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ERN1 knockdown modifies the effect of glucose deprivation on homeobox gene expressions in U87 glioma cells Cover

ERN1 knockdown modifies the effect of glucose deprivation on homeobox gene expressions in U87 glioma cells

Open Access
|Aug 2020

References

  1. Alimohammadi E, Bagheri SR, Salehi AS, Rizevandi P, Rezaie Z, Abdi A. Prognostic factors in patients with glioblastoma multiforme: focus on the pathologic variants. Acta Neurol Belg 2019. Online ahead of print.10.1007/s13760-019-01171-x
  2. Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, Luis A, McCarthy N, Montibeller L, More S, Papaioannou A, Puschel F, Sassano ML, Skoko J, Agostinis P, de Belleroche J, Eriksson LA, Fulda S, Gorman AM, Healy S, Kozlov A, Munoz-Pinedo C, Rehm M, Chevet E, Samali A. Endoplasmic reticulum stress signalling - from basic mechanisms to clinical applications. FEBS J 286, 241–278, 2019.10.1111/febs.14608
  3. Auf G, Jabouille A, Guerit S, Pineau R, Delugin M, Bouchecareilh M, Favereaux A, Maitre M, Gaiser T, von Deimling A, Czabanka M, Vajkoczy P, Chevet E, Bikfalvi A, Moenner M. A shift from an angiogenic to invasive phenotype induced in malignant glioma by inhibition of the unfolded protein response sensor IRE1. Proc Natl Acad Sci U S A 107, 15553–15558, 2010.10.1073/pnas.0914072107
  4. Auf G, Jabouille A, Delugin M, Guerit S, Pineau R, North S, Platonova N, Maitre M, Favereaux A, Vajkoczy P, Seno M, Bikfalvi A, Minchenko D, Minchenko O, Moenner M. High epiregulin expression in human U87 glioma cells relies on IRE1alpha and promotes autocrine growth through EGF receptor. BMC Cancer 13, 597, 2013.10.1186/1471-2407-13-597
  5. Awale S, Lu J, Kalauni SK, Kurashima Y, Tezuka Y, Kadota S, Esumi H. Identification of arctigenin as an antitumor agent having the ability to eliminate the tolerance of cancer cells to nutrient starvation. Cancer Res 66, 1751–1757, 2006.10.1158/0008-5472.CAN-05-3143
  6. Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F, Wang ZV, Zorzano A, Hill JA, Jaimovich E, Quest AF, Lavandero S. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 301, 215–290, 2013.10.1016/B978-0-12-407704-1.00005-1
  7. Chen HQ, Zhao J, Li Y, Huang YJ, Chen DJ, He LX, Wang LQ, Zheng CF, Wang J, Cao J, Shu WQ, Liu JY, Liu WB. Epigenetic inactivation of LHX6 mediated microcystin-LR induced hepatocarcinogenesis via the Wnt/beta-catenin and P53 signaling pathways. Environ Pollut 252, 216–226, 2019.10.1016/j.envpol.2019.05.049
  8. Colombo SL, Palacios-Callender M, Frakich N, Carcamo S, Kovacs I, Tudzarova S, Moncada S. Molecular basis for the differential use of glucose and glutamine in cell proliferation as revealed by synchronized HeLa cells. Proc Natl Acad Sci USA 108, 21069–21074, 2011.10.1073/pnas.1117500108
  9. Fonseca-Alves CE, Kobayashi PE, Laufer-Amorim R. Evaluation of NKX3.1 and C-MYC expression in canine prostatic cancer. Res Vet Sci 118, 365–370, 2018.10.1016/j.rvsc.2018.04.001
  10. Gu Y, Qi C, Sun X, Ma X, Zhang H, Hu L, Yuan J, Yu Q. Arctigenin preferentially induces tumor cell death under glucose deprivation by inhibiting cellular energy metabolism. Biochem Pharmacol 84, 468–476, 2012.10.1016/j.bcp.2012.06.002
  11. Guca E, Sunol D, Ruiz L, Konkol A, Cordero J, Torner C, Aragon E, Martin-Malpartida P, Riera A, Macias MJ. TGIF1 homeodomain interacts with Smad MH1 domain and represses TGF-beta signaling. Nucleic Acids Res 46, 9220–9235, 2018.10.1093/nar/gky680
  12. Guo H, Nan Y, Zhen Y, Zhang Y, Guo L, Yu K, Huang Q, Zhong Y. miRNA-451 inhibits glioma cell proliferation and invasion by downregulating glucose transporter 1. Tumour Biol 37, 13751–13761, 2016.10.1007/s13277-016-5219-3
  13. Hamaidi I, Coquard C, Danilin S, Dormoy V, Beraud C, Rothhut S, Barthelmebs M, Benkirane-Jessel N, Lindner V, Lang H, Massfelder T. The Lim1 oncogene as a new therapeutic target for metastatic human renal cell carcinoma. Oncogene 38, 60–72, 2019.10.1038/s41388-018-0413-y
  14. Hassler JR, Scheuner DL, Wang S, Han J, Kodali VK, Li P, Nguyen J, George JS, Davis C, Wu SP, Bai Y, Sartor M, Cavalcoli J, Malhi H, Baudouin G, Zhang Y, Yates Iii JR, Itkin-Ansari P, Volkmann N, Kaufman RJ. The IRE1α/ XBP1s pathway is essential for the glucose response and protection of β cells. PLoS Biol 13, e1002277, 2015.10.1371/journal.pbio.1002277
  15. He Y, Fan Q, Cai T, Huang W, Xie X, Wen Y, Shi Z. Molecular mechanisms of the action of Arctigenin in cancer. Biomed Pharmacother 108, 403–407, 2018.10.1016/j.biopha.2018.08.158
  16. Hetz C, Axten JM, Patterson JB. Pharmacological targeting of the unfolded protein response for disease intervention. Nat Chem Biol 15, 764–775, 2019.10.1038/s41589-019-0326-2
  17. Huber AL, Lebeau J, Guillaumot P, Petrilli V, Malek M, Chilloux J, Fauvet F, Payen L, Kfoury A, Renno T, Chevet E, Manie SN. p58(IPK)-mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression under low glucose. Mol Cell 49, 1049–1059, 2013.10.1016/j.molcel.2013.01.009
  18. Iurlaro R, Puschel F, Leon-Annicchiarico CL, O’Connor H, Martin SJ, Palou-Gramon D, Lucendo E, Munoz-Pinedo C. Glucose deprivation induces ATF4-mediated apoptosis through TRAIL death receptors. Mol Cell Biol 37, e00479–16, 2017.10.1128/MCB.00479-16
  19. Ji Y, Jiang J, Huang L, Feng W, Zhang Z, Jin L, Xing X. Spermassociated antigen 4 (SPAG4) as a new cancer marker interacts with Nesprin3 to regulate cell migration in lung carcinoma. Oncol Rep 40, 783–792, 2018.10.3892/or.2018.6473
  20. Jiang J, Zheng M, Zhang M, Yang X, Li L, Wang SS, Wu JS, Yu XH, Wu JB, Pang X, Tang YJ, Tang YL, Liang XH. PRRX1 regulates cellular phenotype plasticity and dormancy of head and neck squamous cell carcinoma through miR-642b-3p. Neoplasia 21, 216–229, 2019.10.1016/j.neo.2018.12.001
  21. Kataoka K, Yoshitomo-Nakagawa K, Shioda S, Nishizawa M. A set of Hox proteins interact with the Maf oncoprotein to inhibit its DNA binding, transactivation, and transforming activities. J Biol Chem 276, 819–826, 2001.10.1074/jbc.M007643200
  22. Kim JY, Hwang JH, Cha MR, Yoon MY, Son ES, Tomida A, Ko B, Song SW, Shin-ya K, Hwang YI, Park HR. Arctigenin blocks the unfolded protein response and shows therapeutic antitumor activity. J Cell Physiol 224, 33–40, 2010.10.1002/jcp.22085
  23. Knaup KX, Monti J, Hackenbeck T, Jobst-Schwan T, Klanke B, Schietke RE, Wacker I, Behrens J, Amann K, Eckardt KU, Warnecke C, Wiesener MS. Hypoxia regulates the sperm associated antigen 4 (SPAG4) via HIF, which is expressed in renal clear cell carcinoma and promotes migration and invasion in vitro. Mol Carcinog 53, 970–978, 2014.10.1002/mc.22065
  24. Korkmaz KS, Korkmaz CG, Ragnhildstveit E, Kizildag S, Pretlow TG, Saatcioglu F. Full-length cDNA sequence and genomic organization of human NKX3A - alternative forms and regulation by both androgens and estrogens. Gene 260, 25–36, 2000.10.1016/S0378-1119(00)00453-4
  25. Le Magnen C, Virk RK, Dutta A, Kim JY, Panja S, Lopez-Bujanda ZA, Califano A, Drake CG, Mitrofanova A, Abate-Shen C. Cooperation of loss of NKX3.1 and inflammation in prostate cancer initiation. Dis Model Mech 11, dmm035139, 2018.10.1242/dmm.035139
  26. Li Q, Ma L, Wu Z, Wang G, Huang Q, Shen Z, Yu R. Zinc finger Ebox binding homeobox 2 functions as an oncogene in human laryngeal squamous cell carcinoma. Mol Med Rep 19, 4545–4552, 2019.10.3892/mmr.2019.10126
  27. Liang TS, Zheng YJ, Wang J, Zhao JY, Yang DK, Liu ZS. MicroRNA-506 inhibits tumor growth and metastasis in nasopharyngeal carcinoma through the inactivation of the Wnt/beta-catenin signaling pathway by down-regulating LHX2. J Exp Clin Cancer Res 38, 97, 2019.10.1186/s13046-019-1023-4
  28. Liu Z, Dai J, Shen H. Systematic analysis reveals long noncoding RNAs regulating neighboring transcription factors in human cancers. Biochim Biophys Acta Mol Basis Dis 1864, 2785–2792, 2018.10.1016/j.bbadis.2018.05.006
  29. Logue SE, McGrath EP, Cleary P, Greene S, Mnich K, Almanza A, Chevet E, Dwyer RM, Oommen A, Legembre P, Godey F, Madden EC, Leuzzi B, Obacz J, Zeng Q, Patterson JB, Jager R, Gorman AM, Samali A. Inhibition of IRE1 RNase activity modulates the tumor cell secretome and enhances response to chemotherapy. Nat Commun 9, 3267, 2018.10.1038/s41467-018-05763-8
  30. Mai T, Markov GJ, Brady JJ, Palla A, Zeng H, Sebastiano V, Blau HM. NKX3-1 is required for induced pluripotent stem cell reprogramming and can replace OCT4 in mouse and human iPSC induction. Nat Cell Biol 20, 900–908, 2018.10.1038/s41556-018-0136-x
  31. Manie SN, Lebeau J, Chevet E. Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 3. Orchestrating the unfolded protein response in oncogenesis: an update. Am J Physiol Cell Physiol 307, C901–C907, 2014.10.1152/ajpcell.00292.2014
  32. Marchand B, Pitarresi JR, Reichert M, Suzuki K, Laczko D, Rustgi AK. PRRX1 isoforms cooperate with FOXM1 to regulate the DNA damage response in pancreatic cancer cells. Oncogene 38, 4325–4339, 2019.10.1038/s41388-019-0725-6
  33. Minchenko AG, Leshchinsky I, Opentanova I, Sang N, Srinivas V, Armstead VE, Caro J. Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J Biol Chem 277, 6183–6187, 2002.10.1074/jbc.M110978200
  34. Minchenko DO, Kharkova AP, Hubenia OV, Minchenko OH. Insulin receptor, IRS1, IRS2, INSIG1, INSIG2, RRAD, and BAIAP2 gene expressions in glioma U87 cells with ERN1 loss of function: effect of hypoxia and gluta-mine or glucose deprivation. Endocr Reg 47, 15–26, 2013.10.4149/endo_2013_01_15
  35. Minchenko DO, Danilovskyi SV, Kryvdiuk IV, Bakalets TV, Lypova NM, Karbovskyi LL, Minchenko OH. Inhibition of ERN1 modifies the hypoxic regulation of the expression of TP53-related genes in U87 glioma cells. Endoplasm Reticul Stress Dis 1, 18–26, 2014.10.2478/ersc-2014-0001
  36. Minchenko DO, Kharkova AP, Tsymbal DO, Karbovskyi LL, Minchenko OH. IRE1 inhibition affects the expression of insulin-like growth factor binding protein genes and modifies its sensitivity to glucose deprivation in U87 glioma cells. Endocr Reg 49, 185–197, 2015a.10.4149/endo_2015_04_185
  37. Minchenko DO, Tsymbal DO, Riabovol OO, Viletska YM, Lahanovska YO, Sliusar MY, Bezrodnyi BH, Minchenko OH. Hypoxic regulation of EDN1, EDNRA, EDNRB, and ECE1 gene expressions in IRE1 knockdown U87 glioma cells. Endocr Reg 53, 250–262, 2019.10.2478/enr-2019-0025
  38. Minchenko OH, Tsymbal DO, Minchenko DO, Kovalevska OV, Karbovskyi LL, Bikfalvi A. Inhibition of ERN1 signaling enzyme affects hypoxic regulation of the expression of E2F8, EPAS1, HOXC6, ATF3, TBX3 and FOXF1 genes in U87 glioma cells. Ukr Biochem J 87(2): 76–87, 2015b.10.15407/ubj87.02.076
  39. Minchenko OH, Tsymbal DO, Moenner M, Kovalevska OV, Lypova NM. Inhibition of the endoribonuclease of ERN1 signaling enzyme affects the expression of proliferation-related genes in U87 glioma cells. Endoplasm Reticul Stress Dis 2, 18–29, 2015c.10.1515/ersc-2015-0002
  40. Miyashita K, Kitajima K, Goyama S, Kitamura T, Hara T. Overexpression of Lhx2 suppresses proliferation of human T cell acute lymphoblastic leukemia-derived cells, partly by reducing LMO2 protein levels. Biochem Biophys Res Commun 495, 2310–2316, 2018.10.1016/j.bbrc.2017.12.135
  41. Nathalia E, Theardy MS, Elvira S, Rosellinny G, Liyanto AS, Utama MP, Sumarpo A. Downregulation of tumor-suppressor gene LHX6 in cancer: a systematic review. Rom J Intern Med 56, 135–142, 2018.10.2478/rjim-2018-0008
  42. Papaioannou A, Chevet E. Driving cancer tumorigenesis and metastasis through UPR signaling. Curr Top Microbiol Immunol 414, 159–192, 2018.10.1007/82_2017_36
  43. Riabovol OO, Tsymbal DO, Minchenko DO, Lebid-Biletska KM, Sliusar MY, Rudnytska OV, Minchenko OH. Effect of glucose deprivation on the expression of genes encoding glucocorticoid receptor and some related factors in ERN1-knockdown U87 glioma cells. Endocr Regul 53, 237–249, 2019.10.2478/enr-2019-0024
  44. Teramoto K, Katoh H. The cystine/glutamate antiporter xCT is a key regulator of EphA2 S897 phosphorylation under glucose-limited conditions. Cell Signal 62, 109329, 2019.10.1016/j.cellsig.2019.05.014
  45. Tsymbal DO, Minchenko DO, Kryvdiuk IV, Riabovol OO, Halkin OV, Ratushna OO, Minchenko OH. Expression of proliferation related transcription factor genes in U87 glioma cells with IRE1 knockdown upon glucose and glutamine deprivation. Fiziol Zh 62, 3–15, 2016a.10.15407/fz62.01.003
  46. Tsymbal DO, Minchenko DO, Riabovol OO, Ratushna OO, Minchenko OH. IRE1 knockdown modifies glucose and glutamine deprivation effects on the expression of proliferation related genes in U87 glioma cells. Biotechnol Acta 9, 26–37, 2016b.10.15407/biotech9.01.026
  47. Wang Y, Li L, Wang H, Li J, Yang H. Silencing TGIF suppresses migration, invasion and metastasis of MDAMB231 human breast cancer cells. Oncol Rep 39, 802–808, 2018.10.3892/or.2017.6133
  48. Wang X, Yang R, Wang Q, Wang Y, Ci H, Wu S. Aberrant expression of vasculogenic mimicry, PRRX1, and CIP2A in clear cell renal cell carcinoma and its clinicopathological significance. Medicine (Baltimore) 98, e17028, 2019.10.1097/MD.0000000000017028
  49. Yalcin A, Clem BF, Imbert-Fernandez Y, Ozcan SC, Peker S, O’Neal J, Klarer AC, Clem AL, Telang S, Chesney J. 6-Phosphofructo-2-kinase (PFKFB3) promotes cell cycle progression and suppresses apoptosis via Cdk1-mediated phosphorylation of p27. Cell Death and Disease 5, e1337, 2014.10.1038/cddis.2014.292
  50. Yalim-Camci I, Balcik-Ercin P, Cetin M, Odabas G, Tokay N, Sayan AE, Yagci T. ETS1 is coexpressed with ZEB2 and mediates ZEB2-induced epithelial-mesenchymal transition in human tumors. Mol Carcinog 58, 1068–1081, 2019.10.1002/mc.22994
  51. Yan L, Cai K, Sun K, Gui J, Liang J. MiR-1290 promotes proliferation, migration, and invasion of glioma cells by targeting LHX6. J Cell Physiol 233, 6621–6629, 2018.10.1002/jcp.26381
  52. Yang H, Zhang H, Pan T, Wang H, Wang Y. Benzo(a)pyrene promotes migration, invasion and metastasis of lung adenocarcinoma cells by upregulating TGIF. Toxicol Lett 294, 11–19, 2018.10.1016/j.toxlet.2018.05.005
  53. Zhao S, Cai J, Li J, Bao G, Li D, Li Y, Zhai X, Jiang C, Fan L. Bioinformatic profiling identifies a glucose-related risk signature for the malignancy of glioma and the survival of patients. Mol Neurobiol 54, 8203–8210, 2017.10.1007/s12035-016-0314-4
  54. Zhu D, Gu L, Li Z, Jin W, Lu Q, Ren T. MiR-138-5p suppresses lung adenocarcinoma cell epithelial-mesenchymal transition, proliferation and metastasis by targeting ZEB2. Pathol. Res Pract 215, 861–872, 2019.10.1016/j.prp.2019.01.029
DOI: https://doi.org/10.2478/enr-2020-0022 | Journal eISSN: 1336-0329 | Journal ISSN: 1210-0668
Language: English
Page range: 196 - 206
Published on: Aug 27, 2020
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2020 Dariia O. Tsymbal, Dmytro O. Minchenko, Olena O. Khita, Olha V. Rudnytska, Yulia M. Viletska, Yulia O. Lahanovska, Qiuxia He, Kechun Liu, Oleksandr H. Minchenko, published by Slovak Academy of Sciences, Institute of Experimental Endocrinology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.