The ERN1 signaling pathway of unfolded protein controls the expression of EDEM1 and its hypoxic regulation in glioblastoma cells
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References
- Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, Dynlacht BD. XBP1 controls diverse cell type- and conditions-specific transcriptional regulatory networks. Molecular Cell 27, 53–66, 2007.
- 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.
- 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 USA 107, 15553–15558, 2010.
- 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.
- Avril T, Vauleon E, Chevet E. Endoplasmic reticulum stress signaling and chemotherapy resistance in solid cancers. Oncogenesis 6, e373, 2017.
- Batie M, Rocha S. Gene transcription and chromatin regulation in hypoxia. Biochem Soc Trans 48, 1121–1128, 2020.
- Chevet E, Hetz C, Samali A. Endoplasmic reticulum stress-activated cell reprogramming in oncogenesis. Cancer Discov 5, 586–597, 2015.
- Chiritoiu M, Chiritoiu GN, Munteanu CVA, Pastrama F, Ivessa NE, Petrescu SM. EDEM1 drives misfolded protein degradation via ERAD and exploits ER-phagy as back-up mechanism when ERAD is impaired. Int J Mol Sci 21, 3468, 2020.
- Das I, Png CW, Oancea I, Hasnain SZ, Lourie R, Proctor M, Eri RD, Sheng Y, Crane DI, Florin TH, McGuckin MA. Glucocorticoids alleviate intestinal ER stress by enhancing protein folding and degradation of misfolded proteins. J Exp Med 210, 1201‒1216, 2013.
- Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumor. Nat Rev Cancer 8, 705–713, 2008.
- Doultsinos D, Avril T, Lhomond S, Dejeans N, Guedat P, Chevet E. Control of the unfolded protein response in health and disease. SLAS Discov 22, 787–800, 2017.
- Flintoaca Alexandru PR, Chiritoiu GN, Lixandru D, Zurac S, Ionescu-Targoviste C, Petrescu SM. EDEM1 regulates the insulin mRNA level by inhibiting the endoplasmic reticulum stress-induced IRE1/JNK/c-Jun pathway. iScience 26, 107956, 2023.
- Ghenea S, Chiritoiu M, Tacutu R, Miranda-Vizuete A, Petrescu SM. Targeting EDEM protects against ER stress and improves development and survival in C. elegans. PLoS Genet 18, e1010069, 2022.
- Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol
- Katsuki R, Kanuka M, Ohta R, Yoshida S, Tamura T. Turnover of EDEM1, an ERAD-enhancing factor, is mediated by multiple degradation routes. Genes Cells 29, 486‒502, 2024.
- Krasnytska DA, Viletska YM, Minchenko DO, Khita OO, Tsymbal DO, Cherednychenko AA, Kozynkevych HE, Oksiom NS, Minchenko OH. ERN1 dependent impact of glucose and glutamine deprivations on <em>PBX3</em>, <em>PBXIP1</em>, <em>PAX6</em>, <em>MEIS1</em>, and <em>MEIS2</em> gene expressions in U87 glioma cells. Endocr Regul 57, 37–47, 2023.
- 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.
- Minchenko A, Caro J. Regulation of endothelin-1 gene expression in human microvascular endothelial cells by hypoxia and cobalt: role of hypoxia responsible element. Mol Cell Biochem 208, 53–62, 2000.
- Minchenko A, Leshchinsky I, Opentanova I, Sang N, Srinivas V, Armstead V, 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.
- Minchenko O, Opentanova I, Minchenko D, Ogura T, Esumi H. Hypoxia induces transcription of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 4 gene via hypoxia-inducible factor-1alpha activation. FEBS Lett 576, 14–20, 2004.
- Minchenko OH, Tsymbal DO, Minchenko DO, Moenner M, Kovalevska OV, Lypova NM. Inhibition of kinase and endoribonuclease activity of ERN1/IRE1a affects expression of proliferation-related genes in U87 glioma cells. Endoplasm Reticul Stress Dis 2, 18–29, 2015.
- 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 Regul 53, 250–262, 2019.
- Minchenko DO, Khita OO, Tsymbal DO, Danilovskyi SV, Rudnytska OV, Halkin OV, Kryvdiuk IV, Smeshkova MV, Yakymchuk MM, Bezrodnyi BH, Minchenko OH. Expression of IDE and PITRM1 genes in IRE1 knockdown U87 glioma cells: effect of hypoxia and glucose deprivation. Endocr Regul 54, 183–195, 2020.
- Minchenko OH, Tsymbal DO, Khita OO, Minchenko DO. Inhibition of ERN1 signaling is important for the suppression of tumor growth. Clin Cancer Drugs 8, 27–38, 2021.
- Minchenko OH, Khita OO, Krasnytska DA, Viletska YM, Rudnytska OV, Hnatiuk OS, Minchenko DO. ERN1 knockdown affects the expression of TGIF1 and other homeobox genes in U87MG glioblastoma cells. Arch Biochem Biophys 758, 110073, 2024a.
- Minchenko OH, Sliusar MY, Khikhlo YP, Halkin OV, Viletska YM, Khita OO, Minchenko DO. Knockdown of ERN1 disturbs the expression of phosphoserine aminotransferase 1 and related genes in glioblastoma cells. Arch Biochem Biophys 759, 110104, 2024b.
- Minchenko OH, Sliusar MY, Khita OO, Minchenko DO, Viletska YM, Halkin OV, Ledvadna LO, Cherednychenko AA, Khikhlo YP. Inhibition of signaling protein ERN1 increases the sensitivity of serine synthesis gene expressions to glucose and glutamine deprivations in U87MG glioblastoma cells. Endocr Regul 58, 91–100, 2024c.
- Miura K, Katsuki R, Yoshida S, Ohta R, Tamura T. Identification of EGF receptor and thrombospondin-1 as endogenous targets of ER-associated degradation enhancer EDEM1 in HeLa cells. Int J Mol Sci 24, 12171, 2023.
- Molinari M, Calanca V, Galli C, Lucca P, Paganetti P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299, 1397–1400, 2003.
- Nowakowska-Golacka J, Czapiewska J, Sominka H, Sowa-Rogozinska N, Slominska-Wojewodzka M. EDEM1 regulates amyloid precursor protein (APP) metabolism and amyloid-beta production. Int J Mol Sci 23, 117, 2021.
- Obacz J, Avril T, Le Reste PJ, Urra H, Quillien V, Hetz C, Chevet E. Endoplasmic reticulum proteostasis in glioblastoma-from molecular mechanisms to therapeutic perspectives. Sci Signal 10, eaal2323, 2017.
- Oda Y, Hosokawa N, Wada I, Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299, 1394–1397, 2003.
- Olivari S, Galli C, Alanen H, Ruddock L, Molinari M. A novel stress-induced EDEM variant regulating endoplasmic reticulum-associated glycoprotein degradation. J Biol Chem 280, 2424–2428, 2005.
- Papaioannou A, Chevet E. Driving cancer tumorigenesis and metastasis through UPR signaling. Curr Top Microbiol Immunol 414, 159‒192, 2018.
- Papaioannou A, Higa A, Jegou G, Jouan F, Pineau R, Saas L, Avril T, Pluquet O, Chevet E. Alterations of EDEM1 functions enhance ATF6 pro-survival signaling. FEBS J 285, 4146–4164, 2018.
- Pathak H, Varghese J. Edem1 activity in the fat body regulates insulin signalling and metabolic homeostasis in Drosophila. Life Sci Alliance 4, e202101079, 2021.
- Pelizzari-Raymundo D, Doultsinos D, Pineau R, Sauzay C, Koutsandreas T, Langlais T, Carlesso A, Gkotsi E, Negroni L, Avril T, Chatziioannou A, Chevet E, Eriksson LA, Guillory X. A novel IRE1 kinase inhibitor for adjuvant glioblastoma treatment. iScience 26, 106687, 2023.
- Pelizzari-Raymundo D, Maltret V, Nivet M, Pineau R, Papaioannou A, Zhou X, Caradec F, Martin S, Le Gallo M, Avril T, Chevet E, Lafont E. IRE1 RNase controls CD95-mediated cell death. EMBO Rep 25, 1792–1813, 2024.
- Roth J, Zuber C. Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 147, 269–284, 2017.
- Rudnytska OV, Khita OO, Minchenko, Tsymbal DO, Yefimova YV, Sliusar MY, Minchenko OH. The low doses of SWCNTs exhibit a genotoxic effect on the normal human astrocytes by disrupting the functional integrity of the genome. Curr Res Toxicol 2, 64–71, 2021.
- Semenza GL. A compendium of proteins that interact with HIF-1α. Exp Cell Res 356, 128–135, 2017.
- Sliusar MY, Minchenko DO, Khita OO, Tsymbal DO, Viletska YM, Luzina OY, Danilovskyi SV, Ratushna OO, Minchenko OH. Hypoxia controls the expression of genes responsible for serine synthesis in U87MG cells on ERN1-dependent manner. Endocr Regul 57, 252–261, 2023.
- Sun RC, Denko NC. Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth. Cell Metab 19, 285–292, 2014.
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Published on: Mar 12, 2025
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© 2025 Oleksandr H. Minchenko, Vita O. Hrebennykova, Yuliia M. Viletska, Oksana S. Hnatiuk, Myroslava Y. Sliusar, Halyna E. Kozynkevych, Dmytro O. Minchenko, published by Slovak Academy of Sciences
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