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Prognostic Role of Chicken Ovalbumin Upstream Promoter Transcription Factor II in Isocitrate Dehydrogenase-Mutant Glioma with 1p19q Co-Deletion

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Abstract

Background

Chicken ovalbumin upstream promoter transcription factor II is known to play a crucial role in the tumor microenvironment. However, the role of NR2F2 in gliomas is unknown.

Methods

The genomic and clinical data of 530 cases of lower grade gliomas (LGGs) patients and 167 cases of glioblastoma (GBM) patients in The Cancer Genome Atlas (TCGA) were extracted for analysis. R2 and UCSC Xena browser were used for Kaplan–Meier survival in the GSE16011 dataset and TCGA dataset, respectively. GraphPad Prism 7 was used to compare the differences in NR2F2 expression between various groups and subtypes.

Results

LGG patients with low NR2F2 expression had a significantly favorable outcome compared with those with high NR2F2 expression (p < 0.05). By matching histological subtypes and gene expression profiles of LGG patients, grade II glioma group showed lowest levels of NR2F2 expression compared with grade III gliomas and GBM. Patients diagnosed with astrocytoma have highest expression of NR2F2 but lowest OS (p < 0.05). In LGGs, NR2F2 expression was significantly downregulated in patient group with IDH mutation and 1p19q co-deletion (p < 0.05).

Conclusion

Our study suggests that NR2F2 can be used as a prognostic marker in LGG patients with IDH mutation and 1p19 co-deletion.

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References

  • Bao Y, Gu D, Feng W, Sun X, Wang X, Zhang X, Shi Q, Cui G, Yu H, Tang C, Deng A (2014) COUP-TFII regulates metastasis of colorectal adenocarcinoma cells by modulating Snail1. Br J Cancer 111(5):933–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cancer Genome Atlas Research N, Brat DJ, Verhaak RG et al (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372(26):2481–2498

    Article  CAS  Google Scholar 

  • Ceccarelli M, Barthel FP, Malta TM, Sabedot TS, Salama SR, Murray BA, Morozova O, Newton Y, Radenbaugh A, Pagnotta SM, Anjum S, Wang J, Manyam G, Zoppoli P, Ling S, Rao AA, Grifford M, Cherniack AD, Zhang H, Poisson L, Carlotti CG Jr, Tirapelli DPC, Rao A, Mikkelsen T, Lau CC, Yung WKA, Rabadan R, Huse J, Brat DJ, Lehman NL, Barnholtz-Sloan JS, Zheng S, Hess K, Rao G, Meyerson M, Beroukhim R, Cooper L, Akbani R, Wrensch M, Haussler D, Aldape KD, Laird PW, Gutmann DH, Noushmehr H, Iavarone A, Verhaak RGW, Anjum S, Arachchi H, Auman JT, Balasundaram M, Balu S, Barnett G, Baylin S, Bell S, Benz C, Bir N, Black KL, Bodenheimer T, Boice L, Bootwalla MS, Bowen J, Bristow CA, Butterfield YSN, Chen QR, Chin L, Cho J, Chuah E, Chudamani S, Coetzee SG, Cohen ML, Colman H, Couce M, D’Angelo F, Davidsen T, Davis A, Demchok JA, Devine K, Ding L, Duell R, Elder JB, Eschbacher JM, Fehrenbach A, Ferguson M, Frazer S, Fuller G, Fulop J, Gabriel SB, Garofano L, Gastier-Foster JM, Gehlenborg N, Gerken M, Getz G, Giannini C, Gibson WJ, Hadjipanayis A, Hayes DN, Heiman DI, Hermes B, Hilty J, Hoadley KA, Hoyle AP, Huang M, Jefferys SR, Jones CD, Jones SJM, Ju Z, Kastl A, Kendler A, Kim J, Kucherlapati R, Lai PH, Lawrence MS, Lee S, Leraas KM, Lichtenberg TM, Lin P, Liu Y, Liu J, Ljubimova JY, Lu Y, Ma Y, Maglinte DT, Mahadeshwar HS, Marra MA, McGraw M, McPherson C, Meng S, Mieczkowski PA, Miller CR, Mills GB, Moore RA, Mose LE, Mungall AJ, Naresh R, Naska T, Neder L, Noble MS, Noss A, O’Neill BP, Ostrom QT, Palmer C, Pantazi A, Parfenov M, Park PJ, Parker JS, Perou CM, Pierson CR, Pihl T, Protopopov A, Radenbaugh A, Ramirez NC, Rathmell WK, Ren X, Roach J, Robertson AG, Saksena G, Schein JE, Schumacher SE, Seidman J, Senecal K, Seth S, Shen H, Shi Y, Shih J, Shimmel K, Sicotte H, Sifri S, Silva T, Simons JV, Singh R, Skelly T, Sloan AE, Sofia HJ, Soloway MG, Song X, Sougnez C, Souza C, Staugaitis SM, Sun H, Sun C, Tan D, Tang J, Tang Y, Thorne L, Trevisan FA, Triche T, van den Berg DJ, Veluvolu U, Voet D, Wan Y, Wang Z, Warnick R, Weinstein JN, Weisenberger DJ, Wilkerson MD, Williams F, Wise L, Wolinsky Y, Wu J, Xu AW, Yang L, Yang L, Zack TI, Zenklusen JC, Zhang J, Zhang W, Zhang J, Zmuda E (2016) Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse glioma. Cell. 164(3):550–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Qin J, Cheng CM, Tsai MJ, Tsai SY (2012) COUP-TFII is a major regulator of cell cycle and Notch signaling pathways. Mol Endocrinol 26(8):1268–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng W, Ren X, Zhang C, Han S, Wu A (2017) Expression and prognostic value of microRNAs in lower-grade glioma depends on IDH1/2 status. J Neuro-Oncol 132(2):207–218

    Article  CAS  Google Scholar 

  • Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, Fantin VR, Jang HG, Jin S, Keenan MC, Marks KM, Prins RM, Ward PS, Yen KE, Liau LM, Rabinowitz JD, Cantley LC, Thompson CB, Vander Heiden MG, Su SM (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462(7274):739–U752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelmann D, Mayoli-Nussle D, Mayrhofer C et al (2013) E2F1 promotes angiogenesis through the VEGF-C/VEGFR-3 axis in a feedback loop for cooperative induction of PDGF-B. J Mol Cell Biol 5(6):391–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, Li Y, Bhagwat N, Vasanthakumar A, Fernandez HF, Tallman MS, Sun Z, Wolniak K, Peeters JK, Liu W, Choe SE, Fantin VR, Paietta E, Löwenberg B, Licht JD, Godley LA, Delwel R, Valk PJM, Thompson CB, Levine RL, Melnick A (2010) Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18(6):553–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldman M, Craft B, Kamath A, Brooks AN, Zhu J, Haussler D (2018) The UCSC Xena Platform for cancer genomics data visualization and interpretation. 2018:326470

  • Gravendeel LA, Kouwenhoven MC, Gevaert O et al (2009) Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res 69(23):9065–9072

    Article  CAS  PubMed  Google Scholar 

  • Hawkins SM, Loomans HA, Wan YW, Ghosh-Choudhury T, Coffey D, Xiao W, Liu Z, Sangi-Haghpeykar H, Anderson ML (2013) Expression and functional pathway analysis of nuclear receptor NR2F2 in ovarian cancer. J Clin Endocrinol Metab 98(7):E1152–E1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang LE, Cohen AL, Colman H, Jensen RL, Fults DW (2017) Couldwell WT. IGFBP2 expression predicts IDH-mutant glioma patient survival. Oncotarget 8(1):191–202

    PubMed  Google Scholar 

  • Jeong BC, Kang IH, Hwang YC, Kim SH, Koh JT (2014) MicroRNA-194 reciprocally stimulates osteogenesis and inhibits adipogenesis via regulating COUP-TFII expression. Cell Death Dis 5:e1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karsy M, Guan J, Huang LE (2018) Prognostic role of mitochondrial pyruvate carrier in isocitrate dehydrogenase-mutant glioma. J Neurosurg 1:1–11

    Article  Google Scholar 

  • Litchfield LM, Klinge CM (2012) Multiple roles of COUP-TFII in cancer initiation and progression. J Mol Endocrinol 49(3):R135–R148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820

    Article  Google Scholar 

  • Qin J, Chen X, Xie X, Tsai MJ, Tsai SY (2010) COUP-TFII regulates tumor growth and metastasis by modulating tumor angiogenesis. Proc Natl Acad Sci U S A 107(8):3687–3692

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin J, Wu SP, Creighton CJ et al (2013) COUP-TFII inhibits TGF-beta-induced growth barrier to promote prostate tumorigenesis. Nature 493(7431):236–240

    Article  CAS  PubMed  Google Scholar 

  • Qin J, Tsai SY, Tsai MJ (2014) The critical roles of COUP-TFII in tumor progression and metastasis. Cell Biosci 4(1):58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M (2006) Epidemiology and molecular pathology of glioma. Nat Clin Pract Neurol 2:494–503

    Article  PubMed  Google Scholar 

  • Shaw EJ, Haylock B, Husband D, du Plessis D, Sibson DR, Warnke PC, Walker C (2010) Gene expression in oligodendroglial tumors. Anal Cell Pathol (Amst) 33(2):81–94

    Article  CAS  Google Scholar 

  • Shin SW, Kwon HC, Rho MS, Choi HJ, Kwak JY, Park JI (2009) Clinical significance of chicken ovalbumin upstream promoter-transcription factor II expression in human colorectal cancer. Oncol Rep 21(1):101–106

    PubMed  Google Scholar 

  • Shinawi T, Hill VK, Krex D, Schackert G, Gentle D, Morris MR, Wei W, Cruickshank G, Maher ER, Latif F (2013) DNA methylation profiles of long- and short-term glioblastoma survivors. Epigenetics 8(2):149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18(3):636–645

    Article  CAS  PubMed  Google Scholar 

  • Swift MR, Pham VN, Castranova D, Bell K, Poole RJ, Weinstein BM (2014) SoxF factors and Notch regulate nr2f2 gene expression during venous differentiation in zebrafish. Dev Biol 390(2):116–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiburcio PDB, Xiao B, Chai Y, Asper S, Tripp SR, Gillespie DL, Jensen RL, Huang LE (2018) IDH1R132H is intrinsically tumor-suppressive but functionally attenuated by the glutamate-rich cerebral environment. Oncotarget 9:9

    Article  Google Scholar 

  • Walker C, Haylock B, Husband D, Joyce KA, Fildes D, Jenkinson MD, Smith T, Broome J, du Plessis DG, Warnke PC (2006) Clinical use of genotype to predict chemosensitivity in oligodendroglial tumors. Neurology 66(11):1661–1667

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Xu M, Qin J et al (2016) MPC1, a key gene in cancer metabolism, is regulated by COUPTFII in human prostate cancer. Oncotarget 7(12):14673–14683

    PubMed  PubMed Central  Google Scholar 

  • Xiao B, Fan Y, Ye M et al (2018) Downregulation of COUP-TFII inhibits glioblastoma growth via targeting MPC1. Oncol Lett 15(6):9697–9702

    PubMed  PubMed Central  Google Scholar 

  • Xu M, Qin J, Tsai SY, Tsai MJ (2015) The role of the orphan nuclear receptor COUP-TFII in tumorigenesis. Acta Pharmacol Sin 36(1):32–36

    Article  CAS  PubMed  Google Scholar 

  • Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360(8):765–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Liu J, Qiu J, Fu X, Tang Q, Yang F, Zhao Z, Wang H (2016) MicroRNA-382 inhibits prostate cancer cell proliferation and metastasis through targeting COUP-TFII. Oncol Rep 36(6):3707–3715

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Wang G, Guo S (2013) Regulation of angiogenesis via Notch signaling in breast cancer and cancer stem cells. Biochim Biophys Acta 1836(2):304–320

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dong Jie, PhD and Jiang Kaimo for their language editing assistance.

We acknowledge the TCGA Research Network (http://cancergenome.nih.gov/) for providing patient data.

Funding

This work was supported by the National Natural Science Foundation of China (No. 81470048 and No.81641076).

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Correspondence to Yuqi Zhang.

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Chai, Y., Liu, W., Wang, C. et al. Prognostic Role of Chicken Ovalbumin Upstream Promoter Transcription Factor II in Isocitrate Dehydrogenase-Mutant Glioma with 1p19q Co-Deletion. J Mol Neurosci 68, 234–242 (2019). https://doi.org/10.1007/s12031-019-01281-4

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