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Research Articles

Mechanisms underlying citrinin-induced toxicity via oxidative stress and apoptosis-mediated by mitochondrial-dependent pathway in SH-SY5Y cells

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Pages 944-954 | Received 02 Feb 2022, Accepted 08 Aug 2022, Published online: 06 Sep 2022

References

  • Abdel Wahab, S.I., et al., 2009. In vitro ultramorphological assessment of apoptosis induced by Zerumbone on (HeLa). Journal of Biomedicine & Biotechnology, 2009 (2009), 769568. https://doi.org/10.1155/2009/769568
  • Agarwal, R., and Kaye, S.B., 2003. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nature Reviews. Cancer, 3 (7), 502–516. https://doi.org/10.1038/nrc1123
  • Ali, A.G., et al., 2017. A novel adamantane thiadiazole derivative induces mitochondria-mediated apoptosis in lung carcinoma cell line. Bioorganic & Medicinal Chemistry, 25 (1), 241–253. https://doi.org/10.1016/j.bmc.2016.10.040
  • Alley, M.C., et al., 1988. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Research, 48 (3), 589–601.
  • Bose, D., et al., 2016. Heat killed attenuated leishmania induces apoptosis of HepG2 cells through ROS mediated p53 dependent mitochondrial pathway. Cellular Physiology and Biochemistry, 38 (4), 1303–1318. https://doi.org/10.1159/000443125
  • Bouaziz, C., et al., 2011. Molecular events involved in ochratoxin A induced mitochondrial pathway of apoptosis, modulation by Bcl-2 family members. Environmental Toxicology, 26 (6), 579–590. https://doi.org/10.1002/tox.20581
  • Bouslimi, A., et al., 2008. Cytotoxicity and oxidative damage in kidney cells exposed to the mycotoxins ochratoxin A and citrinin: Individual and combined effects. Toxicology Mechanisms and Methods, 18 (4), 341–349. https://doi.org/10.1080/15376510701556682
  • Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72 (1-2), 248–254.
  • Braunberg, R.C., et al., 1994. Interaction of citrinin and ochratoxin A. Natural Toxins, 2 (3), 124–131. https://doi.org/10.1002/nt.2620020307
  • Chagas, G.M., Campello, A.P., and Klüppel, M.L.W., 1992. Mechanism of citrinin‐induced dysfunction of mitochondria. I. Effects on respiration, enzyme activities and membrane potential of renal cortical mitochondria. Journal of Applied Toxicology : JAT, 12 (2), 123–129. https://doi.org/10.1002/jat.2550120209
  • Chagas, G.M., et al., 1994. Alterations Induced by Citrinin in Cultured Kidney Cells. Cell Structure and Function, 19 (2), 103–108. https://doi.org/10.1247/csf.19.103
  • Chan, W.H., 2007. Citrinin induces apoptosis via a mitochondria-dependent pathway and inhibition of survival signals in embryonic stem cells, and causes developmental injury in blastocysts. The Biochemical Journal, 404 (2), 317–326. https://doi.org/10.1042/BJ20061875
  • Chan, W.H., and Shiao, N.H., 2007. Effect of citrinin on mouse embryonic development in vitro and in vivo. Reproductive Toxicology (Elmsford, N.Y.), 24 (1), 120–125. https://doi.org/10.1016/j.reprotox.2007.04.070
  • Chang, C.H., et al., 2009. Activation of ERK and JNK signaling pathways by mycotoxin citrinin in human cells. Toxicology and Applied Pharmacology, 237 (3), 281–287. https://doi.org/10.1016/j.taap.2009.03.021
  • Chang, C.H., et al., 2011. Mycotoxin citrinin induced cell cycle G2/M arrest and numerical chromosomal aberration associated with disruption of microtubule formation in human cells. Toxicological Sciences, 119 (1), 84–92. https://doi.org/10.1093/toxsci/kfq309
  • Chen, C.C., and Chan, W.H., 2009. Inhibition of citrinin-induced apoptotic biochemical signaling in human hepatoma G2 cells by resveratrol. International Journal of Molecular Sciences, 10 (8), 3338–3357. https://doi.org/10.3390/ijms10083338
  • Chen, T., and Wong, Y.S., 2009. Selenocystine induces caspase-independent apoptosis in MCF-7 human breast carcinoma cells with involvement of p53 phosphorylation and reactive oxygen species generation. The International Journal of Biochemistry & Cell Biology, 41 (3), 666–676. https://doi.org/10.1016/j.biocel.2008.07.014
  • Cheng, X., et al., 2013. Gestational diabetes mellitus impairs nrf2-mediated adaptive antioxidant defenses and redox signaling in fetal endothelial cells in utero. Diabetes, 62 (12), 4088–4097. https://doi.org/10.2337/db13-0169
  • Circu, M.L., and Aw, T.Y., 2010. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radical Biology & Medicine, 48 (6), 749–762. https://doi.org/10.1016/j.freeradbiomed.2009.12.022
  • Cory, S., and Adams, J.M., 2002. The Bcl2 family: Regulators of the cellular life-or-death switch. Nature Reviews. Cancer, 2 (9), 647–656. https://doi.org/10.1038/nrc883
  • Crowley, L.C., et al., 2016. Quantitation of apoptosis and necrosis by annexin V binding, propidium iodide uptake, and flow cytometry. Cold Spring Harbor Protocols, 2016 (11), pdb.prot087288. https://doi.org/10.1101/pdb.prot087288
  • Czerwinski, M., Kiem, H.P., and Slattery, J.T., 1997. Human CD34+ cells do not express glutathione S-transferases alpha. Gene Therapy, 4 (3), 268–270. https://doi.org/10.1038/sj.gt.3300381
  • Da Lozzo, E.J., Oliveira, M.B., and Carnieri, E.G., 1998. Citrinin-induced mitochondrial permeability transition. Journal of Biochemical and Molecular Toxicology, 121., (5), 291–297. https://doi.org/10.1002/(SICI)1099-0461(1998)12:5 ≤ 291::AID-JBT5 ≥ 3.0.CO;2-G
  • David, S.S., O'Shea, V.L., and Kundu, S., 2007. Base-excision repair of oxidative DNA damage. Nature, 447 (7147), 941–950.
  • De Souza Prestes, A., et al., 2019. Methylglyoxal disturbs the expression of antioxidant, apoptotic and glycation responsive genes and triggers programmed cell death in human leukocytes. Toxicology in Vitro, 55, 33–42. https://doi.org/10.1016/j.tiv.2018.11.001
  • EFSA (European Food and Safety Authority), Panel on Contaminants in the Food Chain 2012. European Food and Safety Authority (EFSA) scientific opinion on the risk for public and animal health related to the presence of citrinin in food and feed. EFSA Journal., 10, 2605. https://doi.org/10.2903/j.efsa.2012.2605
  • EFSA (European Food and Safety Authority), Panel on Contaminants in the Food Chain 2020. European Food and Safety Authority (EFSA) scientific opinion on risk assessment of ochratoxin a in food. EFSA Journal., 18, 6113. Available from: https://doi.org/10.2903/j.efsa.2020.6113
  • El Golli Bennour, E., et al., 2009. Comparative mechanisms of zearalenone and ochratoxin a toxicities on cultured HepG2 cells: Is oxidative stress a common process? Environmental Toxicology, 24 (6), 538–548. https://doi.org/10.1002/tox.20449
  • Faraonio, R., et al., 2006. p53 suppresses the Nrf2-dependent transcription of antioxidant response genes. The Journal of Biological Chemistry, 281 (52), 39776–39784. https://doi.org/10.1074/jbc.M605707200
  • Flajs, D., and Peraica, M., 2009. Toxicological properties of citrinin. Arhiv za Higijenu Rada i Toksikologiju, 60 (4), 457–464. https://doi.org/10.2478/10004-1254-60-2009-1992
  • Föllmann, W., Behm, C., and Degen, G.H., 2014. Toxicity of the mycotoxin citrinin and its metabolite dihydrocitrinone and of mixtures of citrinin and ochratoxin A in vitro. Archives of Toxicology, 88 (5), 1097–1107. https://doi.org/10.1007/s00204-014-1216-8
  • Gao, Y., Yan, Y., and Huang, T., 2015. Human age‑related cataracts: Epigenetic suppression of the nuclear factor erythroid 2‑related factor 2‑mediated antioxidant system. Molecular Medicine Reports, 11 (2), 1442–1447.
  • Gayathri, L., et al., 2015. Hepatotoxic effect of ochratoxin A and citrinin, alone and in combination, and protective effect of vitamin E: In vitro study in HepG2 cell. Food and Chemical Toxicology, 83, 151–163.
  • Gupta, M., et al., 1979. Effects of ochratoxin A and citrinin on kidney functions. IRCS Medical Science, 7 (9), 446.
  • Gupta, M., et al., 1983. Hematological changes produced in mcie by ochratoxin A and citrinin. Toxicology, 26 (1), 55–62. https://doi.org/10.1016/0300-483X(83)90056-2
  • Gupta, S.C., et al., 2007. Induction of hsp70, alterations in oxidative stress markers and apoptosis against dichlorvos exposure in transgenic Drosophila melanogaster: Modulation by reactive oxygen species. Biochimica et Biophysica Acta, 1770 (9), 1382–1394. https://doi.org/10.1016/j.bbagen.2007.05.010
  • Hood, R.D., Hayes, A.W., and Scammell, J.G., 1976. Effects of prenatal administration of citrinin and viriditoxin to mice. Food and Cosmetics Toxicology, 14 (3), 175–178. https://doi.org/10.1016/S0015-6264(76)80419-1
  • Huang, Y.T., et al., 2009. Activation of JNK and PAK2 is essential for citrinin-induced apoptosis in a human osteoblast cell line. Environmental Toxicology, 24 (4), 343–356. https://doi.org/10.1002/tox.20434
  • IARC (International Agency for Research on Cancer) 1986. Citrinin: Some naturally occurring and synthetic food components, furocoumarins and ultraviolet radiation. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 40, 67–83.
  • IARC (International Agency for Research on Cancer) 1993. Some naturally occurring substances: heterocyclic aromatic amines and mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 56, 397–444.
  • Itoh, K., et al., 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the aminoterminal NeH2 domain. Genes & Development, 13 (1), 76–86.
  • Jeong, S.Y., et al., 2009. Apoptosis induction of human leukemia cells by Streptomycessp. SY-103 metabolites through activation of caspase-3 and inactivation of Akt. International Journal of Molecular Medicine, 25 (01), 31–40. https://doi.org/10.3892/ijmm_00000310
  • Karaman, E.F., and Ozden, S., 2019. Alterations in global DNA methylation and metabolism-related genes caused by zearalenone in MCF7 and MCF10F cells. Mycotoxin Research, 35 (3), 309–320. https://doi.org/10.1007/s12550-019-00358-8
  • Klarić, M.Š., et al., 2012. A potential role of calcium in apoptosis and aberrant chromatin forms in porcine kidney PK15 cells induced by individual and combined ochratoxin A and citrinin. Archives of Toxicology, 86 (1), 97–107. https://doi.org/10.1007/s00204-011-0735-9
  • Krejci, M.E., Bretz, N.S., and Koechel, D.A., 1996. Citrinin produces acute adverse changes in renal function and ultrastructure in pentobarbital-anesthetized dogs without concomitant reductions in [potassium]plasma. Toxicology, 106 (1-3), 167–177. https://doi.org/10.1016/0300-483X(95)03183-G
  • Kumar, R., et al., 2011. Citrinin-generated reactive oxygen species cause cell cycle arrest leading to apoptosis via the intrinsic mitochondrial pathway in mouse skin. Toxicological Sciences, 122 (2), 557–566. https://doi.org/10.1093/toxsci/kfr143
  • Lee, O.H., et al., 2007. An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. The Journal of Biological Chemistry, 282 (50), 36412–36420. https://doi.org/10.1074/jbc.M706517200
  • Liu, B.H., et al., 2003. Evaluation of genotoxic risk and oxidative DNA damage in mammalian cells exposed to mycotoxins, patulin and citrinin. Toxicology and Applied Pharmacology, 191 (3), 255–263. https://doi.org/10.1016/S0041-008X(03)00254-0
  • Lurá, M.C., et al., 2001. Actividad de metabolitos de penicillium citrinum sobre ratones mus musculus. Revista Iberoamericana de Micologia, 18 (4), 183–186.
  • Mosmann, T., 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65 (1-2), 55–63. https://doi.org/10.1016/0022-1759(83)90303-4
  • Orrenius, S., Gogvadze, V., and Zhivotovsky, B., 2007. Mitochondrial oxidative stress: Implications for cell death. Annual Review of Pharmacology and Toxicology, 47, 143–183. https://doi.org/10.1146/annurev.pharmtox.47.120505.105122
  • Qingqing, H., et al., 2012. Toxic effects of citrinin on the male reproductive system in mice. Experimental and Toxicologic Pathology, 64 (5), 465–469. https://doi.org/10.1016/j.etp.2010.10.015
  • Öztaş, E., et al., 2021. Cellular stress pathways are linked to acetamiprid-induced apoptosis in SH-SY5Y neural cells. Biology, 10 (9), 820. https://doi.org/10.3390/biology10090820
  • Rašić, D., et al., 2019. Oxidative stress as a mechanism of combined OTA and CTN toxicity in rat plasma, liver and kidney. Human & Experimental Toxicology, 38 (4), 434–445. https://doi.org/10.1177/0960327118819049
  • Ribeiro, S.M.R., et al., 1997. Mechanism of citrinin-induced dysfunction of mitochondria. V. Effect on the homeostasis of the reactive oxygen species. Cell Biochemistry and Function, 15 (3), 203–209. https://doi.org/10.1002/(SICI)1099-0844(199709)15:3 ≤ 203::AID-CBF742 ≥ 3.0.CO;2-J
  • Ricci, C., et al., 2008. Mitochondrial DNA damage triggers mitochondrial-superoxide generation and apoptosis. American Journal of Physiology. Cell Physiology, 294 (2), C413–C422. https://doi.org/10.1152/ajpcell.00362.2007
  • Rosa, S.C., et al., 2009. Impaired glucose transporter-1 degradation and increased glucose transport and oxidative stress in response to high glucose in chondrocytes from osteoarthritic versus normal human cartilage. Arthritis Research & Therapy, 11 (3), R80. https://doi.org/10.1186/ar2713
  • Salah, A., et al., 2019. Eugenol protects against citrinin-induced cytotoxicity and oxidative damages in cultured human colorectal HCT116 cells. Environmental Science and Pollution Research International, 26 (30), 31374–31383. https://doi.org/10.1007/s11356-019-06212-9
  • Salah, A., et al., 2017. Citrinin induces apoptosis in human HCT116 colon cancer cells through endoplasmic reticulum stress. Journal of Toxicology and Environmental Health. Part A, 80 (23-24), 1230–1241. https://doi.org/10.1080/15287394.2017.1359127
  • Senyildiz, M., et al., 2017. Effects of BPA on global DNA methylation and global histone 3 lysine modifications in SH-SY5Y cells: An epigenetic mechanism linking the regulation of chromatin modifiying genes. Toxicology in Vitro, 44 (2017), 313–321. https://doi.org/10.1016/j.tiv.2017.07.028
  • Sharath Babu, G.R., et al., 2017. Pelargonidin Modulates Keap1/Nrf2 Pathway Gene Expression and Ameliorates Citrinin-Induced Oxidative Stress in HepG2 Cells. Frontiers in Pharmacology, 8, 868. https://doi.org/10.3389/fphar.2017.00868
  • Singh, N.D., et al., 2007. Citrinin and endosulfan induced maternal toxicity in pregnant Wistar rats: Pathomorphological study. Journal of Applied Toxicology, 27 (6), 589–601. https://doi.org/10.1002/jat.1242
  • Singh, N., et al., 2006. Toxicity of endosulfan and citrinin alone and in combination in pregnant rats: Clinico-haematological and serum biochemical alterations. Indian Journal of Veterinary Pathology, 30 (1), 27–31.
  • Spevakova, I., et al., 2021. The protective effect of stilbenes resveratrol and pterostilbene individually and combined with mycotoxin citrinin in human adenocarcinoma HT-29 cell line in vitro. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 56 (1), 75–88. https://doi.org/10.1080/10934529.2020.1839279
  • Sun, M.H., et al., 2020. Citrinin exposure disrupts organelle distribution and functions in mouse oocytes. Environmental Research, 185 (2020), 109476. https://doi.org/10.1016/j.envres.2020.109476
  • Vanacloig-Pedros, E., Proft, M., and Pascual-Ahuir, A., 2016. Different toxicity mechanisms for citrinin and ochratoxin a revealed by transcriptomic analysis in yeast. Toxins, 8 (10), 273. https://doi.org/10.3390/toxins8100273
  • Wasternack, C., and Weisser, J., 1992. Inhibition of RNA- and DNA-synthesis by citrinin and its effects on DNA precursor-metabolism in V79-E cells. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 101 (1-2), 225–230. https://doi.org/10.1016/0305-0491(92)90183-R
  • Wu, T.S., et al., 2013. Cardiotoxicity of mycotoxin citrinin and involvement of microRNA-138 in Zebrafish embryos. Toxicological Sciences, 136 (2), 402–412. https://doi.org/10.1093/toxsci/kft206
  • Wu, Y., et al., 2017. Citrinin exposure affects oocyte maturation and embryo development by inducing oxidative stress-mediated apoptosis. Oncotarget, 8 (21), 34525–34533. https://doi.org/10.18632/oncotarget.15776
  • Wu, D., et al., 2022. Citrinin-induced hepatotoxicity in mice is regulated by the Ca2+/endoplasmic reticulum stress signaling pathway. Toxins, 14 (4), 259.https://doi.org/10.3390/toxins14040259
  • Yoneyama, M., and Sharma, R.P., 1987. Biochemical alterations induced by citrinin in cultured kidney epithelial cell systems. Archives of Environmental Contamination and Toxicology, 16 (6), 765–770. https://doi.org/10.1007/BF01055428
  • Yu, F.Y., et al., 2006. Citrinin induces apoptosis in HL-60 cells via activation of the mitochondrial pathway. Toxicology Letters, 161 (2), 143–151. https://doi.org/10.1016/j.toxlet.2005.08.009

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