Nishioka M., Suehiro Y., Hirata H., Oka M., Imai K., Dahiya R., Hinoda Y. Down-regulation of frizzled-7 decreases survival, invasion and metastatic capabilities of colon cancer cells. Br. J. Cancer 2009, 101:1374-1381.
46. Ueno K., Hiura M., Suehiro Y., Hazama S., Hirata H., Oka M., Imai K., Dahiya R., Hinoda Y. Frizzled-7 as a potential therapeutic target in colorectal cancer. Neoplasia 2008, 10:697-705.
47. van der Meide W.F., Snellenberg S., Meijer C.J., Baalgergen A., Helmerhorst T.J., van der Sluis W.B., Snijders P.J., Steenbergen R.D. Promoter methylation analysis of WNT/beta-catenin signaling pathway regulators to detect adenocarcinoma or its precursor lesion of the cervix. Gynecol. Oncol. 2011, 123:116-122.
48. Wegner M. Transcriptional control in myelinating glia: flavors and spices. Glia 2000, 31:1-14.
49. Wegner M. Expression of transcription factors during oligodendroglial development. Microsc. Res. Tech. 2001, 52:746-752.
50. Xu Q., Yuan X., Liu G., Black K.L., Yu J.S. Hedgehog signaling regulates brain tumor-initiating cell proliferation and portends shorter survival for patients with PTEN-coexpressing glioblastomas. Stem Cells 2008, 26:3018-3026.
51. Yasunaga M., Tada S., Torikai-Nishikawa S., Nakano Y., Okada M., Jakt L.M., Nishikawa S., Chiba T., Era T. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat. Biotechnol. 2005, 23:1542-1550.
52. Yates A.J. An overview of principles for classifying brain tumors. Mol. Chem. Neuropathol. 1992, 17:103-120.
53. Ye Y.W., Wu J.H., Wang C.M., Zhou Y., Du C.Y., Zheng B.Q., Cao X., Zhou X.Y., Sun M.H., Shi Y.Q. Sox17 regulates proliferation and cell cycle during gastric cancer progression. Cancer Lett. 2011, 307:124-131.
54. Zheng Y., Miskimins W.K. Far upstream element binding protein 1 activates translation of p27Kip1 mRNA through its internal ribosomal entry site. Int. J. Biochem. Cell Biol. 2011, 43:1641-1648.