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Original Articles

Valproic acid promotes SOD2 acetylation: a potential mechanism of valproic acid-induced oxidative stress in developing systems

, , , , , , , & show all
Pages 1130-1144 | Received 08 Jul 2021, Accepted 08 Dec 2021, Published online: 19 Jan 2022

References

  • Rahman M, Nguyen H. 2021. Valproic Acid. StatPearls. Treasure Island (FL).
  • Koren G, Nava-Ocampo AA, Moretti ME, et al. Major malformations with valproic acid. Can Fam Physician. 2006;52:441–442.
  • Vinten J, Adab N, Kini U, et al. Neuropsychological effects of exposure to anticonvulsant medication in utero. Neurology. 2005;64(6):949–954.
  • Gaily E, Kantola-Sorsa E, Hiilesmaa V, et al. Normal intelligence in children with prenatal exposure to carbamazepine. Neurology. 2004;62(1):28–32.
  • Eikel D, Lampen A, Nau H. Teratogenic effects mediated by inhibition of histone deacetylases: evidence from quantitative structure activity relationships of 20 valproic acid derivatives. Chem Res Toxicol. 2006;19(2):272–278.
  • Wilffert B, Altena J, Tijink L, et al. Pharmacogenetics of drug-induced birth defects: what is known so far? Pharmacogenomics. 2011;12(4):547–558.
  • Vajda FJ, O'Brien TJ, Lander CM, et al. Teratogenesis in repeated pregnancies in antiepileptic drug-treated women. Epilepsia. 2013;54(1):181–186.
  • Ornoy A. Valproic acid in pregnancy: how much are we endangering the embryo and fetus? Reprod Toxicol. 2009;28(1):1–10.
  • Jones DP. Extracellular redox state: refining the definition of oxidative stress in aging. Rejuvenation Res. 2006;9(2):169–181.
  • Hansen JM, Jones DP, Harris C. The redox theory of development. Antioxid Redox Signal. 2020;32(10):715–740.
  • Kwak MK, Wakabayashi N, Itoh K, et al. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J Biol Chem. 2003;278(10):8135–8145.
  • Kobayashi M, Li L, Iwamoto N, et al. The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol Cell Biol. 2009;29(2):493–502.
  • Harris C, Hansen JM. Nrf2-mediated resistance to oxidant-induced redox disruption in embryos. Birth Defects Res B Dev Reprod Toxicol. 2012;95(3):213–218.
  • Salimi A, Alyan N, Akbari N, et al. Selenium and L-carnitine protects from valproic acid-induced oxidative stress and mitochondrial damages in rat cortical neurons. Drug Chem Toxicol. 2020;4:1–8.
  • Hussein AM, Awadalla A, Abbas KM, et al. Chronic valproic acid administration enhances oxidative stress, upregulates IL6 and downregulates Nrf2, Glut1 and Glut4 in rat's liver and brain. Neuroreport. 2021;32(10):840–850.
  • Salsaa M, Pereira B, Liu J, et al. Valproate inhibits mitochondrial bioenergetics and increases glycolysis in Saccharomyces cerevisiae. Sci Rep. 2020;10(1):11785.
  • Tung EW, Winn LM. Valproic acid increases formation of reactive oxygen species and induces apoptosis in postimplantation embryos: a role for oxidative stress in valproic acid-induced neural tube defects. Mol Pharmacol. 2011;80(6):979–987.
  • Chen Y, Zhang J, Lin Y, et al. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 2011;12(6):534–541.
  • He C, Danes JM, Hart PC, et al. SOD2 acetylation on lysine 68 promotes stem cell reprogramming in breast cancer. Proc Natl Acad Sci USA. 2019;116(47):23534–23541.
  • Gottlicher M, Minucci S, Zhu P, et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. Embo J. 2001;20(24):6969–6978.
  • Leszczynski P, Smiech M, Teeli AS, et al. Neurogenesis using P19 embryonal carcinoma cells. J Vis Exp. 2019;24(146).
  • Marikawa Y, Tamashiro DA, Fujita TC, et al. Dual roles of Oct4 in the maintenance of mouse P19 embryonal carcinoma cells: as negative regulator of wnt/beta-catenin signaling and competence provider for brachyury induction. Stem Cells Dev. 2011;20(4):621–633.
  • McBurney MW. P19 embryonal carcinoma cells. Int J Dev Biol. 1993;37(1):135–140.
  • Sargent CY, Berguig GY, McDevitt TC. Cardiomyogenic differentiation of embryoid bodies is promoted by rotary orbital suspension culture. Tissue Eng Part A. 2009;15(2):331–342.
  • Harris C. Rodent whole embryo culture. Methods Mol Biol. 2012;889:215–237.
  • Gnaiger E. Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. Int J Biochem Cell Biol. 2009;41(10):1837–1845.
  • Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol. 2002;348:93–112.
  • Hansen JM, Harris C. Glutathione during embryonic development. Biochim Biophys Acta. 2015;1850(8):1527–1542.
  • Kirlin WG, Cai J, Thompson SA, et al. Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic Biol Med. 1999;27(11-12):1208–1218.
  • Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552(Pt 2):335–344.
  • Hansen JM. Oxidative stress as a mechanism of teratogenesis. Birth Defect Res C. 2006;78(4):293–307.
  • Hansen JM, Harris C. Redox control of teratogenesis. Reprod Toxicol. 2013;35:165–179.
  • Mohammed MA, Gharib DM, Reyad HR, et al. Antioxidant and anti-inflammatory properties of alpha-lipoic acid protect against valproic acid-induced liver injury. Can J Physiol Pharmacol. 2021;99(5):499–505.
  • Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, et al. Mitochondria and reactive oxygen species. Free Radic Biol Med. 2009;47(4):333–343.
  • Li Y, Huang TT, Carlson EJ, et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11(4):376–381.
  • Lebovitz RM, Zhang H, Vogel H, et al. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA. 1996;93(18):9782–9787.
  • Koroglu OF, Gunata M, Vardi N, et al. Protective effects of naringin on valproic acid-induced hepatotoxicity in rats. Tissue Cell. 2021;72:101526.
  • Al-Amin MM, Rahman MM, Khan FR, et al. Astaxanthin improves behavioral disorder and oxidative stress in prenatal valproic acid-induced mice model of autism. Behav Brain Res. 2015;286:112–121.
  • Varum S, Rodrigues AS, Moura MB, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One. 2011;6(6):e20914.
  • Folmes CD, Nelson TJ, Martinez-Fernandez A, et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab. 2011;14(2):264–271.
  • Kelly GM, Gatie MI. Mechanisms regulating stemness and differentiation in embryonal carcinoma cells. Stem Cells Int. 2017;2017:1–20.
  • Imhoff BR, Hansen JM. Differential redox potential profiles during adipogenesis and osteogenesis. Cell Mol Biol Lett. 2011;16(1):149–161.
  • Yanes O, Clark J, Wong DM, et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat Chem Biol. 2010;6(6):411–417.
  • Ansenberger-Fricano K, Ganini D, Mao M, et al. The peroxidase activity of mitochondrial superoxide dismutase. Free Radic Biol Med. 2013;54:116–124.
  • Zhu Y, Zou X, Dean AE, et al. Lysine 68 acetylation directs MnSOD as a tetrameric detoxification complex versus a monomeric tumor promoter. Nat Commun. 2019;10(1):2399.
  • Gao J, Feng Z, Wang X, et al. SIRT3/SOD2 maintains osteoblast differentiation and bone formation by regulating mitochondrial stress. Cell Death Differ. 2018;25(2):229–240.
  • Simon G, Moog C, Obert G. Valproic acid reduces the intracellular level of glutathione and stimulates human immunodeficiency virus. Chem Biol Interact. 1994;91(2-3):111–121.
  • Jurima-Romet M, Abbott FS, Tang W, et al. Cytotoxicity of unsaturated metabolites of valproic acid and protection by vitamins C and E in glutathione-depleted rat hepatocytes. Toxicology. 1996;112(1):69–85.
  • Kiang TK, Teng XW, Surendradoss J, et al. Glutathione depletion by valproic acid in sandwich-cultured rat hepatocytes: Role of biotransformation and temporal relationship with onset of toxicity. Toxicol Appl Pharmacol. 2011;252(3):318–324.
  • Oztay F, Tunali S, Kayalar O, et al. The protective effect of vitamin U on valproic acid-induced lung toxicity in rats via amelioration of oxidative stress. J Biochem Mol Toxicol. 2020;34(12):e22602.
  • Mathers J, Fraser JA, McMahon M, et al. Antioxidant and cytoprotective responses to redox stress. Biochem Soc Symp. 2004;71:157–176.
  • Palsamy P, Bidasee KR, Shinohara T. Valproic acid suppresses Nrf2/Keap1 dependent antioxidant protection through induction of endoplasmic reticulum stress and Keap1 promoter DNA demethylation in human lens epithelial cells. Exp Eye Res. 2014;121:26–34.
  • Yu JI, Choi C, Shin SW, et al. Valproic acid sensitizes hepatocellular carcinoma cells to proton therapy by suppressing NRF2 activation. Sci Rep. 2017;7(1):14986.
  • Qiu X, Brown K, Hirschey MD, et al. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 2010;12(6):662–667.
  • Wang S, Zhang C, Niyazi S, et al. A novel cytoprotective peptide protects mesenchymal stem cells against mitochondrial dysfunction and apoptosis induced by starvation via Nrf2/Sirt3/FoxO3a pathway. J Transl Med. 2017;15(1):33.
  • Oh JY, Choi GE, Lee HJ, et al. 17beta-Estradiol protects mesenchymal stem cells against high glucose-induced mitochondrial oxidants production via Nrf2/Sirt3/MnSOD signaling. Free Radic Biol Med. 2019;130:328–342.
  • Zhou Q, Wang X, Shao X, et al. tert-Butylhydroquinone treatment alleviates Contrast-Induced nephropathy in rats by activating the Nrf2/Sirt3/SOD2 signaling pathway. Oxid Med Cell Longev. 2019;2019:4657651.
  • Locatelli M, Zoja C, Zanchi C, et al. Manipulating sirtuin 3 pathway ameliorates renal damage in experimental diabetes. Sci Rep. 2020;10(1):8418.
  • Abdel Khalek W, Cortade F, Ollendorff V, et al. SIRT3, a mitochondrial NAD+-dependent deacetylase, is involved in the regulation of myoblast differentiation. PLoS One. 2014;9(12):e114388.
  • Hsu YC, Wu YT, Yu TH, et al. Mitochondria in mesenchymal stem cell biology and cell therapy: from cellular differentiation to mitochondrial transfer. Semin Cell Dev Biol. 2016;52:119–131.
  • Ding Y, Yang H, Wang Y, et al. Sirtuin 3 is required for osteogenic differentiation through maintenance of PGC-1ɑ-SOD2-mediated regulation of mitochondrial function. Int J Biol Sci. 2017;13(2):254–264.
  • Hsu YC, Wu YT, Tsai CL, et al. Current understanding and future perspectives of the roles of sirtuins in the reprogramming and differentiation of pluripotent stem cells. Exp Biol Med (Maywood)). 2018;243(6):563–575.

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