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Home Archive 2016 № 1 IRE1 KNOCKDOWN MODIFIES GLUCOSE AND GLUTAMINE DEPRIVATION EFFECTS ON THE EXPRESSION OF PROLIFERATION RELATED GENES IN U87 GLIOMA CELLS D. O. Tsymbal, D. O. Minchenko, O. O. Riabovol, O. O. Ratushna, O. H. Minchenko
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ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)


"Biotechnologia Acta" V. 9, No 1, 2016
https://doi.org/10.15407/biotech9.01.026
Р. 26-37, Bibliography 49, English
Universal Decimal Classification: 577.112:616

IRE1 KNOCKDOWN MODIFIES GLUCOSE AND GLUTAMINE DEPRIVATION EFFECTS ON THE EXPRESSION OF PROLIFERATION RELATED GENES IN U87 GLIOMA CELLS

D. O. Tsymbal 1, D. O. Minchenko 1, 2, O. O. Riabovol 1, O. O. Ratushna 1, O. H. Minchenko1

1 Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine, Kyiv
2 Bohomolets National Medical University, Kyiv

We have studied the expression of genes encoding proliferation related factors and enzymes such as IL13RA2, KRT18, CD24, ING1, ING2, MYL9, BET1, TRAPPC3, ENDOG, POLG, TSFM, and MTIF2 in U87 glioma cells upon glucose and glutamine deprivation in relation to inhibition of inositol requiring enzyme 1, a central mediator of endoplasmic reticulum stress. It was shown that glutamine deprivation leads to up-regulation of the expression of BET1, MYL9, and MTIF2 genes and down-regulation of CD24, ING2, ENDOG, POLG, and TSFM genes in control (with native IRE1) glioma cells. At the same time, glucose deprivation enhances the expression of MYL9 gene only and decreases – ING1, ING2, and MTIF2 genes in control glioma cells. Thus, effect of glucose and glutamine deprivation on gene expressions in glioma cells is gene-specific. Inhibition of inositol requiring enzyme 1 by dnIRE1 significantly modifies the effect of both glutamine and glucose deprivation on the expression of most studied genes with different direction and magnitude, especially for ING2, CD24, and MTIF2 genes. Present study demonstrates that IRE1 knockdown modifies glucose and glutamine deprivation effects on the expression of proliferation related genes and possibly contributes to slower tumor growth of these glioma cells after inhibition of IRE1 signaling enzyme.

Key words: proliferation related genes expression, IRE1 inhibition, glucose and glutamine deprivation, glioma cells

© Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine, 2008

  • References
    • 1. Clarke H. J., Chambers J. E., Liniker E., Marciniak S. J. Endoplasmic reticulum stress in malignancy. Cancer Cell. 2014, 25 (5), 563–573. doi: 10.1016/j.ccr.2014.03.015.

      2. Wang S., Kaufman R. J. The impact of the unfolded protein response on human disease. J. Cell. Biol. 2012, V. 197, P. 857–867. doi: 10.1083/jcb.201110131.

      3. Yadav R. K., Chae S. W., Kim H. R., Chae H. J. Endoplasmic reticulum stress and cancer. J. Cancer Prev. 2014, 19 (2), 75–88. doi: 10.15430/JCP.2014.19.2.75.

      4. Cao S. S., Kaufman R. J. Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin. Ther. Targets. 2013, 17 (4), 437–448. doi: 10.1517/14728222.2013.756471.

      5. Bravo R. 1., Parra V., Gatica D., Rodriguez A. E., Torrealba N., Paredes F., Wang Z. V., Zorzano A., Hill J. A., Jaimovich E., Quest A. F., Lavandero S. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int. Rev. Cell. Mol. Biol. 2013, V. 301, P. 215–290. doi: 10.1016/B978-0-12-407704-1.00005-1.

      6. Manié S. N., 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. 2014, 307 (10), 901–907. doi: 10.1152/ajpcell.00292.2014.

      7. Minchenko O. H., Kharkova A. P., Bakalets T. V., Kryvdiuk I. V. Endoplasmic reticulum stress, its sensor and signaling systems and the role in the regulation of gene expressions in malignant tumor growth and hypoxia. Ukr Biokhim. Zh. 2013, 85 (5), 5–16. (In Ukrainian).

      8. Moenner M., Pluquet O., Bouchecareilh M., Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 2007, 67 (22), 10631–10634. doi: 10.1158/0008-5472.CAN-07-1705.

      9. Drogat B., Auguste P., Nguyen D. T., Bouchecareilh M., Pineau R., Nalbantoglu J., Kaufman R. J., Chevet E., Bikfalvi A., Moenner M. IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo. Cancer Res. 2007, 67 (14), 6700–6707. doi: 10.1158/0008-5472.CAN-06-3235.

      10. Auf G., Jabouille A., Guerit S., Pineau R., North S., Platonova N., Maitre M., Favereaux A., Vajkoczy P., Seno M., Bikfalvi A., Minchenko D., Minchenko O., Moenner M. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (35), 15553–15558. doi: 10.1073/pnas.0914072107.

      11. Minchenko O. H., Kubaichuk K. I., Minchenko D. O., Kovalevska O. V., Kulinich A. O., Lypova N. M. Molecular mechanisms of IRE-1-mediated angiogenesis. Int. J. Physiol. Pathophysiol. 2014, 5 (1), 1–22. http://dx.doi.org/10.1615/IntJPhysPathophys.v5.i1.10

      12. Colombo S. L., 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. U.S.A. 2011, 108 (52), 21069–21074. doi: 10.1073/pnas. 1117500108.

      13. Yalcin A., Clem B. F., Imbert-Fernandez Y., Ozcan S. C., Peker S., ONeal J., Klarer A. C., Clem A. L., 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. 2014, V. 5, P. e1337. doi: 10.1038/cddis.2014.292.

      14. Huber A. L., Lebeau J., Guillaumot P., Pétrilli V., Malek M., Chilloux J., Fauvet F., Payen L., Kfoury A., Renno T., Chevet E., Manié S. N. p58(IPK)-mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression upon low glucose. Mol. Cell. 2013, 49 (6), 1049–1059. doi: 10.1016/j.molcel.2013.01.009.

      15. Lenihan C. R., Taylor C. T. The impact of hypoxia on cell death pathways. Biochem. Soc. Trans. 2013, V. 41, P. 657–663. doi: 10.1042/BST20120345.

      16. Han J., Back S. H., Hur J., Lin Y. H., Gildersleeve R., Shan J., Yuan C. L., Krokowski D., Wang S., Hatzoglou M., Kilberg M. S., Sartor M. A., Kaufman R. J. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell. Biol. 2013, 15 (5), 481–490. doi: 10.1038/ncb2738.

      17. Maurel M., Chevet E., Tavernier J., Gerlo S. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem. Sci. 2014, 39 (5), 245–254. doi: 10.1016/j.tibs. 2014.02.008.

      18. Malhotra J. D., Kaufman R. J. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb. Perspect. Biol. 2011, V. 3, P. a004424. doi: 10.1101/cshperspect.a004424.

      19. Pluquet O., Dejeans N., Chevet E. Watching the clock: endoplasmic reticulum-mediated control of circadian rhythms in cancer. Ann. Med. 2014, 46 (4), 233–243. doi: 10.3109/07853890.2013.874664.

      20. Auf G., Jabouille A., Delugin M., Guérit 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. 2013, V. 13, P. 597. doi: 10.1186/1471-2407-13-597.

      21. Minchenko D. O., Kubaichuk K. I., Hubenia O. V., Kryvdiuk I. V., Kharkova A. P., Herasymenko R. M., Sulik R. V., Karbovskyi L. L., Minchenko O. H. Endoplasmic reticulum stress and angiogenesis in cancer. Int. J. Physiol. Pathophysiol. 2014, 5 (3), 261–281.
      http://dx.doi.org/10.1615/IntJPhysPathophys.v5.i3.90

      22. Pluquet O., Dejeans N., Bouchecareilh M., Lhomond S., Pineau R., Higa A., Delugin M., Combe C., Loriot S., Cubel G., Dugot-Senant N., Vital A., Loiseau H., Gosline S. J., Taouji S., Hallett M., Sarkaria J. N., Anderson K., Wu W., Rodriguez F. J., Rosenbaum J., Saltel F., Fernandez-Zapico M. E., Chevet E. Posttranscriptional regulation of PER1 underlies the oncogenic function of IREα. Cancer Res. 2013, 73 (15), 4732–4743. doi: 10.1158/0008-5472.CAN-12-3989.

      23. Acosta-Alvear D., Zhou Y., Blais A., Tsikitis M., Lents N. H., Arias C., Lennon C. J., Kluger Y., Dynlacht D. D. XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell. 2007, V. 27, P. 53–66. doi:10.1016/j.molcel.2007.06.011.

      24. Hollien J., Lin J. H., Li H., Stevens N., Walter P., Weissman J. S. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell. Biol. 2009, 186 (3), 323–331. doi: 10.1083/jcb.200903014.

      25. Aragón T., van Anken E., Pincus D., Serafimova I. M., Korennykh A. V., Rubio C. A., Walter P. Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature. 2009, 457 (7230), 736–740. doi: 10.1038/nature07641.

      26. Hassler J., Cao S. S., Kaufman R. J. IRE1, a double-edged sword in pre-miRNA slicing and cell death. Dev. Cell. 2012, 23 (5), 921–923. doi: 10.1016/j.devcel.2012.10.025.

      27. Barderas R., Bartolome R. A., Fernandez-Acenero M. J., Torres S., Casal J. I. High expression of IL-13 receptor alpha2 in colorectal cancer is associated with invasion, liver metastasis, and poor prognosis. Cancer Res. 2012, 72 (11), 2780–2790. doi: 10.1158/0008-5472.CAN-11-4090.

      28. Taguchi A., Taylor A. D., Rodriguez J., Celiktaş M., Liu H., Ma X., Zhang Q., Wong C. H., Chin A., Girard L., Behrens C., Lam W. L., Lam S., Minna J. D., Wistuba I. I., Gazdar A. F., Hanash S. M. A search for novel cancer/testis antigens in lung cancer identifies VCX/Y genes, expanding the repertoire of potential immunotherapeutic targets. Cancer Res. 2014, 74 (17), 4694–4705. doi: 10.1158/0008-5472.CAN-13-3725.

      29. Parlato M., Souza-Fonseca-Guimaraes F., Philippart F., Misset B., Adib-Conquy M., Cavaillon J. M. CD24-triggered caspase-dependent apoptosis via mitochondrial membrane depolarization and reactive oxygen species production of human neutrophils is impaired in sepsis. J. Immunol. 2014, 192 (5), 2449–2459. doi: 10.4049/jimmunol.1301055.

      30. Chen J., Tran U. M., Rajarajacholan U., Thalappilly S., Riabowol K. ING1b-inducible microRNA203 inhibits cell proliferation. Br. J. Cancer. 2013, 108 (5), 1143–1148. doi: 10.1038/bjc.2013.50.

      31. Huang Y. Q., Han Z. D., Liang Y. X., Lin Z. Y., Ling X. H., Fu X., Cai C., Bi X. C., Dai Q. S., Chen J. H., He H. C., Chen Y. R., Jiang F. N., Zhong W. D. Decreased expression of myosin light chain MYL9 in stroma predicts malignant progression and poor biochemical recurrence-free survival in prostate cancer. Med. Oncol. 2014, 31 (1), 820. doi: 10.1007/s12032-013-0820-4.

      32. Bose P., Thakur S., Thalappilly S., Ahn B. Y., Satpathy S., Feng X., Suzuki K., Kim S. W., Riabowol K. ING1 induces apoptosis through direct effects at the mitochondria. Cell Death Dis. 2013, V. 4, P. E788. doi: 10.1038/cddis.2013.321.

      33. Liu J., Lin Y., Yang H., Deng Q., Chen G., He J. The expression of p33(ING1), p53, and autophagy-related gene Beclin1 in patients with non-small cell lung cancer. Tumour Biol. 2011, 32 (6), 1113–1121. doi: 10.1007/s13277-011-0211-4.

      34. Guo X. B., Jing C. Q., Li L. P., Zhang L., Shi Y. L., Wang J. S., Liu J. L., Li C. S. Down-regulation of miR-622 in gastric cancer promotes cellular invasion and tumor metastasis by targeting ING1 gene. World J. Gastroenterol. 2011, 17 (14), 1895–1902. doi: 10.3748/wjg.v17.i14.1895.

      35. Thalappilly S., Feng X., Pastyryeva S., Suzuki K., Muruve D., Larocque D., Richard S., Truss M., von Deimling A., Riabowol K., Tallen G. The p53 tumor suppressor is stabilized by inhibitor of growth 1 (ING1) by blocking polyubiquitination. PLoS ONE. 2011, 6 (6), E21065. doi: 10.1371/journal. pone.0021065.

      36. Zhang H., Chen X., Wang J., Guang W., Han W., Zhang H., Tan X., Gu Y. EGR1 decreases the malignancy of human non-small cell lung carcinoma by regulating KRT18 expression. Sci. Rep. 2014, V. 4, P. 5416. doi: 10.1038/srep05416.

      37. Zhang T., Hong W. Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J. Biol. Chem. 2001, 276 (29), 27480–27487. doi: 10.1074/jbc.M102786200.

      38. Zhdanov D. D., Fahmi T., Wang X., Apostolov E. O., Sokolov N. N., Javadov S., Basnakian A. G. Regulation of Apoptotic Endonucleases by EndoG. DNA Cell Biol. 2015, 34 (5), 316–326. doi: 10.1089/dna.2014.2772.

      39. Linkowska K., Jawień A., Marszałek A., Malyarchuk B. A., Tońska K., Bartnik E., Skonieczna K., Grzybowski T. Mitochondrial DNA Polymerase γ Mutations and Their Implications in mtDNA Alterations in Colorectal Cancer. Ann. Hum. Genet. 2015, Apr 7. doi: 10.1111/ahg.12111.

      40. Lee W. T., St John J. The control of mitochondrial DNA replication during development and tumorigenesis. Ann. N. Y. Acad. Sci. 2015, V. 1350, P. 95–106. doi: 10.1111/nyas.12873.

      41. Le Roy F., Silhol M, Salehzada T., Bisbal C. Regulation of mitochondrial mRNA stability by RNase L is translation-dependent and controls IFNalpha-induced apoptosis. Cell Death Differ. 2007, 14 (8), 1406–1413. doi:10.1038/sj.cdd. 4402130.

      42. Swan E. J., Maxwell A. P., McKnight A. J. Distinct methylation patterns in genes that affect mitochondrial function are associated with kidney disease in blood-derived DNA from individuals with Type 1 diabetes. Diabet. Med. 2015, 32 (8), 1110–1115. doi: 10.1111/dme.12775.

      43. Zhang X., Bian X., Kong J. The proapoptotic protein BNIP3 interacts with VDAC to induce mitochondrial release of endonuclease G. PLoS One. 2014, 9 (12), e113642. doi: 10.1371/journal.pone.0113642.

      44. Minchenko D. O., Karbovskyi L. L., Danilovskyi S. V., Moenner M., Minchenko O. H. Effect of hypoxia and glutamine or glucose deprivation on the expression of retinoblastoma and retinoblastoma-related genes in ERN1 knockdown glioma U87 cell line. Am. J. Mol. Biol. 2012, 2 (1), 21–31. doi:10.4236/ajmb.2012.21003.

      45. Bochkov V. N., Philippova M., Oskolkova O., Kadl A., Furnkranz A., Karabeg E., Breuss J., Minchenko O. H., Mechtcheriakova D., Hohensinner P., Rychli K., Wojta J., Resink T., Binder B. R., 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. 2006, 99 (8), 900–908. doi: 10.1161/01.RES.0000245485.04489.ee.

      46. Minchenko D. O., Danilovskyi S. V., Kryvdiuk I. V., Bakalets T. V., Yavorskyi V. V., Sulik R. V., Hubenia O. V., Minchenko O. H. Effect of glutamine and glucose deprivation on the expression of TP53, MDM2, USP7 and PERP genes in glioma U87 cells with IRE-1 knockdown. Int. J. Adv. Med. Sci. 2014, 2 (2), 13–8.

      47. Minchenko D. O., Danilovskyi S. V., Kryvdiuk I. V., Hlushchak N. A., Kovalevska O. V., Karbovskyi L. L., Minchenko O. H. Acute L-glutamine deprivation affects the expression of TP53-related protein genes in U87 glioma cells. Fiziol Zh. 2014, 60 (4), 11–21.

      48. Minchenko D. O., Kharkova A. P., Karbovskyi L. L., Minchenko O. H. 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. 2015, 49 (2), 73–83. doi:10.4149/endo_2015_02_73.

      49. Minchenko D. O., Kharkova A. P., Tsymbal D. O., Karbovskyi L. L., Minchenko O. H. Inhibition of IRE1 affects the expression of insulin-like growth factor binding protein genes and modifies its sensitivity to glucose deprivation in U87 glioma cells. Endocr. Regul. 2015, 49 (4), 185–197. doi:10.4149/endo_2015_04_185.






 

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Home Archive 2016 № 1 IRE1 KNOCKDOWN MODIFIES GLUCOSE AND GLUTAMINE DEPRIVATION EFFECTS ON THE EXPRESSION OF PROLIFERATION RELATED GENES IN U87 GLIOMA CELLS D. O. Tsymbal, D. O. Minchenko, O. O. Riabovol, O. O. Ratushna, O. H. Minchenko

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