1,296
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

The function and mechanism of the JARID2/CCND1 axis in modulating glioma cell growth and sensitivity to temozolomide (TMZ)

, , , &
Pages 392-403 | Received 25 Dec 2020, Accepted 03 Jun 2021, Published online: 12 Jul 2021

References

  • Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. 2015. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro Oncol. 17(Suppl 4):iv1–iv62. doi:10.1093/neuonc/nov189.
  • Ostrom QT, Gittleman H, De Blank PM, Finlay JL, Gurney JG, McKean-Cowdin R, Stearns DS, Wolff JE, Liu M, Wolinsky Y, et al. 2016. American brain tumor association adolescent and young adult primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro Oncol. 18(Suppl 1):i1–i50. doi:10.1093/neuonc/nov297.
  • Zanders ED, Svensson F, Bailey DS. 2019. Therapy for glioblastoma: is it working? Drug Discov Today. 24(5):1193–1201. doi:10.1016/j.drudis.2019.03.008.
  • Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, et al. 2014. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 370(8):699–708. doi:10.1056/NEJMoa1308573.
  • Weller M, van den Bent M, Hopkins K, Tonn JC, Stupp R, Falini A, Cohen-Jonathan-Moyal E, Frappaz D, Henriksson R, Balana C, et al. 2014. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol. 15(9):e395–403. doi:10.1016/S1470-2045(14)70011-7.
  • Friedman HS, Kerby T, Calvert H. 2000. Temozolomide and treatment of malignant glioma. Clin Cancer Res. 6(7):2585–2597.
  • Karachi A, Dastmalchi F, Mitchell DA, Rahman M. 2018. Temozolomide for immunomodulation in the treatment of glioblastoma. Neuro Oncol. 20(12):1566–1572. doi:10.1093/neuonc/noy072.
  • Hombach-Klonisch S, Mehrpour M, Shojaei S, Harlos C, Pitz M, Hamai A, Siemianowicz K, Likus W, Wiechec E, Toyota BD, et al. 2018. Glioblastoma and chemoresistance to alkylating agents: involvement of apoptosis, autophagy, and unfolded protein response. Pharmacol Ther. 184:13–41. doi:10.1061/j.pharmthera.2017.10.017.
  • Lu Y, Kwintkiewicz J, Liu Y, Tech K, Frady LN, Su Y-T, Bautista W, Moon SI, MacDonald J, Ewend MG, et al. 2017. Chemosensitivity of IDH1-Mutated Gliomas due to an impairment in PARP1-Mediated DNA repair. Cancer Res. 77(7):1709–1718. doi:10.1158/0008-5472.CAN-16-2773.
  • SongTao Q, Lei Y, Si G, YanQing D, HuiXia H, XueLin Z, LanXiao W, Fei Y. 2012. IDH mutations predict longer survival and response to temozolomide in secondary glioblastoma. Cancer Sci. 103(2):269–273. doi:10.1111/j.1349-7006.2011.02134.x.
  • Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, Paris S, Boisselier B, Idbaih A, Laigle-Donadey F, et al. 2010. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology. 75(17):1560–1566. doi:10.1212/WNL.0b013e3181f96282.
  • Lin L, Cai J, Tan Z, Meng X, Li R, Li Y, Jiang C. 2021. Mutant IDH1 Enhances Temozolomide Sensitivity via Regulation of the ATM/CHK2 Pathway in Glioma. Cancer Res Treat. 53(2):367–377. doi:10.4143/crt.2020.506
  • Tran AN, Lai A, Li S, Pope WB, Teixeira S, Harris RJ, Woodworth DC, Nghiemphu PL, Cloughesy TF, Ellingson BM. 2014. Increased sensitivity to radiochemotherapy in IDH1 mutant glioblastoma as demonstrated by serial quantitative MR volumetry. Neuro Oncol. 16(3):414–420. doi:10.1093/neuonc/not198
  • Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, Fantin VR, Jang HG, Jin S, Keenan MC, et al. 2010. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 465(7300):966. doi:10.1038/nature09132.
  • Chowdhury R, Yeoh KK, Tian Y-M, Hillringhaus L, Bagg EA, Rose NR, Leung IKH, Li XS, Woon ECY, Yang M, et al. 2011. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep. 12(5):463–469. doi:10.1038/embor.2011.43.
  • Lu C, Thompson CB. 2012. Metabolic regulation of epigenetics. Cell Metab. 16(1):9–17. doi:10.1016/j.cmet.2012.06.001.
  • Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim S-H, Ito S, Yang C, Wang P, Xiao M-T, et al. 2011. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell. 19(1):17–30. doi:10.1016/j.ccr.2010.12.014.
  • Wang P, Wu J, Ma S, Zhang L, Yao J, Hoadley K, Wilkerson M, Perou C, Guan K-L, Ye D, et al. 2015. Oncometabolite D-2-Hydroxyglutarate inhibits ALKBH DNA repair enzymes and sensitizes IDH mutant cells to alkylating agents. Cell Rep. 13(11):2353–2361. doi:10.1016/j.celrep.2015.11.029.
  • Yamashita AS, Da Costa Rosa M, Borodovsky A, Festuccia WT, Chan T, Riggins GJ. 2019. Demethylation and epigenetic modification with 5-azacytidine reduces IDH1 mutant glioma growth in combination with temozolomide. Neuro Oncol. 21(2):189–200. doi:10.1093/neuonc/noy146.
  • Celik H, Koh WK, Kramer AC, Ostrander EL, Mallaney C, Fisher DAC, Xiang J, Wilson WC, Martens A, Kothari A, et al. 2018. JARID2 functions as a tumor suppressor in myeloid neoplasms by repressing self-renewal in hematopoietic progenitor cells. Cancer Cell. 34(5):741–756 e8. doi:10.1016/j.ccell.2018.10.008.
  • Li G, Margueron R, Ku M, Chambon P, Bernstein BE, Reinberg D. 2010. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24(4):368–380. doi:10.1101/gad.1886410.
  • Herz HM, Shilatifard A. 2010. The JARID2-PRC2 duality. Genes Dev. 24(9):857–861. doi:10.1101/gad.1921610.
  • Cifuentes-Rojas C, Hernandez A, Sarma K, Lee J. 2014. Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell. 55(2):171–185. doi:10.1016/j.molcel.2014.05.009.
  • Wang J, Wang Q, Cui Y, Liu ZY, Zhao W, Wang CL, Dong Y, Hou L, Hu G, Luo C, et al. 2012. Knockdown of cyclin D1 inhibits proliferation, induces apoptosis, and attenuates the invasive capacity of human glioblastoma cells. J Neurooncol. 106(3):473–484. doi:10.1007/s11060-011-0692-4.
  • Arcella A, Oliva MA, Staffieri S, Aalberti S, Grillea G, Madonna M, Bartolo M, Pavone L, Giangaspero F, Cantore G, et al. 2015. In vitro and in vivo effect of human lactoferrin on glioblastoma growth. J Neurosurg. 123(4):1026–1035. doi:10.3171/2014.12.JNS14512.
  • Shirato H, Ogawa S, Nakajima K, Inagawa M, Kojima M, Tachibana M, Shinkai Y, Takeuchi T. 2009. A jumonji (Jarid2) protein complex represses cyclin D1 expression by methylation of histone H3-K9. J Biol Chem. 284(2):733–739. doi:10.1074/jbc.M804994200.
  • Su C-L, Deng T-R, Shang Z, Xiao Y. 2015. JARID2 inhibits leukemia cell proliferation by regulating CCND1 expression. Int J Hematol. 102(1):76–85. doi:10.1007/s12185-015-1797-x.
  • Nakajima K, Inagawa M, Uchida C, Okada K, Tane S, Kojima M, Kubota M, Noda M, Ogawa S, Shirato H, et al. 2011. Coordinated regulation of differentiation and proliferation of embryonic cardiomyocytes by a jumonji (Jarid2)-cyclin D1 pathway. Development. 138(9):1771–1782. doi:10.1242/dev.059295.
  • Mayer RL, Schwarzmeier JD, Gerner MC, Bileck A, Mader JC, Meier-Menches SM, Gerner SM, Schmetterer KG, Pukrop T, Reichle A, et al. 2018. Proteomics and metabolomics identify molecular mechanisms of aging potentially predisposing for chronic lymphocytic leukemia. Mol Cell Proteomics. 17(2):290–303. doi:10.1074/mcp.RA117.000425.
  • Slezak-Prochazka I, Kluiver J, de Jong D, Smigielska-Czepiel K, Kortman G, Winkle M, Rutgers B, Koerts J, Visser L, Diepstra A, et al. 2016. Inhibition of the miR-155 target NIAM phenocopies the growth promoting effect of miR-155 in B-cell lymphoma. Oncotarget. 7(3):2391–2400. doi:10.18632/oncotarget.6165.
  • Puda A, Milosevic JD, Berg T, Klampfl T, Harutyunyan AS, Gisslinger B, Rumi E, Pietra D, Malcovati L, Elena C, et al. 2012. Frequent deletions of JARID2 in leukemic transformation of chronic myeloid malignancies. Am J Hematol. 87(3):245–250. doi:10.1002/ajh.22257.
  • Jiang T, Nam D-H, Ram Z, Poon W-S, Wang J, Boldbaatar D, Mao Y, Ma W, Mao Q, You Y, et al. 2021. Clinical practice guidelines for the management of adult diffuse gliomas. Cancer Lett. 499:60–72. doi:10.1016/j.canlet.2020.10.050.
  • Han B, Meng X, Wu P, Li Z, Li S, Zhang Y, Zha C, Ye Q, Jiang C, Cai J, et al. 2020. ATRX/EZH2 complex epigenetically regulates FADD/PARP1 axis, contributing to TMZ resistance in glioma. Theranostics. 10(7):3351–3365. doi:10.7150/thno.41219.
  • Wen Z-P, Zeng W-J, Chen Y-H, Li H, Wang J-Y, Cheng Q, Yu J, Zhou -H-H, Liu -Z-Z, Xiao J, et al. 2019. Knockdown ATG4C inhibits gliomas progression and promotes temozolomide chemosensitivity by suppressing autophagic flux. J Exp Clin Cancer Res. 38(1):298. doi:10.1186/s13046-019-1287-8.
  • Bao Z, Chen L, Guo S. 2019. Knockdown of SLC34A2 inhibits cell proliferation, metastasis, and elevates chemosensitivity in glioma. J Cell Biochem. 120(6):10205–10214. doi:10.1002/jcb.28305.
  • Li M, Liang RF, Wang X, Mao Q, Liu YH. 2017. BKM120 sensitizes C6 glioma cells to temozolomide via suppression of the PI3K/Akt/NF-kappaB/MGMT signaling pathway. Oncol Lett. 14(6):6597–6603. doi:10.3892/ol.2017.7034.
  • Cao Y, Li X, Kong S, Shang S, Qi Y. 2020. CDK4/6 inhibition suppresses tumour growth and enhances the effect of temozolomide in glioma cells. J Cell Mol Med. 24(9):5135–5145. doi:10.1111/jcmm.15156.
  • Sumorek-Wiadro J, Zając A, Bądziul D, Langner E, Skalicka-Woźniak K, Maciejczyk A, Wertel I, Rzeski W, Jakubowicz-Gil J. 2020. Coumarins modulate the anti-glioma properties of temozolomide. Eur J Pharmacol. 881:173207. doi:10.1016/j.ejphar.2020.173207.
  • Wu Y, Dong L, Bao S, Wang M, Yun Y, Zhu R. 2016. FK228 augmented temozolomide sensitivity in human glioma cells by blocking PI3K/AKT/mTOR signal pathways. Biomed Pharmacother. 84:462–469. doi:10.1016/j.biopha.2016.09.051.
  • Shao N, Mao J, Xue L, Wang R, Zhi F, Lan Q. 2019. Carnosic acid potentiates the anticancer effect of temozolomide by inducing apoptosis and autophagy in glioma. J Neurooncol. 141(2):277–288. doi:10.1007/s11060-018-03043-5.
  • Liu X, Kang J, Liu F, Wen S, Zeng X, Liu K, Luo Y, Ji X, Zhao S. 2016. Overexpression of iASPP-SV in glioma is associated with poor prognosis by promoting cell viability and antagonizing apoptosis. Tumour Biol. 37(5):6323–6330. doi:10.1007/s13277-015-4503-y.
  • Chen R, Liu H, Cheng Q, Jiang B, Peng R, Zou Q, Yang W, Yang X, Wu X, Chen Z, et al. 2016. MicroRNA-93 promotes the malignant phenotypes of human glioma cells and induces their chemoresistance to temozolomide. Biol Open. 5(6):669–677. doi:10.1242/bio.015552.
  • Ma L, Li J. 2020. MicroRNA-519d-3p inhibits cell proliferation and cell cycle G1/S transition in glioma by targeting CCND1. Biosci Biotechnol Biochem. 84(2):297–304. doi:10.1080/09168451.2019.1682510.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.