Have a personal or library account? Click to login
Endoplasmic reticulum stress-dependent regulation of the expression of serine hydroxymethyltransferase 2 in glioblastoma cells Cover

Endoplasmic reticulum stress-dependent regulation of the expression of serine hydroxymethyltransferase 2 in glioblastoma cells

Open Access
|Jun 2024

References

  1. 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 condition-specific transcriptional regulatory networks. Molecular Cell 27, 53–66, 2007.
  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.
  3. Anderson DD, Quintero CM, Stover PJ. Identification of a de novo thymidylate biosynthesis pathway in mammalian mitochondria. Proc Natl Acad Sci USA 108, 15163–15168, 2011.
  4. 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.
  5. 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.
  6. Avril T, Vauleon E, Chevet E. Endoplasmic reticulum stress signaling and chemotherapy resistance in solid cancers. Oncogenesis 6, e373, 2017.
  7. 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.
  8. Chevet E, Hetz C, Samali A. Endoplasmic reticulum stress-activated cell reprogramming in oncogenesis. Cancer Discov 5, 586–597, 2015.
  9. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumor. Nat Rev Cancer 8, 705–713, 2008.
  10. 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.
  11. Ducker GS, Ghergurovich JM, Mainolfi N, Suri V, Jeong SK, Hsin-Jung Li S, Friedman A, Manfredi MG, Gitai Z, Kim H, Rabinowitz JD. Human SHMT inhibitors reveal defective glycine import as a targetable metabolic vulnerability of diffuse large B-cell lymphoma. Proc Natl Acad Sci USA 114, 11404–11409, 2017.
  12. Engel AL, Lorenz NI, Klann K, Munch C, Depner C, Steinbach JP, Ronellenfitsch MW, Luger AL. Serine-dependent redox homeostasis regulates glioblastoma cell survival. Br J Cancer 122, 1391–1398, 2020.
  13. Giardina G, Brunotti P, Fiascarelli A, Cicalini A, Costa MG, Buckle AM, di Salvo ML, Giorgi A, Marani M, Paone A, Rinaldo S, Paiardini A, Contestabile R, Cutruzzola F. How pyridoxal 5’-phosphate differentially regulates human cytosolic and mitochondrial serine hydroxymethyltransferase oligomeric state. FEBS J 282, 1225–1241, 2015.
  14. He L, Ding Y, Zhou X, Li T, Yin Y. Serine signaling governs metabolic homeostasis and health. Trends Endocrinol Metab 34, 361–372, 2023.
  15. Hennequart M, Labuschagne CF, Tajan M, Pilley SE, Cheung EC, Legrave NM, Driscoll PC, Vousden KH. The impact of physiological metabolite levels on serine uptake, synthesis and utilization in cancer cells. Nat Commun 12, 6176, 2021.
  16. Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol 21, 421–438, 2020.
  17. 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 PBX3, PBXIP1, PAX6, MEIS1, and MEIS2 gene expressions in U87 glioma cells. Endocr Reg 57, 37–47, 2023.
  18. Li AM, Ye J. Reprogramming of serine, glycine and one-carbon metabolism in cancer. Biochim Biophys Acta Mol Basis Dis 1866, 165841, 2020.
  19. 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.
  20. Maddocks OD, Berkers CR, Mason SM, Zheng L, Blyth K, Gottlieb E, Vousden KH. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature 493, 542–546, 2013.
  21. Mattaini KR, Sullivan MR, Vander Heiden MG. The importance of serine metabolism in cancer. J Cell Biol 214, 249–257, 2016.
  22. 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.
  23. 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.
  24. 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.
  25. 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. Cell Pathology 2, 18–29, 2015.
  26. 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.
  27. 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 Reg 54, 183–195, 2020.
  28. 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.
  29. 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 Reg 58, 91–100, 2024.
  30. Minton DR, Nam M, McLaughlin DJ, Shin J, Bayraktar EC, Alvarez SW, Sviderskiy VO, Papagiannakopoulos T, Sabatini DM, Birsoy K, Possemato R. Serine catabolism by SHMT2 is required for proper mitochondrial translation initiation and maintenance of formylmethionyl-tRNAs. Mol Cell 69, 610–621.e5, 2018.
  31. Morscher RJ, Ducker GS, Li SH, Mayer JA, Gitai Z, Sperl W, Rabinowitz JD. Mitochondrial translation requires folate-dependent tRNA methylation. Nature 554, 128–132, 2018.
  32. Nguyen TH, Vemu PL, Hoy GE, Boudjadi S, Chatterjee B, Shern JF, Khan J, Sun W, Barr FG. Serine hydroxymethyltransferase 2 expression promotes tumorigenesis in rhabdomyosarcoma with 12q13-q14 amplification. J Clin Invest 131, e138022, 2021.
  33. 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.
  34. Papaioannou A, Chevet E. Driving cancer tumorigenesis and metastasis through UPR signaling. Curr Top Microbiol Immunol 414, 159–192, 2018.
  35. Qiao Z, Li Y, Cheng Y, Li S, Liu S. SHMT2 regulates esophageal cancer cell progression and immune Escape by mediating m6A modification of c-myc. Cell Biosci 13, 203, 2023.
  36. 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.
  37. Semenza GL. A compendium of proteins that interact with HIF-1α. Exp Cell Res 356, 128–135, 2017.
  38. Shan Y, Liu D, Li Y, Wu C, Ye Y. The expression and clinical significance of serine hydroxymethyltransferase2 in gastric cancer. PeerJ 12, e16594, 2024.
  39. 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 Reg 23, 57, 252–261, 2023.
  40. 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.
  41. Tajan M, Hennequart M, Cheung EC, Zani F, Hock AK, Legrave N, Maddocks ODK, Ridgway RA, Athineos D, Suarez-Bonnet A, Ludwig RL, Novellasdemunt L, Angelis N, Li VSW, Vlachogiannis G, Valeri N, Mainolfi N, Suri V, Friedman, Manfredi M, Blyth K, Sansom OJ, Vousden KH. Serine synthesis pathway inhibition cooperates with dietary serine and glycine limitation for cancer therapy. Nat Commun 12, 366, 2021.
  42. Tedeschi PM, Markert EK, Gounder M, Lin H, Dvorzhinski D, Dolfi SC, Chan LL, Qiu J, DiPaola RS, Hirshfield KM, Boros LG, Bertino JR, Oltvai ZN, Vazquez A. Contribution of serine, folate and glycine metabolism to the ATP, NADPH and purine requirements of cancer cells. Cell Death Dis 4, e877, 2013.
  43. Wang W, Wang M, Du T, Hou Z, You S, Zhang S, Ji M, Xue N, Chen X. SHMT2 promotes gastric cancer development through regulation of HIF1alpha/VEGF/STAT3 signaling. Int J Mol Sci 24, 7150, 2023.
  44. Xie SY, Shi DB, Ouyang Y, Lin F, Chen XY, Jiang TC, Xia W, Guo L, Lin HX. SHMT2 promotes tumor growth through VEGF and MAPK signaling pathway in breast cancer. Am J Cancer Res 12, 3405–3421, 2022.
  45. Yang M, Vousden KH. Serine and one-carbon metabolism in cancer. Nat Rev Cancer 16, 650–662, 2016.
  46. Zhang Y, Huang H, Liu P, Xie Y. NFYB increases chemosensitivity in glioblastoma by promoting HDAC5-mediated transcriptional inhibition of SHMT2. J Neuropathol Exp Neurol 82, 911–920, 2023.
DOI: https://doi.org/10.2478/enr-2024-0016 | Journal eISSN: 1336-0329 | Journal ISSN: 1210-0668
Language: English
Page range: 144 - 152
Published on: Jun 11, 2024
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2024 Oleksandr H. Minchenko, Myroslava Y. Sliusar, Olena O. Khita, Yuliia M. Viletska, Olha Y. Luzina, Serhiy V. Danilovskyi, Dmytro O. Minchenko, published by Slovak Academy of Sciences, Institute of Experimental Endocrinology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.