Sulforaphane alleviates methamphetamine-induced oxidative damage and apoptosis via the Nrf2-mediated pathway in vitro and in vivo

References

• Ares, A. M., Valverde, S., Bernal, J. L., Nozal, M. J., & Bernal, J. (2015). Development and validation of a LC-MS/MS method to determine sulforaphane in honey. Food Chemistry, 181, 263–269. https://doi.org/10.1016/j.foodchem.2015.02.085
   PubMed Web of Science ®Google Scholar
• Bakir, S., Catalkaya, G. F., Ceylan, D., Khan, H., Guldiken, B., Capanoglu, E., & Kamal, M. A. (2020). Role of dietary antioxidants in neurodegenerative diseases: Where are we standing? Current Pharmaceutical Design, 26(7), 714–729. https://doi.org/10.2174/1381612826666200107143619
   PubMed Web of Science ®Google Scholar
• Banerjee, S., Aykin-Burns, N., Krager, K. J., Shah, S. K., Melnyk, S. B., Hauer-Jensen, M., & Pawar, S. A. (2016). Loss of C/EBPdelta enhances IR-induced cell death by promoting oxidative stress and mitochondrial dysfunction. Free Radical Biology & Medicine, 99, 296–307. https://doi.org/10.1016/j.freeradbiomed.2016.08.022
   PubMed Web of Science ®Google Scholar
• Borgmann, K., & Ghorpade, A. (2018). Methamphetamine augments concurrent astrocyte mitochondrial stress, oxidative burden, and antioxidant capacity: Tipping the balance in HIV-associated neurodegeneration. Neurotoxicity Research, 33(2), 433–447. https://doi.org/10.1007/s12640-017-9812-z
   PubMed Web of Science ®Google Scholar
• Brant, L. Y. D., Desta, H., Khoo, T. C., Sharikova, A. V., Mahajan, S. D., & Khmaladze, A. (2019). Methamphetamine-induced apoptosis in glial cells examined under marker-free imaging modalities. Journal of Biomedical Optics, 24, 1–10. https://doi.org/10.1117/1.JBO.24.4.046503
   PubMed Web of Science ®Google Scholar
• Chan, T. K., Loh, X. Y., Peh, H. Y., Tan, W. N. F., Tan, W. S. D., Li, N., Tay, I. J. J., Wong, W. S. F., & Engelward, B. P. (2016). House dust mite-induced asthma causes oxidative damage and DNA double-strand breaks in the lungs. The Journal of Allergy and Clinical Immunology, 138(1), 84–96.e1. https://doi.org/10.1016/j.jaci.2016.02.017
   PubMed Web of Science ®Google Scholar
• Chen, H., Wu, J., Zhang, J., Fujita, Y., Ishima, T., Iyo, M., & Hashimoto, K. (2012). Protective effects of the antioxidant sulforaphane on behavioral changes and neurotoxicity in mice after the administration of methamphetamine. Psychopharmacology, 222(1), 37–45. https://doi.org/10.1007/s00213-011-2619-3
   PubMed Web of Science ®Google Scholar
• Choi, S. J., & Kim, H. S. (2018). Deregulation of Nrf2/ARE signaling pathway causes susceptibility of dystrophin-deficient myotubes to menadione-induced oxidative stress. Experimental Cell Research, 364(2), 224–233. https://doi.org/10.1016/j.yexcr.2018.02.013
   PubMed Web of Science ®Google Scholar
• Faghiri, Z., & Bazan, N. G. (2010). PI3K/Akt and mTOR/p70S6K pathways mediate neuroprotectin D1-induced retinal pigment epithelial cell survival during oxidative stress-induced apoptosis. Experimental Eye Research, 90(6), 718–725. https://doi.org/10.1016/j.exer.2010.03.002
   PubMed Web of Science ®Google Scholar
• Feng, S., Xu, Z. F., Wang, F., Yang, T., Liu, W., Deng, Y., & Xu, B.(2017). Sulforaphane prevents methylmercury-induced oxidative damage and excitotoxicity through activation of the Nrf2-ARE pathway. Molecular Neurobiology, 54(1), 375–391. https://doi.org/10.1007/s12035-015-9643-y
   PubMed Web of Science ®Google Scholar
• Gao, Y., Chu, S. F., Zhang, Z., Ai, Q. D., Xia, C. Y., Huang, H. Y., & Chen, N. H. (2019). Ginsenoside Rg1 prevents Acetaminophen-induced oxidative stress and apoptosis via Nrf2/ARE signaling pathway. Journal of Asian Natural Products Research, 21(8), 782–797. https://doi.org/10.1080/10286020.2018.1504024
   PubMed Web of Science ®Google Scholar
• Gu, Y. H., Wang, Y., Bai, Y., Liu, M., & Wang, H. L. (2017). Endoplasmic reticulum stress and apoptosis via PERK-eIF2alpha-CHOP signaling in the methamphetamine-induced chronic pulmonary injury. Environmental Toxicology and Pharmacology, 49, 194–201. https://doi.org/10.1016/j.etap.2017.01.003
   PubMed Web of Science ®Google Scholar
• Han, C., Wei, Y. Y., Wang, X., Cui, Y. Q., Bao, Y. Z., & Shi, W. Y. (2019). Salvia miltiorrhiza polysaccharides protect against lipopolysaccharide-induced liver injury by regulating NF-κb and Nrf2 pathway in mice. Food and Agricultural Immunology, 30(1), 979–994. https://doi.org/10.1080/09540105.2019.1652250
   Web of Science ®Google Scholar
• Jang, J., & Cho, I. H. (2016). Sulforaphane ameliorates 3-nitropropionic acid-induced striatal toxicity by activating the Keap1-Nrf2-ARE pathway and inhibiting the MAPKs and NF-κB pathway. Molecular Neurobiology, 53(4), 2619–2635. https://doi.org/10.1007/s12035-015-9230-2
   PubMed Web of Science ®Google Scholar
• Jeong, J. Y., Cha, H. J., Choi, E. O., Kim, C. H., Kim, G. Y., Yoo, Y. H., Hwang, H. J., Park, H. T., Yoon, H. M., & Choi, Y. H. (2019). Activation of the Nrf2/HO-1 signaling pathway contributes to the protective effects of baicalein against oxidative stress-induced DNA damage and apoptosis in HEI193 Schwann cells. International Journal of Medical Sciences, 16(1), 145–155. https://doi.org/10.7150/ijms.27005
   PubMed Web of Science ®Google Scholar
• Jiao, Z., Chang, J., Li, J., Nie, D., Cui, H., & Guo, D. (2017). Sulforaphane increases Nrf2 expression and protects alveolar epithelial cells against injury caused by cigarette smoke extract. Molecular Medicine Reports, 16(2), 1241–1247. https://doi.org/10.3892/mmr.2017.6700
   PubMed Web of Science ®Google Scholar
• Johnson, Z., Venters, J., Guarraci, F. A., & Zewail-Foote, M. (2015). Methamphetamine induces DNA damage in specific regions of the female rat brain. Clinical and Experimental Pharmacology & Physiology, 42(6), 570–575. https://doi.org/10.1111/1440-1681.12404
   PubMed Web of Science ®Google Scholar
• Jumnongprakhon, P., Govitrapong, P., Tocharus, C., Pinkaew, D., & Tocharus, J. (2015). Melatonin protects methamphetamine-induced neuroinflammation through NF-κB and Nrf2 pathways in glioma cell line. Neurochemical Research, 40(7), 1448–1456. https://doi.org/10.1007/s11064-015-1613-2
   PubMed Web of Science ®Google Scholar
• Kang, Y., Lee, J. H., Seo, Y. H., Jang, J. H., Jeong, C. H., Lee, S. Y., Jeong, G. S., & Park, B. (2019). Epicatechin prevents methamphetamine-induced neuronal cell death via inhibition of ER stress. Biomolecules & Therapeutics, 27(2), 145–151. https://doi.org/10.4062/biomolther.2018.092
   PubMed Web of Science ®Google Scholar
• Kim, N. Y., Ahn, S. G., & Kin, S. A. (2017). Cinnamaldehyde protects human dental pulp cells against oxidative stress through the Nrf2/HO-1-dependent antioxidant response. European Journal of Pharmacology, 815, 73–79. https://doi.org/10.1016/j.ejphar.2017.09.004
   PubMed Web of Science ®Google Scholar
• Kim, J., & Keum, Y. S. (2016). NRF2, a key regulator of antioxidants with two faces towards cancer. Oxidative Medicine and Cellular Longevity, 2746457. https://doi.org/10.1155/2016/2746457
   PubMed Web of Science ®Google Scholar
• Li, B., Chen, R., Chen, L., Qiu, P. M., Ai, X. Y., Huang, E. P., Huang, W. Y., Chen, C. X., Liu, C., Lin, Z. M., Xie, W. B., & Wang, H. J. (2017). Effects of DDIT4 in methamphetamine-induced autophagy and apoptosis in dopaminergic neurons. Molecular Neurobiology, 54(3), 1642–1660. https://doi.org/10.1007/s12035-015-9637-9
   PubMed Web of Science ®Google Scholar
• Lord, K. C., Shenouda, S. K., McIlwain, E., Charalampidis, D. P., Lucchesi, A., & Varner, K. J. (2010). Oxidative stress contributes to methamphetamine-induced left ventricular dysfunction. Cardiovascular Research, 87(1), 111–118. https://doi.org/10.1093/cvr/cvq043
   PubMed Web of Science ®Google Scholar
• Menegon, S., Columbano, A., & Giordano, S. (2016). The dual roles of NRF2 in cancer. Trends in Molecular Medicine, 22(7), 578–593. https://doi.org/10.1016/j.molmed.2016.05.002
   PubMed Web of Science ®Google Scholar
• Meo, S. D., Reed, T. T., Venditti, P., & Victor, V. M. (2016). Role of ROS and RNS sources in physiological and pathological conditions. Oxidative Medicine and Cellular Longevity, 2016, 1245049. https://doi.org/10.1155/2016/1245049
   PubMed Web of Science ®Google Scholar
• Murray, J., Barbara, J. A., Dunkley, S. A., Lopez, A. F., Van Ostade, X., Condliffe, A. M., Dransfield, I., Haslett, C., & Chilvers, E. R. (1997). Regulation of neutrophil apoptosis by tumor necrosis factor-alpha: Requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood, 90(7), 2772–2783. https://doi.org/10.1182/blood.V90.7.2772
   PubMed Web of Science ®Google Scholar
• Noh, J. R., Kim, Y. H., Huwang, J. H., Choi, D. H., Kim, K. S., Oh, W. K., & Lee, C. H. (2015). Sulforaphane protects against Acetaminophen-induced hepatotoxicity. Food and Chemical Toxicology, 80, 193–200. https://doi.org/10.1016/j.fct.2015.03.020
   PubMed Web of Science ®Google Scholar
• Nordahl, T. E., Salo, R., & Leamon, M. (2003). Neuropsychological effects of chronicmethamphetamine use on neurotransmitters and cognition: A review. The Journal of Neuropsychiatry and Clinical Neurosciences, 15(3), 317–325. https://doi.org/10.1176/jnp.15.3.317
   PubMed Web of Science ®Google Scholar
• Okonkwo, A., Mitra, J., Johnson, G. S., Li, L., Dashwood, W. M., Hegde, M. L., Yue, C., Dashwood, R. H., & Rajendran, P. (2018). Heterocyclic analogs of sulforaphane trigger DNA damage and impede DNA repair in colon cancer cells: Interplay of HATs and HDACs. Molecular Nutrition & Food Research, 62(18), e1800228. https://doi.org/10.1002/mnfr.201800228
   PubMed Web of Science ®Google Scholar
• Pamies, D., Block, K., Lau, P., Gribaldo, L., Pardo, C. A., Barreras, P., Smirnova, L., Wiersma, D., Zhao, L., Harris, G., Hartung, T., & Hogberg, H. T. (2018). Rotenone exerts developmental neurotoxicity in a human brain spheroid model. Toxicology and Applied Pharmacology, 354, 101–114. https://doi.org/10.1016/j.taap.2018.02.003
   PubMed Web of Science ®Google Scholar
• Potula, R., Hawkins, B. J., Cenna, J. M., Fan, S., Dykstra, H. S., Ramirez, H. B., Morsey, B., Brodie, M. R., & Persidsky, Y. (2010). Methamphetamine causes mitrochondrial oxidative damage in human T lymphocytes leading to functional impairment. Journal of Immunology, 185(5), 2867–2876. https://doi.org/10.4049/jimmunol.0903691
   PubMed Web of Science ®Google Scholar
• Poulose, S. M., Miller, M. G., Scott, T., & Shukitt-Hale, B. (2017). Nutritional factors affecting adult neurogenesis and cognitive function. Advances in Nutrition: An International Review Journal, 8(6), 804–811. https://doi.org/10.3945/an.117.016261
   Web of Science ®Google Scholar
• Prakash, M. D., Tangalakis, K., Antonipillai, J., Stojanovska, L., Nurgali, K., & Apostolopoulos, V. (2017). Methamphetamine: Effects on the brain, gut and immune system. Pharmacological Research, 120, 60–67. https://doi.org/10.1016/j.phrs.2017.03.009
   PubMed Web of Science ®Google Scholar
• Qiao, D., Xu, J., Le, C., Huang, E., Liu, C., Qiu, P., Lin, Z., Xie, W. B., & Wang, H. (2014). Insulin-like growth factor binding protein 5 (IGFBP5) mediates methamphetamine-induced dopaminergic neuron apoptosis. Toxicology Letters, 230(3), 444–453. https://doi.org/10.1016/j.toxlet.2014.08.010
   PubMed Web of Science ®Google Scholar
• Qiao, H. H., Zhu, L. N., Wang, Y., Hui, J. L., Xie, W. B., Liu, C., Chen, L., & Qiu, P. M. (2019). Implications of alpha-synuclein nitration at tyrosine 39 in methamphetamine-induced neurotoxicity in vitro and in vivo. Neural Regeneration Research, 14(2), 319–327. https://doi.org/10.4103/1673-5374.244795
   PubMed Web of Science ®Google Scholar
• Ramirez, R. L., Perez 3rd., V. J., & Zamanian, R. T. (2018). Methamphetamine and the risk of pulmonary arterial hypertension. Current Opinion in Pulmonary Medicine, 24(5), 416–424. https://doi.org/10.1097/MCP.0000000000000513
   PubMed Web of Science ®Google Scholar
• Ramirez, S. H., Potula, R., Fan, S., Eidem, T., Papugani, A., Reichenbach, N., Dykstra, H., Weksler, B. B., Romero, I. A., Couraud, P. O., & Persidsky, Y. (2009). Methamphetamine disrupts blood-brain barrier function by induction of oxidative stress in brain endothelial cells. Journal Of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism, 29(12), 1933–1945. https://doi.org/10.1038/jcbfm.2009.112
   PubMed Web of Science ®Google Scholar
• Russo, M., Spagnuolo, C., Russo, G. L., Wozniak, K. S., Daglia, M., Sobarzo-Sanchez, E., Nabavi, S. F., & Nabavi, S. M. (2018). Nrf2 targeting by sulforaphane: A potential therapy for cancer treatment. Critical Reviews in Food Science and Nutrition, 58(8), 1391–1405. https://doi.org/10.1080/10408398.2016.1259983
   PubMed Web of Science ®Google Scholar
• Sajja, R. K., Prasad, S., Tang, S., Kaisar, M. A., & Cucullo, L. (2017). Blood-brain barrier disruption in diabetic mice is linked to Nrf2 signaling deficits: Role of ABCB10? Neuroscience Letter, 653, 152–158. https://doi.org/10.1016/j.neulet.2017.05.059
   PubMed Web of Science ®Google Scholar
• Shaerzadeh, F., Streit, W. J., Heysieattalab, S., & Khoshbouei, H. (2018). Methamphetamine neurotoxicity, microglia, and neuroinflammation. Journal of Neuroinflammation, 15(1), 341. https://doi.org/10.1186/s12974-018-1385-0
   PubMed Web of Science ®Google Scholar
• Shah, A., Kumar, S., Simon, S. D., Singh, D. P., & Kumar, A. (2013). HIV gp120- and methamphetamine-mediated oxidative stress induces astrocyte apoptosis via cytochrome P450 2E1. Cell Death & Disease, 4(10), e850. https://doi.org/10.1038/cddis.2013.374
   PubMed Web of Science ®Google Scholar
• Solhi, H., Malekirad, A., Kazemifar, A. M., & Sharifi, F. (2014). Oxidative stress and lipid peroxidation in prolonged users of methamphetamine. Drug Metabolism Letters, 7(2), 79–82. https://doi.org/10.2174/187231280702140520191324
   PubMedGoogle Scholar
• Szeto, Y. T., Tse, R. S. C., Benzie, I. F. F., Kalle, W., & Pak, S. C. (2014). An in vitro study of Sanchi (Panax pseudoginseng) for its DNA protective effect. Food and Agricultural Immunology, 25(3), 332–340. https://doi.org/10.1080/09540105.2013.794202
   Web of Science ®Google Scholar
• Tarozzi, A., Angeloni, C., Malaguti, M., Morroni, F., Hrelia, S., & Hrelia, P. (2013). Sulforaphane as a potential protective phytochemical against neurodegenerative diseases. Oxidative Medicine and Cellular Longevity, 2013. Article id 415078. https://doi.org/10.1155/2013/415078
   Web of Science ®Google Scholar
• Thrash-Williams, B., Ahuja, M., Karuppagounder, S. S., Uthayathas, S., Suppiramaniam, V., & Dhanasekaran, M. (2013). Assessment of therapeutic potential of amantadine in methamphetamine induced neurotoxicity. Neurochemical Research, 38(10), 2084–2094. https://doi.org/10.1007/s11064-013-1117-x
   PubMed Web of Science ®Google Scholar
• Tian, X., Ru, Q., Xiong, Q., Yue, K., Chen, L., Ma, B., Gan, W., Si, Y., Xiao, H., & Li, C. (2017). Neurotoxicity induced by methamphetamine-heroin combination in PC12 cells. Neuroscience Letters, 647, 1–7. https://doi.org/10.1016/j.neulet.2017.03.005
   PubMed Web of Science ®Google Scholar
• Vahidirad, M., Arab-Nozari, M., Mohammadi, H., Zamani, E., & Shaki, F. (2018). Protective effect of captopril against diazinon induced nephrotoxicity and neurotoxicity via inhibition of ROS-NO pathway. Drug and Chemical Toxicology, 41(3), 287–293. https://doi.org/10.1080/01480545.2017.1391830
   PubMed Web of Science ®Google Scholar
• Wang, Y., Gu, Y. H., Liu, M., Bai, Y., Liang, L. Y., & Wang, H. L. (2017). TBHQ alleviated endoplasmic reticulum stress-apoptosis and oxidative stress by PERK-Nrf2 crosstalk in methamphetamine-induced chronic pulmonary toxicity. Oxidative Medicine and Cellular Longevity, 2017, 4310475. https://doi.org/10.1155/2017/4310475
   PubMed Web of Science ®Google Scholar
• Wang, L., Howell, M. E. A., Wallace, A. S., Hawkins, C., Nickic, C. A., Kohne, C., Hall, K. H., Moorman, J. P., Yao, Z. Q., Ning, S. B., & Lieberman, P. M. (2019). P62-mediated selective autophage endows virus-transformed cells with insusceptibility to DNA damage under oxidative stress. PloS Pathogens, 15(4), e1007541. https://doi.org/10.1371/journal.ppat.1007541
   PubMed Web of Science ®Google Scholar
• Wang, A. S., Xu, Y., Zhang, Z. W., Lu, B. B., Yin, X. A., Yao, J., Han, L. Y. Z., Zou, Q., Li, Z., & Zhang, X. H. (2017). Sulforaphane protects MLE-12 lung epithelial cells against oxidative damage caused by ambient air particulate matter. Food & Function, 8(12), 4555–4562. https://doi.org/10.1039/C7FO00969K
   PubMed Web of Science ®Google Scholar
• Wells, P. G., Bhatia, S., Drake, D. M., & Miller-Pinsler, L. (2016). Fetal oxidative stress mechanisms of neurodevelopmental deficits and exacerbation by ethanol and methamphetamine. Birth Defects Research, Part C, Embryo Today: Reviews, 108(2), 108–130. https://doi.org/10.1002/bdrc.21134
   PubMed Web of Science ®Google Scholar
• Wongprayoon, P., & Govitrapong, P. (2016). Melatonin attenuates methamphetamine-induced neurotoxicity. Current Pharmceutical Design, 22(8), 1022–1032. https://doi.org/10.2174/1381612822666151214125657
   PubMed Web of Science ®Google Scholar
• Wongprayoon, P., & Govitrapong, P. (2017). Melatonin protects SH-SY5Y neuronal cells against methamphetamine-induced endoplasmic reticulum stress and apoptotic cell death. Neurotoxic Research, 31(1), 1–10. https://doi.org/10.1007/s12640-016-9647-z
   PubMed Web of Science ®Google Scholar
• Xiong, Q., Ru, Q., Tian, X., Zhou, M., Chen, L., Li, Y., & Li, C. (2018). Krill oil protects PC12 cells against methamphetamine-induced neurotoxicity by inhibiting apoptotic response and oxidative stress. Nutrition Research, 58, 84–94. https://doi.org/10.1016/j.nutres.2018.07.006
   PubMed Web of Science ®Google Scholar
• Xu, W. P., Yang, M. J., Gao, J. F., Zhang, Y., & Tao, L. M. (2018). Oxidative stress and DNA damage induced by spinosad exposure in Spodotera frugiperda Sf9 cells. Food and Agricultural Immunology, 29(1), 171–181. https://doi.org/10.1080/09540105.2017.1364708
   Web of Science ®Google Scholar
• Yang, S. H., He, J. B., Yu, L. H., Li, L., Long, M., Liu, M. D., & Li, P. (2019). Protective role of curcumin in cadmium-induced testicular injury in mice by attenuating oxidative stress via Nrf2/ARE pathway. Environmental Science and Pollution Research, 26(33), 34575–34583. https://doi.org/10.1007/s11356-019-06587-9
   PubMed Web of Science ®Google Scholar
• Yang, S. H., Yu, L. H., Li, L., Guo, Y., Zhang, Y., Long, M., Li, P., & He, J. B. (2018). Protective mechanism of sulforaphane on cadmium-induced sertoli cell injury in mice testis via Nrf2/ARE signaling pathway. Molecules, 23(7), 1774. https://doi.org/10.3390/molecules23071774
   Web of Science ®Google Scholar
• Yu, S., Zhu, L., Shen, Q., Bai, X., & Di, X. (2015). Recent advances in methamphetamine neurotoxicity mechanisms and its molecular pathophysiology. Behavioural Neurology, 2015, 103969. https://doi.org/10.1155/2015/103969
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Guo, W., Chen, H., Gao, J. F., Tao, L. M., Li, Z., & Xu, W. P. (2019). The cytotoxic effects of spinetoram on human HepG2 cells by inducing DNA damage and mitochondria-associated apoptosis. Food and Agricultural Immunology, 30(1), 1020–1032. https://doi.org/10.1080/09540105.2019.1650900
   Web of Science ®Google Scholar