Glucose deprivation affects the expression of genes encoding cAMP-activated protein kinase and related proteins in U87 glioma cells in ERN1 dependent manner

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.0914072107293260020702765Search in Google Scholar

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, 2013.10.1186/1471-2407-13-597387867024330607Search in Google Scholar

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-05-314316452235Search in Google Scholar

Beristain AG, Molyneux, Joshi PA, Pomroy NC, Di Grappa MA, Chang MC, Kirschner LS, Prive GG, Pujana MA, Khokha R. PKA SD signaling drives mammary tumorigenesis through Src. Oncogene 34, 1160–1173, 2015.10.1038/onc.2014.4124662820Search in Google Scholar

Bochkov VN, Philippova M, Oskolkova O, Kadl A, Furnkranz A, Karabeg E, Breuss J, Minchenko OH, Mechtcheriakova D, Hohensinner P, Rychli K, Wojta J, Resink T, Binder BR, Leitinger N. Oxidized phospholipids stimulate angiogenesis via induction of VEGF, IL-8, COX-2 and ADAMTS-1 metalloprotease, implicating a novel role for lipid oxidation in progression and destabilization of atherosclerotic lesions. Circ Res 99, 900–908, 2006.10.1161/01.RES.0000245485.04489.ee16973904Search in Google Scholar

Cantara S, D’Angeli F, Toti P, Lignitto L, Castagna MG, Capuano S, Prabhakar BS, Feliciello A, Pacini F. Expression of the ring ligase PRAJA2 in thyroid cancer. J Clin Endocrinol Metab 97, 4253–4259, 2012.10.1210/jc.2012-236022948757Search in Google Scholar

Caretta A, Mucignat-Caretta C. Protein kinase A in cancer. Cancers (Basel) 3, 913–926, 2011.10.3390/cancers3010913375639624212646Search in Google Scholar

Chevet E, Hetz C, Samali A. Endoplasmic reticulum stress-activated cell reprogramming in oncogenesis. Cancer Discov 5, 586–597, 2015.10.1158/2159-8290.CD-14-149025977222Search in Google Scholar

Cohen JN, Joseph NM, North JP, Onodera C, Zembowicz A, LeBoit PE. Genomic analysis of pigmented epithelioid melanocytomas reveals recurrent alterations in PRKAR1A, and PRKCA genes. Am J Surg Pathol 41, 1333–1346, 2017.10.1097/PAS.000000000000090228796000Search in Google Scholar

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.1117500108324854322106309Search in Google Scholar

Gong M, Ye S, Li WX, Zhang J, Liu Y, Zhu J, Lv W, Zhang H, Wang J, Lu A, He K. Regulatory function of praja ring finger ubiquitin ligase 2 mediated by the P2rx3/P2rx7 axis in mouse hippocampal neuronal cells. Am J Physiol Cell Physiol 318, C1123–C1135, 2020.10.1152/ajpcell.00070.201932267716Search in Google Scholar

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.2012.06.00222687625Search in Google Scholar

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.1002277460742726469762Search in Google Scholar

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.2018.08.15830236849Search in Google Scholar

Hedrick ED, Agarwal E, Leiphrakpam PD, Haferbier KL, Brattain MG, Chowdhury S. Differential PKA activation and AKAP association determines cell fate in cancer cells. J Mol Signal 8, 10, 2013.10.1186/1750-2187-8-10385303224083380Search in Google Scholar

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/s41589-019-0326-231320759Search in Google Scholar

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.2013.01.00923395000Search in Google Scholar

Hughes D, Mallucci GR. The unfolded protein response in neurodegenerative disorders – therapeutic modulation of the PERK pathway. FEBS J 286, 342–355, 2019.10.1111/febs.1442229476642Search in Google Scholar

Huk DJ, Ashtekar A, Magner A, La Perle K, Kirschner LS. Deletion of Rap1b, but not Rap1a or Epac1, reduces protein kinase A-mediated thyroid cancer. Thyroid 28, 1153–1161, 2018.10.1089/thy.2017.0528615445529882482Search in Google Scholar

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–e00516, 2017.10.1128/MCB.00479-16547754928242652Search in Google Scholar

Jewell JL, Fu V, Hong AW, Yu FX, Meng D, Melick CH, Wang H, Lam WM, Yuan HX, Taylor SS, Guan KL. GPCR signaling inhibits mTORC1 via PKA phosphorylation of Raptor. Elife 8, e43038, 2019.10.7554/eLife.43038Search in Google Scholar

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.22085Search in Google Scholar

King MM, Huang CY, Chock PB, Nairn AC, Hemmings HC Jr, Chan KF, Greengard P. Mammalian brain phospho-proteins as substrates for calcineurin. J Biol Chem 259, 8080–8083, 1984.10.1016/S0021-9258(17)39694-1Search in Google Scholar

Knighton DR, Zheng JH, Ten Eyck LF, Xuong NH, Taylor SS, Sowadski JM. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 414–420, 1991.10.1126/science.18623431862343Search in Google Scholar

Kryvdiuk IV, Minchenko DO Hlushchak NA, Ratushna OO, Karbovskyi LL, Minchenko OH. Inhibition of IRE1 signaling modifies effect of glucose deprivation on the expression of TNFα-induced protein and TNF receptor superfamily genes in U87 glioma cells. Ukr Biochem J 87, 36–51, 2015.10.15407/ubj87.06.03627025058Search in Google Scholar

Kubaichuk K, Minchenko D, Kryvdiuk I, Hubenia O, Minchenko O. The expression of CTGF, TEIBS1, PLAU and PLAUR genes in U87 glioma cells with signaling enzyme ERNI loss of function: effect of glucose and gluta-mine deprivation. Eur J Cancer 49, S128–S130, 2013.Search in Google Scholar

Lester LB, Scott JD. Anchoring and scaffold proteins for kinases and phosphatases. Recent Prog Horm Res 52, 409–429, 1997.Search in Google Scholar

Lhomond S, Avril T, Dejeans N, Voutetakis K, Doultsinos D, McMahon M, Pineau R, Obacz J, Papadodima O, Jouan F, Bourien H, Logotheti M, Jegou G, Pallares-Lupon N, Schmit K, Le Reste PJ, Etcheverry A, Mosser J, Barroso K, Vauleon E, Maurel M, Samali A, Patterson JB, Pluquet O, Hetz C, Quillien V, Chatziioannou A, Chevet E. Dual IRE1 RNase functions dictate glioblastoma development. EMBO Mol Med 10, e7929, 2018.10.15252/emmm.201707929584054129311133Search in Google Scholar

Lignitto L, Carlucci A, Sepe M, Stefan E, Cuomo O, Nistico R, Scorziello A, Savoia C, Garbi C, Annunziato L, Feliciello A. Control of PKA stability and signalling by the RING ligase praja2. Nat Cell Biol 13, 412–422, 2011.10.1038/ncb220921423175Search in Google Scholar

Lignitto L, Arcella A, Sepe M, Rinaldi L, Delle Donne R, Gallo A, Stefan E, Bachmann VA, Oliva MA, Tiziana Storlazzi C, L’Abbate A, Brunetti A, Gargiulo S, Gramanzini M, Insabato L, Garbi C, Gottesman ME, Feliciello A. Proteolysis of MOB1 by the ubiquitin ligase praja2 attenuates Hippo signalling and supports glioblastoma growth. Nat Commun 4, 1822, 2013.10.1038/ncomms2791367424223652010Search in Google Scholar

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/s41467-018-05763-8609393130111846Search in Google Scholar

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.M110978200451887111744734Search in Google Scholar

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_1523363253Search in Google Scholar

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-2014-0001Search in Google Scholar

Minchenko DO, Kharkova AP, Tsymbal DO, Karbovskyi LL, Minchenko OH. Expression of insulin-like growth factor binding protein genes and its hypoxic regulation in U87 glioma cells depends on ERN1 mediated signaling pathway of endoplasmic reticulum stress. Endocr Regul 49, 73–83, 2015a.10.4149/endo_2015_02_7325960008Search in Google Scholar

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 Regul 49, 185–197, 2015b.10.4149/endo_2015_04_18526494037Search in Google Scholar

Minchenko DO, Riabovol OO, Halkin OV, Ratushna OO, Tsymbal DO, Minchenko OH. IRE-1α regulates expression of ubiquitin specific peptidases during hypoxic response in U87 glioma cells. Endoplasm Reticul Stress Dis 3, 50–62, 2016a.10.1515/ersc-2016-0003Search in Google Scholar

Minchenko DO, Riabovol OO, Tsymbal DO, Ratushna OO, Minchenko OH. Inhibition of IRE1 affects the expression of genes encoded glucocorticoid receptor and some related factors and their hypoxic regulation in U87 glioma cells. Endocr Regul 50, 127–136, 2016b.10.1515/enr-2016-001427560795Search in Google Scholar

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-2019-002531734650Search in Google Scholar

Minchenko DO, Tsymbal DO, Luzina OY, Riabovol OO, Danilovskyi SV, Minchenko OH. Silencing of NAMPT leads to up-regulation of insulin receptor substrate 1 gene expression in U87 glioma cells. Endocr Reg 54, 31–42, 2020.10.2478/enr-2020-000532597148Search in Google Scholar

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, 76–87, 2015c.10.15407/ubj87.02.076Search in Google Scholar

Minchenko OH, Tsymbal DO, Minchenko DO, Moenner M, Kovalevska OV, Lypova NM. Inhibition of kinase and endoribonuclease activity of ERN1/IRE1α affects expression of proliferation-related genes in U87 glioma cells. Endoplasm Reticul Stress Dis 2, 18–29, 2015d.10.1515/ersc-2015-0002Search in Google Scholar

Minchenko OH, Kryvdiuk IV, Minchenko DO, Riabovol OO, Halkin OV. Inhibition of IRE1 signaling affects expression of a subset genes encoding for TNF-related factors and receptors and modifies their hypoxic regulation in U87 glioma cells. Endoplasm Reticul Stress Dis 3, 1–15, 2016c.10.1515/ersc-2016-0001Search in Google Scholar

Minchenko OH, Tsymbal DO, Minchenko DO, Hnatiuk OS, Prylutskyy YI, Prylutska SV, Ritter U. Suppression of the expression of genes associated with immune response in normal human astrocytes upon treatment by single-walled carbon nanotubes. Toxicology in Vitro 52, 122–130, 2018.10.1016/j.tiv.2018.06.01129906516Search in Google Scholar

Olsen SR, Uhler MD. Inhibition of protein kinase-A by overexpression of the cloned human protein kinase inhibitor. Mol Endocrinol 5, 1246–1256, 1991.10.1210/mend-5-9-12461770951Search in Google Scholar

Papaioannou A, Chevet E. Driving cancer tumorigenesis and metastasis through UPR signaling. Curr Top Microbiol Immunol 414, 159–192, 2018.10.1007/82_2017_3628710693Search in Google Scholar

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-2019-002431734653Search in Google Scholar

Rusmini P, Cortese K, Crippa V, Cristofani R, Cicardi ME, Ferrari V, Vezzoli G, Tedesco B, Meroni M, Messi E, Piccolella M, Galbiati M, Garrè M, Morelli E, Vaccari T, Poletti A. Trehalose induces autophagy via lysosomal-mediated TFEB activation in models of motoneuron degeneration. Autophagy 15, 631–651, 2019.10.1080/15548627.2018.1535292652681230335591Search in Google Scholar

Saloustros E, Salpea P, Starost M, Liu S, Faucz FR, London E, Szarek E, Song WJ, Hussain M, Stratakis CA. Prkar1a gene knockout in the pancreas leads to neuroendocrine tumorigenesis. Endocr Relat Cancer 24, 31–40, 2017.10.1530/ERC-16-0443512394527803029Search in Google Scholar

Shih M, Lin F, Scott JD, Wang HY, Malbon CC. Dynamic complexes of beta2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J Biol Chem 274, 1588–1595, 1999.10.1074/jbc.274.3.15889880537Search in Google Scholar

Singhi AD, Wood LD, Parks E, Torbenson MS, Felsenstein M, Hruban RH, Nikiforova MN, Wald AI, Kaya C, Nikiforov YE, Favazza L, He J, McGrath K, Fasanella KE, Brand RE, Lennon AM, Furlan A, Dasyam AK, Zureikat AH, Zeh HJ, Lee K, Bartlett DL, Slivka A. Recurrent rearrangements in PRKACA and PRKACB in intraductal oncocytic papillary neoplasms of the pancreas and bile duct. Gastroenterology 158, 573–582, 2020.10.1053/j.gastro.2019.10.028701055431678302Search in Google Scholar

Soh RYZ, Lim JP, Samy RP, Chua PJ, Bay BH. A-kinase anchor protein 12 (AKAP12) inhibits cell migration in breast cancer. Exp Mol Pathol 105, 364–370, 2018.10.1016/j.yexmp.2018.10.01030385176Search in Google Scholar

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, 2016.10.15407/fz62.01.00329537195Search in Google Scholar

Tsymbal DO, Minchenko DO, Hnatiuk OS, Luzina OY, Minchenko OH. Effect of hypoxia on the expression of a subset of proliferation related genes in IRE1 knockdown U87 glioma cells. Adv Biol Chem 7, 195–210, 2017.10.4236/abc.2017.76014Search in Google Scholar

Wang S, Cheng Y, Zheng Y, He Z, Chen W, Zhou W, Duan C, Zhang C. PRKAR1A is a functional tumor suppressor inhibiting ERK/Snail/E-cadherin pathway in lung adenocarcinoma. Sci Rep 6, 39630, 2016.10.1038/srep39630517164127995993Search in Google Scholar

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 Dis 5, e1337, 2014.10.1038/cddis.2014.292412308625032860Search in Google Scholar

Yun JW, Kim M, Cho SD, Lee JY, Bae ON, Lim KM. Highly expressed protein kinase A inhibitor α and suppression of protein kinase A may potentiate acetaminophen-induced hepatotoxicity. Toxicol Lett 229, 59–65, 2014.10.1016/j.toxlet.2014.06.01024910983Search in Google Scholar

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/s12035-016-0314-427900679Search in Google Scholar

Zhong J, Wang H, Chen W, Sun Z, Chen J, Xu Y, Weng M, Shi Q, Ma D, Miao C. Ubiquitylation of MFHAS1 by the ubiquitin ligase praja2 promotes M1 macrophage polarization by activating JNK and p38 pathways. Cell Death Dis 8, e2763, 2017.10.1038/cddis.2017.102552068428471450Search in Google Scholar