The NF-κB RelB Protein Is an Oncogenic Driver of Mesenchymal Glioma

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lee, Dong Whan ^a   Ramakrishnan, Dhivya ^a,c   Valenta, John ^a   Parney, Ian F ^b   Bayless, Kayla J ^a   Sitcheran, Raquel ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b MAYO CLINIC CANCER CENTER   (United States)

^c CARIS LIFE SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR RELB; ADIPOCYTOKINE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHI3L1 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LECTIN; NERVE PROTEIN; OLIG2 PROTEIN, HUMAN; RELB PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; MESENCHYMAL GLIOMA; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY MECHANISM; TUMOR GENE; TUMOR GROWTH; TUMOR XENOGRAFT; YKL 40 GENE; ANIMAL; BRAIN TUMOR; GENETICS; MESODERM; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION;

ADIPOKINES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GLIOMA; HUMANS; LECTINS; MESODERM; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; NF-KAPPA B; TRANSCRIPTION FACTOR RELB;

EID: 84874362151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057489     Document Type: Article

References (42)

1. Bosma I, Reijneveld JC, Douw L, Vos MJ, Postma TJ, et al. (2009) Health-related quality of life of long-term high-grade glioma survivors. Neuro-Oncology 11: 51-58 doi:10.1215/15228517-2008-049.
2. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, et al. (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173 doi:10.1016/j.ccr.2006.02.019.
3. Brennan C, Momota H, Hambardzumyan D, Ozawa T, Tandon A, et al. (2009) Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS ONE 4: e7752 doi:10.1371/journal.pone.0007752.
4. Parsons DW, Jones S, Zhang X, Lin JCH, Leary RJ, et al. (2008) An Integrated Genomic Analysis of Human Glioblastoma Multiforme. Science 321: 1807-1812 doi:10.1126/science.1164382.
5. Hayden MS, Ghosh S, (2012) NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234 doi:10.1101/gad.183434.111.
6. Perkins ND, (2012) The diverse and complex roles of NF-κB subunits in cancer. Nat Rev Cancer 12: 121-132 doi:10.1038/nrc3204.
7. Didonato JA, Mercurio F, Karin M, (2012) NF-κB and the link between inflammation and cancer. Immunol Rev 246: 379-400 doi:10.1111/j.1600-065X.2012.01099.x.
8. Sun S-C, (2012) The noncanonical NF-κB pathway. Immunol Rev 246: 125-140 doi:10.1111/j.1600-065X.2011.01088.x.
9. Xu Y, Josson S, Fang F, Oberley TD, St Clair DK, et al. (2009) RelB enhances prostate cancer growth: implications for the role of the nuclear factor-kappaB alternative pathway in tumorigenicity. Cancer Res 69: 3267-3271 doi:10.1158/0008-5472.CAN-08-4635.
10. Wang X, Belguise K, Kersual N, Kirsch KH, Mineva ND, et al. (2007) Oestrogen signalling inhibits invasive phenotype by repressing RelB and its target BCL2. Nat Cell Biol 9: 470-478 doi:10.1038/ncb1559.
11. Denis-Donini S, Caprini A, Frassoni C, Grilli M, (2005) Members of the NF-kappaB family expressed in zones of active neurogenesis in the postnatal and adult mouse brain. Brain Res Dev Brain Res 154: 81-89 doi:10.1016/j.devbrainres.2004.10.010.
12. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, et al. (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110 doi:10.1016/j.ccr.2009.12.020.
13. Yu S-C, Ping Y-F, Yi L, Zhou Z-H, Chen J-H, et al. (2008) Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer Lett 265: 124-134 doi:10.1016/j.canlet.2008.02.010.
14. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, et al. (2006) 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 9: 391-403 doi:10.1016/j.ccr.2006.03.030.
15. Tso C-L, Shintaku P, Chen J, Liu Q, Liu J, et al. (2006) Primary glioblastomas express mesenchymal stem-like properties. Mol Cancer Res 4: 607-619 doi:10.1158/1541-7786.MCR-06-0005.
16. Ku BM, Lee YK, Ryu J, Jeong JY, Choi J, et al. (2011) CHI3L1 (YKL-40) is expressed in human gliomas and regulates the invasion, growth and survival of glioma cells. Int J Cancer 128: 1316-1326 doi:10.1002/ijc.25466.
17. Liang C-C, Park AY, Guan J-L, (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nature Protocols 2: 329-333 doi:10.1038/nprot.2007.30.
18. Kaufman LJ, Brangwynne CP, Kasza KE, Filippidi E, Gordon VD, et al. (2005) Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophysical Journal 89: 635-650 doi:10.1529/biophysj.105.061994.
19. Bayless KJ, Kwak H-I, Su S-C, (2009) Investigating endothelial invasion and sprouting behavior in three-dimensional collagen matrices. Nature Protocols 4: 1888-1898 doi:10.1038/nprot.2009.221.
20. Francescone RA, Scully S, Faibish M, Taylor SL, Oh D, et al. (2011) Role of YKL-40 in the angiogenesis, radioresistance, and progression of glioblastoma. J Biol Chem 286: 15332-15343 doi:10.1074/jbc.M110.212514.
21. Nutt CL, Betensky RA, Brower MA, Batchelor TT, Louis DN, et al. (2005) YKL-40 is a differential diagnostic marker for histologic subtypes of high-grade gliomas. Clin Cancer Res 11: 2258-2264 doi:10.1158/1078-0432.CCR-04-1601.
22. Kalluri R, (2009) EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest 119: 1417-1419 doi:10.1172/JCI39675.
23. Ligon KL, Huillard E, Mehta S, Kesari S, Liu H, et al. (2007) Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 53: 503-517 doi:10.1016/j.neuron.2007.01.009.
24. Sun Y, Meijer DH, Alberta JA, Mehta S, Kane MF, et al. (2011) Phosphorylation state of Olig2 regulates proliferation of neural progenitors. Neuron 69: 906-917 doi:10.1016/j.neuron.2011.02.005.
25. Kelly JJP, Stechishin O, Chojnacki A, Lun X, Sun B, et al. (2009) Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 27: 1722-1733 doi:10.1002/stem.98.
26. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, et al. (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2: 401-404 doi:10.1158/2159-8290.CD-12-0095.
27. Cancer Genome Atlas Research Network, (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068 doi:10.1038/nature07385.
28. National Cancer Institute (2005) National Cancer Institute. REMBRANDT: 1-1. Available: http://rembrandt.nci.nih.gov. Accessed 29 March 2012.
29. Bren GD, Solan NJ, Miyoshi H, Pennington KN, Pobst LJ, et al. (2001) Transcription of the RelB gene is regulated by NF-kappaB. Oncogene 20: 7722-7733 doi:10.1038/sj.onc.1204868.
30. Raychaudhuri B, Han Y, Lu T, Vogelbaum MA, (2007) Aberrant constitutive activation of nuclear factor kappaB in glioblastoma multiforme drives invasive phenotype. J Neurooncol 85: 39-47 doi:10.1007/s11060-007-9390-7.
31. Smith D, Shimamura T, Barbera S, Bejcek BE, (2008) NF-kappaB controls growth of glioblastomas/astrocytomas. Mol Cell Biochem 307: 141-147 doi:10.1007/s11010-007-9593-4.
32. Powolny-Budnicka I, Riemann M, Tänzer S, Schmid RM, Hehlgans T, et al. (2011) RelA and RelB transcription factors in distinct thymocyte populations control lymphotoxin-dependent interleukin-17 production in γδ T cells. Immunity 34: 364-374 doi:10.1016/j.immuni.2011.02.019.
33. Shih VF-S, Davis-Turak J, Macal M, Huang JQ, Ponomarenko J,et al. (2012) Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-κB pathways. Nat Immunol. doi:10.1038/ni.2446.
34. Oeckinghaus A, Hayden MS, Ghosh S, (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12: 695-708 doi:10.1038/ni.2065.
35. Lee CG, Da Silva CA, Cruz Dela CS, Ahangari F, Ma B, et al. (2011) Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 73: 479-501 doi:10.1146/annurev-physiol-012110-142250.
36. Bhat KP, Pelloski CE, Zhang Y, Kim SH, deLaCruz C, et al. (2008) Selective repression of YKL-40 by NF-kappaB in glioma cell lines involves recruitment of histone deacetylase-1 and-2. FEBS LETTERS 582: 3193-3200 doi:10.1016/j.febslet.2008.08.010.
37. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674 doi:10.1016/j.cell.2011.02.013.
38. Lee J-S, Padmanabhan A, Shin J, Zhu S, Guo F, et al. (2010) Oligodendrocyte progenitor cell numbers and migration are regulated by the zebrafish orthologs of the NF1 tumor suppressor gene. Human Molecular Genetics 19: 4643-4653 doi:10.1093/hmg/ddq395.
39. Lee DY, Yeh T-H, Emnett RJ, White CR, Gutmann DH, (2010) Neurofibromatosis-1 regulates neuroglial progenitor proliferation and glial differentiation in a brain region-specific manner. Genes Dev 24: 2317-2329 doi:10.1101/gad.1957110.
40. Hegedus B, Dasgupta B, Shin JE, Emnett RJ, Hart-Mahon EK, et al. (2007) Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 1: 443-457 doi:10.1016/j.stem.2007.07.008.
41. Liu C, Sage JC, Miller MR, Verhaak RGW, Hippenmeyer S, et al. (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146: 209-221 doi:10.1016/j.cell.2011.06.014.
42. Monje M, Mitra SS, Freret ME, Raveh TB, Kim J, et al. (2011) Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. Proc Natl Acad Sci USA 108: 4453-4458 doi:10.1073/pnas.1101657108.