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Hydrocortisone interacts with endoplasmic reticulum stress in hypoxic regulation of phosphoserine aminotransferase 1 gene expression differently in normal human astrocytes and glioblastoma cells Cover

Hydrocortisone interacts with endoplasmic reticulum stress in hypoxic regulation of phosphoserine aminotransferase 1 gene expression differently in normal human astrocytes and glioblastoma cells

Open Access
|Apr 2025

References

  1. Afshari AR, Sanati M, Aminyavari S, Shakeri F, Bibak B, Keshavarzi Z, Soukhtanloo M, Jalili-Nik M, Sadeghi MM, Mollazadeh H, Johnston TP, Sahebkar A. Advantages and drawbacks of dexamethasone in glioblastoma multiforme. Crit Rev Oncol Hematol 172, 103625, 2022.
  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. 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.
  4. Avril T, Vauleon E, Chevet E. Endoplasmic reticulum stress signaling and chemotherapy resistance in solid cancers. Oncogenesis 6, e373, 2017.
  5. Azher S, Azami O, Amato C, McCullough M, Celentano A, Cirillo N. The non-conventional effects of glucocorticoids in cancer. J Cell Physiol 231, 2368–2373, 2016.
  6. Bao MH, Wong CC. Hypoxia, metabolic reprogramming, and drug resistance in liver cancer. Cells 10, 1715, 2021.
  7. Batie M, Rocha S. Gene transcription and chromatin regulation in hypoxia. Biochem Soc Trans 48, 1121–1128, 2020.
  8. Beaupere C, Liboz A, Feve B, Blondeau B, Guillemain G. Molecular mechanisms of glucocorticoid-induced insulin resistance. Int J Mol Sci 22, 623, 2021.
  9. 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.
  10. Butz H, Patocs A. Mechanisms behind context-dependent role of glucocorticoids in breast cancer progression. Cancer Metastasis Rev 41, 803–832, 2022.
  11. Chevet E, Hetz C, Samali A. Endoplasmic reticulum stress-activated cell reprogramming in oncogenesis. Cancer Discov 5, 586–597, 2015.
  12. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8, 705–713, 2008.
  13. Ding R, Hong W, Huang L, Shao J, Yu W, Xu X. Examination of the effects of microRNA-145-5p and phosphoserine aminotransferase 1 in colon cancer. Bioengineered 13, 12794–12806, 2022.
  14. Ediriweera MK, Jayasena S. The role of reprogrammed glucose metabolism in cancer. Metabolites 13, 345, 2023.
  15. 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.
  16. Frank F, Liu X, Ortlund EA. Glucocorticoid receptor condensates link DNA-dependent receptor dimerization and transcriptional transactivation. Proc Natl Acad Sci USA 118, e2024685118, 2021.
  17. Gao S, Ge A, Xu S, You Z, Ning S, Zhao Y, Pang D. PSAT1 is regulated by ATF4 and enhances cell proliferation via the GSK3beta/beta-catenin/cyclin D1 signaling pathway in ER-negative breast cancer. J Exp Clin Cancer Res 36, 179, 2017.
  18. 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.
  19. Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol 21, 421–438, 2020.
  20. Hirko KA, Eliassen AH. Glucocorticoids and breast cancer risk. BMC Med 19, 187, 2021.
  21. Jin L, Kiang KM, Cheng SY, Leung GK. Pharmacological inhibition of serine synthesis enhances temozolomide efficacy by decreasing O(6)-methylguanine DNA methyltransferase (MGMT) expression and reactive oxygen species (ROS)-mediated DNA damage in glioblastoma. Lab Invest 102, 194–203, 2022.
  22. Kadmiel M, Cidlowski JA. Glucocorticoid receptor signaling in health and disease. Trends Pharmacol Sci 34, 518–530, 2013.
  23. Khadka S, Druffner SR, Duncan BC, Busada JT. Glucocorticoid regulation of cancer development and progression. Front Endocrinol 14, 1161768, 2023.
  24. Kurihara I, Shibata H, Suzuki T, Ando T, Kobayashi S, Hayashi M, Saito I, Saruta T. Expression and regulation of nuclear receptor coactivators in glucocorticoid action. Mol Cell Endocrinol 189, 181–189, 2002.
  25. Lebeaupin C, Yong J, Kaufman RJ. The impact of the ER unfolded protein response on cancer initiation and progression: Therapeutic implications. Adv Exp Med Biol 1243, 113–131, 2020.
  26. Lee SH, Golinska M, Griffiths JR. HIF-1-independent mechanisms regulating metabolic adaptation in hypoxic cancer cells. Cells 10, 2371, 2021.
  27. Leonardi DB, Anselmino N, Brandani JN, Jaworski FM, Paez AV, Mazaira G, Meiss RP, Nunez M, Nemirovsky SI, Giudice J, Galigniana M, Pecci A, Gueron G, Vazquez E, Cotignola J. Heme oxygenase 1 impairs glucocorticoid receptor activity in prostate cancer. Int J Mol Sci 20, 1006, 2019.
  28. Lin KT, Wang LH. New dimension of glucocorticoids in cancer treatment. Steroids 111, 84–88, 2016.
  29. Mattaini KR, Sullivan MR, Vander Heiden M.G. The importance of serine metabolism in cancer. J Cell Biol 214, 249–257, 2016.
  30. Mayayo-Peralta I, Zwart W, Prekovic S. Duality of glucocorticoid action in cancer: tumor-suppressor or oncogene? Endocr Relat Cancer 28, R157–R171, 2021.
  31. Minchenko AG, Tronjko ND. Subcellular distribution of 3H-hydrocortisone and its metabolites in the liver and kidneys of normal and alloxan diabetic rats. Endocrinol Exper 22, 19–28, 1988.
  32. 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.
  33. Minchenko A, Bauer T, Salceda S, Caro J. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab Invest 71, 374–379, 1994.
  34. 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.
  35. Minchenko OH, Ochiai A, Opentanova IL, Ogura T, Minchenko DO, Caro J, Komisarenko SV, Esumi H. Overexpression of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-4 in the human breast and colon malignant tumors. Biochimie 87, 1005–1010, 2005.
  36. 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, 2016.
  37. 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.
  38. 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.
  39. 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.
  40. Minchenko DO, Khita OO, Viletska YM, Sliusar MY, Rudnytska OV, Kozynkevych HE, Bezrodnyi BH, Khikhlo YP, Minchenko OH. Cortisol controls endoplasmic reticulum stress and hypoxia dependent regulation of insulin receptor and related genes expression in HEK293 cells. Endocr Regul 58, 1–10, 2024a.
  41. 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.
  42. Moenner M, Pluquet O, Bouchecareilh M, Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res 67, 10631–10634, 2007.
  43. Obradovic MMS, Hamelin B, Manevski N, Couto JP, Sethi A, Coissieux MM, Munst S, Okamoto R, Kohler H, Schmidt A, Bentires-Alj M. Glucocorticoids promote breast cancer metastasis. Nature 567, 540–544, 2019.
  44. Papaioannou A, Chevet E. Driving cancer tumorigenesis and metastasis through UPR signaling. Curr Top Microbiol Immunol 414, 159–192, 2018.
  45. Psarra AM, Sekeris CE. Glucocorticoids induce mitochondrial gene transcription in HepG2 cells: role of the mitochondrial glucocorticoid receptor. Biochim Biophys Acta 1813, 1814–1821, 2011.
  46. Ratman D, Vanden Berghe W, Dejager L, Libert C, Tavernier J, Beck IM, De Bosscher K. How glucocorticoid receptors modulate the activity of other transcription factors: a scope beyond tethering. Mol Cell Endocrinol 380, 41–54, 2013.
  47. 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.
  48. Sebestyen A, Kopper L, Danko T, Timar J. Hypoxia signaling in cancer: from basics to clinical practice. Pathol Oncol Res 27, 1609802, 2021.
  49. Semenza GL. A compendium of proteins that interact with HIF-1α. Exp Cell Res 356, 128–135, 2017.
  50. 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.
  51. 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.
  52. Vie N, Copois V, Bascoul-Mollevi C, Denis V, Bec N, Robert B, Fraslon C, Conseiller E, Molina F, Larroque C, Martineau P, Del Rio M, Gongora C. Overexpression of phosphoserine aminotransferase PSAT1 stimulates cell growth and increases chemoresistance of colon cancer cells. Mol Cancer 7, 14, 2008.
  53. Wang M, Zhang H, Lu Z, Su W, Tan Y, Wang J, Jia X. PSAT1 mediated EMT of colorectal cancer cells by regulating Pl3K/AKT signaling pathway. J Cancer 15, 3183–3198, 2024.
  54. Yang M, Vousden KH. Serine and one-carbon metabolism in cancer. Nat Rev Cancer 16, 650–662, 2016.
  55. Ye J, Huang X, Tian S, Wang J, Wang H, Feng H, Zhao X, Cao S, Xuan Y, Li X, Ma X, Huang Y, Zhang X. Upregulation of serine metabolism enzyme PSAT1 predicts poor prognosis and promotes proliferation, metastasis and drug resistance of clear cell renal cell carcinoma. Exp Cell Res 437, 113977, 2024.
  56. Zanchi NE, Filho MA, Felitti V, Nicastro H, Lorenzeti FM, Lancha AH Jr. Glucocorticoids: extensive physiological actions modulated through multiple mechanisms of gene regulation. J Cell Physiol 224, 311–315, 2010.
  57. Zhang X, Wang S, Li W, Wang J, Gong Y, Chen Q, Cao S, Pang D, Gao S. PSAT1 promotes metastasis via p-AKT/SP1/ITGA2 axis in estrogen receptor-negative breast cancer cell. Biomolecules 14, 990, 2024.
DOI: https://doi.org/10.2478/enr-2025-0007 | Journal eISSN: 1336-0329 | Journal ISSN: 1210-0668
Language: English
Page range: 48 - 56
Published on: Apr 21, 2025
Published by: Slovak Academy of Sciences
In partnership with: Paradigm Publishing Services
Publication frequency: 1 times per year

© 2025 Oleksandr H. Minchenko, Anastasiia I. Abramchuk, Yevgen P. Khikhlo, Myroslava Y. Sliusar, Oleh V. Halkin, Olha Y. Luzina, Serhiy V. Danilovsryi, Yuliia M. Viletska, Dmytro O. Minchenko, published by Slovak Academy of Sciences
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.