tert-Butyl Hydroperoxide (tBHP)-Induced Lipid Peroxidation and Embryonic Defects Resemble Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency in C. elegans
Abstract
:1. Introduction
2. Results
2.1. Temporal Expression of gspd-1 in C. elegans
2.2. tBHP Reduced Brood Size in C. elegans
2.3. tBHP Stimulated Germ Cell Apoptosis in C. elegans
2.4. tBHP Increased Lipid Peroxidation in C. elegans
2.5. tBHP Enhanced iPLA Activity in C. elegans
3. Discussion
4. Materials and Methods
4.1. Worm Culture
4.2. gspd-1 RNAi Knockdown
4.3. Reverse Transcription and Quantitative PCR (qPCR)
4.4. tBHP Administration
4.5. Brood Size Determination
4.6. Germline Apoptosis Assay
4.7. MDA Assay
4.8. iPLA Assay
4.9. Statistical Analysis
Author Contributions
Funding
Conflicts of Interest
Abbreviations
G6PD | glucose-6-phosphate dehydrogenase |
NADPH | nicotinamide adenine dinucleotide phosphate |
tBHP | tert-butyl hydroperoxide |
MDA | malondialdehyde |
iPLA | calcium-independent phospholipase A2 |
References
- Yang, H.C.; Wu, Y.H.; Yen, W.C.; Liu, H.Y.; Hwang, T.L.; Stern, A.; Chiu, D.T. The Redox Role of G6PD in Cell Growth, Cell Death, and Cancer. Cells 2019, 8, 1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, H.C.; Cheng, M.L.; Ho, H.Y.; Chiu, D.T. The microbicidal and cytoregulatory roles of NADPH oxidases. Microbes Infect. 2011, 13, 109–120. [Google Scholar] [CrossRef] [PubMed]
- Beutler, E. G6PD deficiency. Blood 1994, 84, 3613–3636. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Longo, L.; Vanegas, O.C.; Patel, M.; Rosti, V.; Li, H.; Waka, J.; Merghoub, T.; Pandolfi, P.P.; Notaro, R.; Manova, K.; et al. Maternally transmitted severe glucose 6-phosphate dehydrogenase deficiency is an embryonic lethal. EMBO J. 2002, 21, 4229–4239. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, H.C.; Chen, T.L.; Wu, Y.H.; Cheng, K.P.; Lin, Y.H.; Cheng, M.L.; Ho, H.Y.; Lo, S.J.; Chiu, D.T. Glucose 6-phosphate dehydrogenase deficiency enhances germ cell apoptosis and causes defective embryogenesis in Caenorhabditis elegans. Cell Death Dis. 2013, 4, e616. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, T.L.; Yang, H.C.; Hung, C.Y.; Ou, M.H.; Pan, Y.Y.; Cheng, M.L.; Stern, A.; Lo, S.J.; Chiu, D.T. Impaired embryonic development in glucose-6-phosphate dehydrogenase-deficient Caenorhabditis elegans due to abnormal redox homeostasis induced activation of calcium-independent phospholipase and alteration of glycerophospholipid metabolism. Cell Death Dis. 2017, 8, e2545. [Google Scholar] [CrossRef] [PubMed]
- Ayyadevara, S.; Engle, M.R.; Singh, S.P.; Dandapat, A.; Lichti, C.F.; Benes, H.; Shmookler Reis, R.J.; Liebau, E.; Zimniak, P. Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4-hydroxynonenal. Aging Cell 2005, 4, 257–271. [Google Scholar] [CrossRef] [PubMed]
- Sakamoto, T.; Maebayashi, K.; Tsunoda, Y.; Imai, H. Inhibition of lipid peroxidation during the reproductive period extends the lifespan of Caenorhabditis elegans. J. Clin. Biochem. Nutr. 2020, 66, 116–123. [Google Scholar] [CrossRef] [Green Version]
- Singh, S.P.; Niemczyk, M.; Zimniak, L.; Zimniak, P. Fat accumulation in Caenorhabditis elegans triggered by the electrophilic lipid peroxidation product 4-hydroxynonenal (4-HNE). Aging (Albany N. Y.) 2008, 1, 68–80. [Google Scholar] [CrossRef]
- Rush, G.F.; Gorski, J.R.; Ripple, M.G.; Sowinski, J.; Bugelski, P.; Hewitt, W.R. Organic hydroperoxide-induced lipid peroxidation and cell death in isolated hepatocytes. Toxicol. Appl. Pharmacol. 1985, 78, 473–483. [Google Scholar] [CrossRef]
- Ayala, A.; Munoz, M.F.; Arguelles, S. Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell Longev. 2014, 2014, 360438. [Google Scholar] [CrossRef] [PubMed]
- Hix, S.; Kadiiska, M.B.; Mason, R.P.; Augusto, O. In vivo metabolism of tert-butyl hydroperoxide to methyl radicals. EPR spin-trapping and DNA methylation studies. Chem. Res. Toxicol. 2000, 13, 1056–1064. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Z.; Hartwieg, E.; Horvitz, H.R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 2001, 104, 43–56. [Google Scholar] [CrossRef] [Green Version]
- Yang, H.C.; Wu, Y.H.; Liu, H.Y.; Stern, A.; Chiu, D.T. What has passed is prolog: New cellular and physiological roles of G6PD. Free Radic. Res. 2016, 50, 1047–1064. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.C.; Yu, H.; Liu, Y.C.; Chen, T.L.; Stern, A.; Lo, S.J.; Chiu, D.T. IDH-1 deficiency induces growth defects and metabolic alterations in GSPD-1-deficient Caenorhabditis elegans. J. Mol. Med. (Berl.) 2019, 97, 385–396. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davies, M.J. Detection of peroxyl and alkoxyl radicals produced by reaction of hydroperoxides with rat liver microsomal fractions. Biochem. J. 1989, 257, 603–606. [Google Scholar] [CrossRef] [Green Version]
- Crane, D.; Haussinger, D.; Graf, P.; Sies, H. Decreased flux through pyruvate dehydrogenase by thiol oxidation during t-butyl hydroperoxide metabolism in perfused rat liver. Hoppe Seylers Z. Physiol. Chem. 1983, 364, 977–987. [Google Scholar] [CrossRef]
- Bozzi, A.; Parisi, M.; Strom, R. Erythrocyte glutathione determination in the diagnosis of glucose-6-phosphate dehydrogenase deficiency. Biochem. Mol. Biol. Int. 1996, 40, 561–569. [Google Scholar] [CrossRef]
- Trotta, R.J.; Sullivan, S.G.; Stern, A. Lipid peroxidation and haemoglobin degradation in red blood cells exposed to t-butyl hydroperoxide. The relative roles of haem- and glutathione-dependent decomposition of t-butyl hydroperoxide and membrane lipid hydroperoxides in lipid peroxidation and haemolysis. Biochem. J. 1983, 212, 759–772. [Google Scholar] [CrossRef] [Green Version]
- Trotta, R.J.; Sullivan, S.G.; Stern, A. Lipid peroxidation and haemoglobin degradation in red blood cells exposed to t-butyl hydroperoxide. Effects of the hexose monophosphate shunt as mediated by glutathione and ascorbate. Biochem. J. 1982, 204, 405–415. [Google Scholar] [CrossRef] [Green Version]
- Chaves, M.A.; Leonart, M.S.; do Nascimento, A.J. Oxidative process in erythrocytes of individuals with hemoglobin S. Hematology 2008, 13, 187–192. [Google Scholar] [CrossRef] [PubMed]
- Ewald, C.Y.; Hourihan, J.M.; Blackwell, T.K. Oxidative Stress Assays (arsenite and tBHP) in Caenorhabditis elegans. Bio Protoc. 2017, 7. [Google Scholar] [CrossRef] [PubMed]
- Brault, D.; Neta, P.; Patterson, L.K. The lipid peroxidation model for halogenated hydrocarbon toxicity. Kinetics of peroxyl radical processes involving fatty acids and Fe(III) porphyrins. Chem. Biol. Interact. 1985, 54, 289–297. [Google Scholar] [CrossRef]
- Kucera, O.; Endlicher, R.; Rousar, T.; Lotkova, H.; Garnol, T.; Drahota, Z.; Cervinkova, Z. The effect of tert-butyl hydroperoxide-induced oxidative stress on lean and steatotic rat hepatocytes in vitro. Oxid. Med. Cell. Longev. 2014, 2014, 752506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peterson, B.; Stovall, K.; Monian, P.; Franklin, J.L.; Cummings, B.S. Alterations in phospholipid and fatty acid lipid profiles in primary neocortical cells during oxidant-induced cell injury. Chem. Biol. Interact. 2008, 174, 163–176. [Google Scholar] [CrossRef]
- Peterson, B.; Knotts, T.; Cummings, B.S. Involvement of Ca2+-independent phospholipase A2 isoforms in oxidant-induced neural cell death. Neurotoxicology 2007, 28, 150–160. [Google Scholar] [CrossRef] [PubMed]
- Martin, C.; Martinez, R.; Navarro, R.; Ruiz-Sanz, J.I.; Lacort, M.; Ruiz-Larrea, M.B. tert-Butyl hydroperoxide-induced lipid signaling in hepatocytes: Involvement of glutathione and free radicals. Biochem. Pharmacol. 2001, 62, 705–712. [Google Scholar] [CrossRef]
- McLean, L.R.; Hagaman, K.A.; Davidson, W.S. Role of lipid structure in the activation of phospholipase A2 by peroxidized phospholipids. Lipids 1993, 28, 505–509. [Google Scholar] [CrossRef]
- Erol, B.; Bozlu, M.; Hanci, V.; Tokgoz, H.; Bektas, S.; Mungan, G. Coenzyme Q10 treatment reduces lipid peroxidation, inducible and endothelial nitric oxide synthases, and germ cell-specific apoptosis in a rat model of testicular ischemia/reperfusion injury. Fertil. Steril. 2010, 93, 280–282. [Google Scholar] [CrossRef]
- Li, Y.; Wu, Y.; Jiang, K.; Han, W.; Zhang, J.; Xie, L.; Liu, Y.; Xiao, J.; Wang, X. Mangiferin Prevents TBHP-Induced Apoptosis and ECM Degradation in Mouse Osteoarthritic Chondrocytes via Restoring Autophagy and Ameliorates Murine Osteoarthritis. Oxid. Med. Cell. Longev. 2019, 2019, 8783197. [Google Scholar] [CrossRef]
- Loch-Caruso, R.; Korte, C.S.; Hogan, K.A.; Liao, S.; Harris, C. Tert-Butyl Hydroperoxide Stimulated Apoptosis Independent of Prostaglandin E2 and IL-6 in the HTR-8/SVneo Human Placental Cell Line. Reprod. Sci. 2020. [Google Scholar] [CrossRef] [PubMed]
- Lucarelli, G.; Galleggiante, V.; Rutigliano, M.; Sanguedolce, F.; Cagiano, S.; Bufo, P.; Lastilla, G.; Maiorano, E.; Ribatti, D.; Giglio, A.; et al. Metabolomic profile of glycolysis and the pentose phosphate pathway identifies the central role of glucose-6-phosphate dehydrogenase in clear cell-renal cell carcinoma. Oncotarget 2015, 6, 13371–13386. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saha, S.; Mahalanobish, S.; Dutta, S.; Sil, P.C. Mangiferin ameliorates collateral neuropathy in tBHP induced apoptotic nephropathy by inflammation mediated kidney to brain crosstalk. Food Funct. 2019, 10, 5981–5999. [Google Scholar] [CrossRef] [PubMed]
- Tang, Q.; Zheng, G.; Feng, Z.; Chen, Y.; Lou, Y.; Wang, C.; Zhang, X.; Zhang, Y.; Xu, H.; Shang, P.; et al. Trehalose ameliorates oxidative stress-mediated mitochondrial dysfunction and ER stress via selective autophagy stimulation and autophagic flux restoration in osteoarthritis development. Cell Death Dis. 2017, 8, e3081. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, S.; Wang, W.; Chen, X.; Deng, Y. Sesamin promotes angiogenesis and accelerates wound healing in rats via alleviates TBHP-induced apoptosis in human umbilical vein endothelial cells. Biosci. Biotechnol. Biochem. 2020, 84, 887–897. [Google Scholar] [CrossRef] [PubMed]
- Zhao, C.; Li, T.; Han, B.; Yue, W.; Shi, L.; Wang, H.; Guo, Y.; Lu, Z. DDAH1 deficiency promotes intracellular oxidative stress and cell apoptosis via a miR-21-dependent pathway in mouse embryonic fibroblasts. Free Radic. Biol. Med. 2016, 92, 50–60. [Google Scholar] [CrossRef]
- Zheng, G.; Zhan, Y.; Li, X.; Pan, Z.; Zheng, F.; Zhang, Z.; Zhou, Y.; Wu, Y.; Wang, X.; Gao, W.; et al. TFEB, a potential therapeutic target for osteoarthritis via autophagy regulation. Cell Death Dis. 2018, 9, 858. [Google Scholar] [CrossRef] [Green Version]
- Girard, L.R.; Fiedler, T.J.; Harris, T.W.; Carvalho, F.; Antoshechkin, I.; Han, M.; Sternberg, P.W.; Stein, L.D.; Chalfie, M. WormBook: The online review of Caenorhabditis elegans biology. Nucleic Acids Res. 2007, 35, D472–D475. [Google Scholar] [CrossRef]
- Kamath, R.S.; Fraser, A.G.; Dong, Y.; Poulin, G.; Durbin, R.; Gotta, M.; Kanapin, A.; Le Bot, N.; Moreno, S.; Sohrmann, M.; et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421, 231–237. [Google Scholar] [CrossRef]
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Yang, H.-C.; Yu, H.; Ma, T.-H.; Tjong, W.-Y.; Stern, A.; Chiu, D.T.-Y. tert-Butyl Hydroperoxide (tBHP)-Induced Lipid Peroxidation and Embryonic Defects Resemble Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency in C. elegans. Int. J. Mol. Sci. 2020, 21, 8688. https://doi.org/10.3390/ijms21228688
Yang H-C, Yu H, Ma T-H, Tjong W-Y, Stern A, Chiu DT-Y. tert-Butyl Hydroperoxide (tBHP)-Induced Lipid Peroxidation and Embryonic Defects Resemble Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency in C. elegans. International Journal of Molecular Sciences. 2020; 21(22):8688. https://doi.org/10.3390/ijms21228688
Chicago/Turabian StyleYang, Hung-Chi, Hsiang Yu, Tian-Hsiang Ma, Wen-Ye Tjong, Arnold Stern, and Daniel Tsun-Yee Chiu. 2020. "tert-Butyl Hydroperoxide (tBHP)-Induced Lipid Peroxidation and Embryonic Defects Resemble Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency in C. elegans" International Journal of Molecular Sciences 21, no. 22: 8688. https://doi.org/10.3390/ijms21228688