Eva1 maintains the stem-like character of glioblastoma-initiating cells by activating the noncanonical NF-κB signaling pathway

Cancer Research

Volumn 76, Issue 1, 2016, Pages 171-181

  Ohtsu, Naoki ^a   Nakatani, Yuka ^b,d   Yamashita, Daisuke ^c   Ohue, Shiro ^c   Ohnishi, Takanori ^c   Kondo, Toru ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; CD15 ANTIGEN; EPITHELIAL V LIKE ANTIGEN; GLYCOPROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR SOX2; TUMOR MARKER; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; MPZL2 PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL SELF-RENEWAL; CONTROLLED STUDY; DOWN REGULATION; EVA1 GENE; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BRAIN TUMOR; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; XENOGRAFT;

ANIMALS; BRAIN NEOPLASMS; CELL ADHESION MOLECULES; FEMALE; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84959017880     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0884     Document Type: Article

References (50)

1. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821-8.
2. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene 2004;23:7267-73.
3. Kondo T. Brain cancer stem-like cells. Eur J Cancer 2006;42:1237-42.
4. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006;6:425-36.
5. Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN. Cancer stem cells in glioblastoma. Genes Dev 2015;29:1203-17.
6. Alvarez-Buylla A, Lois C. Neuronal stem cells in the brain of adult vertebrates. Stem Cells 1995;13:263-72.
7. Frisén J, Johansson CB, Lothian C, Lendahl U. Central nervous system stem cells in the embryo and adult. Cell Mol Life Sci 1998;54:935-45.
8. Hide T, Takezaki T, Nakatani Y, Nakamura H, Kuratsu J, Kondo T. Sox11 prevents tumorigenesis of glioma-initiating cells by inducing neuronal differentiation. Cancer Res 2009;69:7953-9.
9. Hide T, Takezaki T, Nakatani Y, Nakamura H, Kuratsu J, Kondo T. Combination of a Ptgs2 inhibitor and an EGFR signaling inhibitor prevents tumorigenesis of oligodendrocyte lineage derived glioma-initiating cells. Stem Cells 2011;29:590-9.
10. Yamashita D, Kondo T, Ohue S, Takahashi H, Ishikawa M, Matoba R, et al. miR340 suppresses the stem-like cell function of glioma-initiating cells by targeting tissue plasminogen activator. Cancer Res 2015;75:1123-33.
11. Kaneko S, Nakatani Y, Takezaki T, Hide T, Yamashita D, Ohtsu N, et al. Ceacam1L modulates STAT3 signaling to control the proliferation of glioblastoma-initiating cells. Cancer Res 2015;75:4224-34.
12. Guttinger M, Sutti F, Panigada M, Porcellini S, Merati B, Mariani M, et al. Epithelial V-like antigen (EVA), a novel member of the immunoglobulin superfamily, expressed in embryonic epithelia with a potential role as homotypic adhesion molecule in thymus histogenesis. J Cell Biol 1998; 141:1061-71.
13. Iacovelli S, Iosue I, Di Cesare S, Guttinger M. Lymphoid EVA1 expression is required for DN1-DN3 thymocytes transition. PLoS ONE 2009;4:e7586.
14. DeMonte L, Porcellini S, Tafi E, Sheridan J, Gordon J, Depreter M, et al. EVA regulates thymic stromal organisation and early thymocyte development. Biochem Biophys Res Commun 2007;356:334-40.
15. Wright E, Rahgozar K, Hallworth N, Lanker S, Carrithers MD. Epithelial Vlike antigen mediates efficacy of anti-alpha4 integrin treatment in a mouse model of multiple sclerosis. PLoS ONE 2013;8:e70954.
16. Kondo T, Raff M. Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells. Genes Dev 2004;18:2963-72.
17. DiDonato JA, Mercurio F, Karin M. NF-kB and the link between inflammation and cancer. Immunol Rev 2012;246:379-400.
18. Thomas M, Klibanov AM. Enhancing polyethylenimine's delivery of plasmid DNA into mammalian cells. Proc Natl Acad Sci U S A 2002; 99:14640-5.
19. Takanaga H, Tsuchida-Straeten N, Nishide K, Watanabe A, Aburatani H, Kondo T. Gli2 is a novel regulator of sox2 expression in telencephalic neuroepithelial cells. Stem Cells 2009;27:165-74.
20. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2:401-4
21. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013;6:pl1.
22. Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009;27:40-8.
23. 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;4:440-52.
24. Lathia JD, Gallagher J, Heddleston JM, Wang J, Eyler CE, Macswords J, et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010;6: 421-32.
25. Temple S. Division and differentiation of isolated CNS blast cells in microculture. Nature 1989;340:471-3.
26. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990;60:585-95.
27. Doetshe F, Cailłe I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-16.
28. Shih VF, Tsui R, Caldwell A, Hoffmann A. A single NF-kB system for both canonical and non-canonical signaling. Cell Res 2011;21:86-102.
29. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad SciU S A 1996;93:9090-5.
30. Priego S, Feddi F, Ferrer P, Mena S, Benlloch M, Ortega A, et al. Natural polyphenols facilitate elimination of HT-29 colorectal cancer xenografts by chemoradiotherapy: a Bcl-2- and superoxide dismutase 2-dependent mechanism. Mol Cancer Ther 2008;7:3330-42.
31. Baud V, Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat Rev Drug Discov 2009;8:33-40.
32. Gyrd-Hansen M, Meier P. IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 2010;10:561-74.
33. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NFkappaB signaling. Nat Immunol 2008;9:1364-70.
34. Su X, Ye J, Hsueh EC, Zhang Y, Hoft DF, Peng G. Tumor microenvironments direct the recruitment and expansion of human Th17 cells. J Immunol 2010;184:1630-41.
35. Kryczek I, Wu K, Zhao E, Wei S, Vatan L, Szeliga W, et al. IL-17+regulatory T cells in the microenvironments of chronic inflammation and cancer. J Immunol 2011;186:4388-95.
36. Wilke CM, Kryczek I, Wei S, Zhao E, Wu K, Wang G, et al. Th17 cells in cancer: help or hindrance? Carcinogenesis 2011;32:643-9.
37. Qi W, Huang X, Wang J. Correlation between Th17 cells and tumor microenvironment. Cell Immunol 2013;285:18-22.
38. Xiang T, Long H, He L, Han X, Lin K, Liang Z, et al. Interleukin-17 produced by tumor microenvironment promotes self-renewal of CD133+ cancer stem-like cells in ovarian cancer. Oncogene 2013;34:165-76.
39. Song X, Gao H, Lin Y, Yao Y, Zhu S, Wang J, et al. Alterations in the microbiota drive interleukin-17C production from intestinal epithelial cells to promote tumorigenesis. Immunity 2014;40:140-52.
40. Powolny-Budnicka I, Riemann M, Tänzer S, Schmid RM, Hehlgans T, Weih F. RelA and RelB transcription factors in distinct thymocyte populations control lymphotoxin-dependent interleukin-17 production in gd T cells. Immunity 2011;34:364-74.
41. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factorbeta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007;26:579-91.
42. Morrison SJ. Neuronal potential and lineage determination by neural stem cells. Curr Opin Cell Biol 2001;13:666-72.
43. Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002;25:471-90.
44. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006;66:7445-52.
45. Voskas D, Ling LS, Woodgett JR. Signals controlling un-differentiated states in embryonic stem and cancer cells: role of the phosphatidylinositol 30 kinase pathway. J Cell Physiol 2014;229:1312-22.
46. Wojcik E, Carrithers LM, Carrithers MD. Characterization of epithelial Vlike antigen in human choroid plexus epithelial cells: potential role in CNS immune surveillance. Neurosci Lett 2011;495:115-20.
47. Macián F, García-Cózar F, Im SH, Horton HF, Byrne MC, Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2012;109: 719-31.
48. Sun SC. Non-canonical NF-kB signaling pathway. Cell Res 2011;21:71-85.
49. Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, et al. NF-kB control energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 2011;13:1272-9.
50. Bhat KP, Balasubramaniyan V, Vaillant B, Ezhilarasan R, Hummelink K, Hollingsworth F, et al. Mesenchymal differentiation mediated by NF-kB promotes radiation resistance in glioblastoma. Cancer Cell 2013;24: 331-46.