"Biotechnologia Acta" V. 9, No 5, 2016
https://doi.org/10.15407/biotech9.05.007
Р. 7-17, Bibliography 48, English
Universal Decimal Classification: 577.112:616
1 Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine, Kyiv
2 Bohomolets National Medical University, Kyiv
We have studied the effect of glucose deprivation on the expression of genes encoding for ubiquitin specific peptidases — USP and autophagy related 7 ATG7 in U87 glioma cells in relation to inhibition of inositol requiring enzyme-1 (IRE1). It was shown that glucose deprivation was downregulated the expression of USP1 and USP10 genes and up-regulated USP4 and USP25 genes in control (transfected by empty vector) glioma cells. At the same time, the expression level of USP14, USP22, and ATG7 genes in these cells did not significantly change upon glucose deprivation condition. Inhibition of ІRE1 signaling enzyme function in U87 glioma cells modified effect of glucose deprivation on the expression of most studied genes. Therefore, glucose deprivation affected the expression level of most ubiquitin specific peptidases genes in relation to the functional activity of IRE1 enzyme, which controls cell proliferation and tumor growth as a central mediator of endoplasmic reticulum stress.
Ключові слова: mRNA expression, USP genes, IRE1 inhibition, glucose deprivation, U87 glioma cells.
© Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine, 2016
References
1. Satija Y. K., Bhardwaj A., Das S. A portrayal of E3 ubiquitin ligases and deubiquitylases in cancer. Int. J. Cancer. 2013, V. 133, P. 2759?2768. https://doi.org/10.1002/ijc.28129
2. Mojsa B., Lassot I., Desagher S. Mcl-1 ubiquitination: unique regulation of an essential survival protein. Cells. 2014, V. 3, P. 418?437. https://doi.org/10.3390/cells3020418
3. Zhang J., Zhang X., Xie F., Zhang Z., van Dam H., Zhang L., Zhou F. The regulation of TGF-?/SMAD signaling by protein deubiquitination. Protein Cell. 2014, V. 5, P. 503?517. https://doi.org/10.1007/s13238-014-0058-8
4. Kessler B. M., Edelmann M. J. PTMs in conversation: activity and function of deubiquitinating enzymes regulated via post-translational modifications. Cell. Biochem. Biophys. 2011, V. 60, P. 21?38. https://doi.org/10.1007/s12013-011-9176-6
5. Li J., Tan Q., Yan M., Liu L., Lin H., Zhao F., Bao G., Kong H., Ge C., Zhang F., Yu T., Li J., He X., Yao M. miRNA-200c inhibits invasion and metastasis of human non-small cell lung cancer by directly targeting ubiquitin specific peptidase 25. Mol. Cancer. 2014, V. 13, P. 166. https://doi.org/10.1186/1476-4598-13-166
6. Danilovskyi S. V., Minchenko D. O., Karbovskyi L. L., Moliavko O. S., Kovalevska O. V., Minchenko O. H. ERN1 knockdown modifies the hypoxic regulation of TP53, MDM2, USP7 and PERP gene expressions in U87 glioma cells. Ukr. Biochem. J. 2014, 86 (4), 90?102. https://doi.org/10.15407/ubj86.04.090
7. Kashiwaba S., Kanao R., Masuda Y., Kusumoto-Matsuo R., Hanaoka F., Masutani C. USP7 is a suppressor of PCNA ubiquitination and oxidative-stress-induced mutagenesis in human cells. Cell Rep. 2015, V. 13, P. 2072?2080. https://doi.org/10.1016/j.celrep.2015.11.014
8. Zhiqiang Z., Qinghui Y., Yongqiang Z., Jian Z., Xin Z., Haiying M., Yuepeng G. USP1 regulates AKT phosphorylation by modulating the stability of PHLPP1 in lung cancer cells. J. Cancer Res. Clin. Oncol. 2012, V. 138, P. 1231?1238. https://doi.org/10.1007/s00432-012-1193-3
9. Lee J. K., Chang N., Yoon Y., Yang H., Cho H., Kim E., Shin Y., Kang W., Oh Y. T., Mun G. I., Joo K. M., Nam D. H., Lee J. USP1 targeting impedes GBM growth by inhibiting stem cell maintenance and radioresistance. Neuro Oncol. 2016, V. 18, P. 37?47. https://doi.org/10.1093/neuonc/nov091
10. Villamil M. A., Liang Q., Chen J., Choi Y. S., Hou S., Lee K. H., Zhuang Z. Serine phosphorylation is critical for the activation of ubiquitin-specific protease 1 and its interaction with WD40-repeat protein UAF1. Biochemistry. 2012, V. 51, P. 9112?9123. https://doi.org/10.1021/bi300845s
11. Garcia-Santisteban I., Zorroza K., Rodriguez J. A. Two nuclear localization signals in USP1 mediate nuclear import of the USP1/UAF1 complex. PLoS ONE. 2012, V. 7, E38570. https://doi.org/10.1371/journal.pone.0038570
12. Li Z., Hao Q., Luo J., Xiong J., Zhang S., Wang T., Bai L., Wang W., Chen M., Wang W., Gu L., Lv K., Chen J. USP4 inhibits p53 and NF-?B through deubiquitinating and stabilizing HDAC2. Oncogene. 2016, V. 35, P. 2902?2912. https://doi.org/10.1038/onc.2015.349
13. Yun S. I., Kim H. H., Yoon J. H., Park W. S., Hahn M. J., Kim H. C., Chung C. H., Kim K. K. Ubiquitin specific protease 4 positively regulates the WNT/?-catenin signaling in colorectal cancer. Mol. Oncol. 2015, V. 9, P. 1834?1851. https://doi.org/10.1016/j.molonc.2015.06.006
14. Zhang J., Zhang X., Xie F., Zhang Z., van Dam H., Zhang L., Zhou F. The regulation of TGF-?/SMAD signaling by protein deubiquitination. Protein Cell. 2014, V. 5, P. 503?517. https://doi.org/10.1007/s13238-014-0058-8
15. Liu H., Xu X. F., Zhao Y., Tang M. C., Zhou Y. Q., Lu J., Gao F. H. MicroRNA-191 promotes pancreatic cancer progression by targeting USP10. Tumour Bio. 2014, V. 35, P. 12157?12163. https://doi.org/10.1007/s13277-014-2521-9
16. Lin Z., Yang H., Tan C., Li J., Liu Z., Quan Q., Kong S., Ye J., Gao B., Fang D. USP10 antagonizes c-Myc transcriptional activation through SIRT6 stabilization to suppress tumor formation. Cell Rep. 2013, V. 5, P. 1639?1649. https://doi.org/10.1016/j.celrep.2013.11.029
17. Wang Y., Wang J., Zhong J., Deng Y., Xi Q., He S., Yang S., Jiang L., Huang M., Tang C., Liu R. Ubiquitin-specific protease 14 (USP14) regulates cellular proliferation and apoptosis in epithelial ovarian cancer. Med. Oncol. 2015, V. 32, P. 379. https://doi.org/10.1007/s12032-014-0379-8
18. Xu D., Shan B., Lee B. H., Zhu K., Zhang T., Sun H., Liu M., Shi L., Liang W., Qian L., Xiao J., Wang L., Pan L., Finley D., Yuan J. Phosphorylation and activation of ubiquitin-specific protease-14 by Akt regulates the ubiquitin-proteasome system. Elife. 2015, V. 4, e10510. https://doi.org/10.7554/eLife.10510
19. D'Arcy P., Wang X., Linder S. Deubiquitinase inhibition as a cancer therapeutic strategy. Pharmacol. Ther. 2015, V. 147, P. 32?54. https://doi.org/10.1016/j.pharmthera.2014.11.002
20. Tang B., Tang F., Li B., Yuan S., Xu Q., Tomlinson S., Jin J., Hu W., He S. High USP22 expression indicates poor prognosis in hepatocellular carcinoma. Oncotarget. 2015, V. 6, P. 12654?12667. https://doi.org/10.18632/oncotarget.3705
21. Liu Y. L., Zheng J., Tang L. J., Han W., Wang J. M., Liu D. W., Tian Q. B. The deubiquitinating enzyme activity of USP22 is necessary for regulating HeLa cell growth. Gene. 2015, V. 572, P. 49?56. https://doi.org/10.1016/j.gene.2015.06.075
22. Ao N., Liu Y., Bian X., Feng H., Liu Y. Ubiquitin-specific peptidase 22 inhibits colon cancer cell invasion by suppressing the signal transducer and activator of transcription 3/matrix metalloproteinase 9 pathway. Mol. Med. Rep. 2015, V. 12, P. 2107?2113.
23. Blount J. R., Burr A. A., Denuc A., Marfany G., Todi S. V. Ubiquitin-specific protease 25 functions in endoplasmic reticulum-associated degradation. PLoS One. 2012, V. 7, e36542. https://doi.org/10.1371/journal.pone.0036542
24. Kim S., Lee D., Lee J., Song H., Kim H. J., Kim K. T. Vaccinia-related kinase 2 controls the stability of the eukaryotic chaperonin TRiC/CCT by inhibiting the deubiquitinating enzyme USP25. Mol. Cell. Biol. 2015, V. 35, P. 1754?1762. https://doi.org/10.1128/MCB.01325-14
25. Galluzzi L., Bravo-San Pedro J. M., Kroemer G. Autophagy mediates tumor suppression via cellular senescence. Trend. Cell Biol. 2016, V. 26, P. 1?3.
26. Moenner M., Pluquet O., Bouchecareilh M., Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 2007, V. 67, P. 10631–10634. https://doi.org/10.1158/0008-5472.CAN-07-1705
27. 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, a004424. https://doi.org/10.1101/cshperspect.a004424
28. Pluquet O., Dejeans N., Chevet E. Watching the clock: endoplasmic reticulum-mediated control of circadian rhythms in cancer. Ann. Med. 2014, V. 46, P. 233?243. https://doi.org/10.3109/07853890.2013.874664
29. Auf G., Jabouille A., Guerit S., Pineau R., Delugin M., Bouchecareilh M., Magnin N., Favereaux A., Maitre M., Gaiser T., von Deimling A., Czabanka M., Vajkoczy P., Chevet E., Bikfalvi A., 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, V. 107, P. 15553–15558. https://doi.org/10.1073/pnas.0914072107
30. Lenihan C. R., Taylor C. T. The impact of hypoxia on cell death pathways. Biochem. Soc. Trans. 2013, V. 41, P. 657–663. https://doi.org/10.1042/BST20120345
31. Chesney J., Clark J., Klarer A. C., Imbert-Fernandez Y., Lane A. N., Telang S. Fructose-2,6-bisphosphate synthesis by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 4 (PFKFB4) is required for the glycolytic response to hypoxia and tumor growth. Oncotarget. 2014, V. 5, P. 6670?6686. https://doi.org/10.18632/oncotarget.2213
32. Hetz C., Chevet E., Harding H. P. Targeting the unfolded protein response in disease. Nat. Rev. Drug Discov. 2013, V. 12, P. 703?719. https://doi.org/10.1038/nrd3976
33. Minchenko O. H., Tsymbal D. O., Moenner M., Minchenko D. O., Kovalevska O. V., Lypova N. M. Inhibition of the endoribonuclease of ERN1 signaling enzyme affects the expression of proliferation-related genes in U87 glioma cells. Endoplasm. Reticul. Stress Dis. 2015, V. 2, P. 18?29. https://doi.org/10.1515/ersc-2015-0002
34. Mani? 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, V. 307, P. 901? 907. https://doi.org/10.1152/ajpcell.00292.2014
35. Minchenko O. H., Kryvdiuk I. V., Minchenko D. O., Riabovol O. O., Halkin O. V. 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. 2016, V. 3, P. 1?15. https://doi.org/10.1515/ersc-2016-0001
36. 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. https://doi.org/10.1073/pnas.1117500108
37. Huber A. L., Lebeau J., Guillaumot P., P?trilli V., Malek M., Chilloux J., Fauvet F., Payen L., Kfoury A., Renno T., Chevet E., Mani? 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.
38. Tsymbal D. O., Minchenko D. O., Riabovol O. O., Ratushna O. O., Minchenko O. H. IRE1 knockdown modifies glucose and glutamine deprivation effects on the expression of proliferation related genes in U87 glioma cells. Biotechnologia Acta. 2016, 9 (1), 26?37. doi: 10.15407/biotech8.06.009.
39. Auf G., Jabouille A., Delugin M., Gu?rit 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. https://doi.org/10.1186/1471-2407-13-597
40. Minchenko D. O., Danilovskyi S. V., Kryvdiuk I. V., Bakalets T. V., Lypova N. M., Karbovsky L. L., Minchenko O. H. Inhibition of ERN1 modifies the hypoxic regulation of the expression of TP53-related genes in U87 glioma cells. Endoplasm. Reticul. Stress Dis. 2014, V. 1, P. 18?26. https://doi.org/10.2478/ersc-2014-0001
41. 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, V. 99, P. 900?908. https://doi.org/10.1161/01.RES.0000245485.04489.ee
42. Hou X., Wang L., Zhang L., Pan X., Zhao W. Ubiquitin-specific protease 4 promotes TNF-alpha-induced apoptosis by deubiquitination of RIP1 in head and neck squamous cell carcinoma. FEBS Lett. 2013, V. 587, P. 311?316. https://doi.org/10.1016/j.febslet.2012.12.016
43. Sun X. X., Challagundla K. B., Dai M. S. Positive regulation of p53 stability and activity by the deubiquitinating enzyme otubain 1. EMBO J. 2012, V. 31, P. 576?592. https://doi.org/10.1038/emboj.2011.434
44. Hu J., Yang D., Zhang H., Liu W., Zhao Y., Lu H., Meng Q., Pang H., Chen X., Liu Y., Cai L. USP22 promotes tumor progression and induces epithelial-mesenchymal transition in lung adenocarcinoma. Lung Cancer. 2015, V. 88, P. 239?245. https://doi.org/10.1016/j.lungcan.2015.02.019
45. Xiong J., Gong Z., Zhou X., Liu J., Jiang H. E., Wu P., Li W. p38 mitogen-activated protein kinase inhibits USP22 transcription in HeLa cells. Biomed Rep. 2015, V. 3, P. 461?467.
46. L?vy J., Cacheux W., Bara M. A., L'Hermitte A., Lepage P., Fraudeau M., Trentesaux C., Lemarchand J., Durand A., Crain A. M., Marchiol C., Renault G., Dumont F., Letourneur F., Delacre M., Schmitt A., Terris B., Perret C., Chamaillard M., Couty J. P., Romagnolo B. Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth. Nat. Cell. Biol. 2015, V. 17, P. 1062?1073. https://doi.org/10.1038/ncb3206
47. Backer M. V., Backer J. M., Chinnaiyan P. Targeting the unfolded protein response in cancer therapy. Meth. Enzymol. 2011, V. 491, P. 37–56. https://doi.org/10.1016/B978-0-12-385928-0.00003-1
48. Johnson G. G., White M. C., Grimaldi M. Stressed to death: targeting endoplasmic reticulum stress response induced apoptosis in gliomas. Curr. Pharm. Des. 2011, V. 17, P. 284?292. https://doi.org/10.2174/138161211795049660