316
Views
25
CrossRef citations to date
0
Altmetric
Original Articles

The implication of mitochondrial dysfunction and mitochondrial oxidative damage in di (2-ethylhexyl) phthalate induced nephrotoxicity in both in vivo and in vitro models

ORCID Icon, , , , , , & ORCID Icon show all
Pages 427-437 | Received 23 Jan 2020, Accepted 16 Apr 2020, Published online: 30 Apr 2020

References

  • Aydemir D, Karabulut G, Şimşek G, Gok M, Barlas N, Ulusu NN. 2018. Impact of the di (2-ethylhexyl) phthalate administration on trace element and mineral levels in relation of kidney and liver damage in rats. Biol Trace Elem Res. 186:474–488.
  • Yang G, Zhou X, Wang J, Zhang W, Zheng H, Lu W, Yuan J. 2012. MEHP-induced oxidative DNA damage and apoptosis in HepG2 cells correlates with p53-mediated mitochondria-dependent signaling pathway. Food Chem Toxicol. 50:2424–2431.
  • Afanasieva K, Prylutska S, Lozovik A, Bogutska K, Sivolob A, Prylutskyy YI, Ritter U, Scharff P; Taras Shevchenko National University of Kyiv, Ukraine. 2015. C60 fullerene prevents genotoxic effects of doxorubicin in human lymphocytes in vitro. Ukr Biochem J. 87:91–98.
  • Amara I, Timoumi R, Graiet I, Ben Salem I, Adelou K, Abid‐Essefi, S. 2019. Di (2‐ethylhexyl) phthalate induces cytotoxicity in HEK‐293 cell line, implication of the Nrf‐2/HO‐1 antioxidant pathway. Environ Toxicol. 34:1034–1042.
  • Barakat R, Lin PC, Park CJ, Best-Popescu C, Bakry HH, Abosalem ME, Abdelaleem NM, Flaws JA, Ko C. 2018. Prenatal exposure to DEHP induces neuronal degeneration and neurobehavioral abnormalities in adult male mice. Toxicol Sci. 164:439–452.
  • Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. 2014. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperthermia. 30:513–523.
  • Bian YY, Guo J, Majeed H, Zhu KX, Guo XN, Peng W, Zhou HM. 2015. Ferulic acid renders protection to HEK293 cells against oxidative damage and apoptosis induced by hydrogen peroxide. In Vitro Cell Dev Biol Anim. 51:722–729.
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
  • Cai J, Shi G, Zhang Y, Zheng Y, Yang J, Liu Q, Gong Y, Yu D, Zhang Z. 2019. Taxifolin ameliorates DEHP-induced cardiomyocyte hypertrophy via attenuating mitochondrial dysfunction and glycometabolism disorder in chicken. Environ Pollut. 255:113155.
  • Chang JW, Liao KW, Huang CY, Huang HB, Chang WT, Jaakkola JJ, Hsu CC, Chen PC, Huang PC. 2020. Phthalate exposure increased the risk of early renal impairment in Taiwanese without type 2 diabetes mellitus. Int J Hyg Environ Health. 224:113414.
  • Cheng B, Yang X, An L, Gao B, Liu X. 2010. Arsenic trioxide-induced apoptosis of Hep-2 cell line through modulating intracellular glutathione (GSH) level. Auris Nasus Larynx. 37:89–94.
  • Chen X, Qin Q, Zhang W, Zhang Y, Zheng H, Liu C, Yang Y, Xiong W, Yuan J. 2013. Activation of the PI3K–AKT–mTOR signaling pathway promotes DEHP-induced Hep3B cell proliferation. Food Chem Toxicol. 59:325–333.
  • Chen H, Zhang W, Rui BB, Yang SM, Xu WP, Wei W. 2016. Di (2-ethylhexyl) phthalate exacerbates non-alcoholic fatty liver in rats and its potential mechanisms. Environ Toxicol Pharmacol. 42:38–44.
  • Dinkova-Kostova AT, Abramov AY. 2015. The emerging role of Nrf2 in mitochondrial function. Free Radical Biol Med. 88:179–188.
  • ECB. 2008. European Chemicals Bureau summary risk assessment report – bis(2-ethylhexyl)phthalate (DEHP) [Online]. Institute for Health and Consumer Protection Toxicology and Chemical Substance (TCS).
  • Erkekoglu P, Giray BK, KıZILGÜN M, Rachidi W, Hininger-Favier I, Roussel AM, Favier A, Hincal F. 2012. Di (2-ethylhexyl) phthalate-induced renal oxidative stress in rats and protective effect of selenium. Toxicol Mech Methods. 22:415–423.
  • Erkekoglu P, Rachidi W, Yuzugullu OG, Giray B, Favier A, Ozturk M, Hincal F. 2010. Evaluation of cytotoxicity and oxidative DNA damaging effects of di (2-ethylhexyl)-phthalate (DEHP) and mono (2-ethylhexyl)-phthalate (MEHP) on MA-10 Leydig cells and protection by selenium. Toxicol Appl Pharmacol. 248:52–62.
  • Erkekoğlu P, Rachidi W, Yüzügüllü O, Giray B, Öztürk M, Favier A, HıNCAL F. 2011. Induction of ROS, p53, p21 in DEHP-and MEHP-exposed LNCaP cells-protection by selenium compounds. Food Chem Toxicol. 49:1565–1571.
  • Feng Y, Wan M. Low intensity ultrasound induces apoptosis via MPT channel on mitochondrial membrane: target for regulating cancer therapy or not? AIP Conference Proceedings. 2017. AIP Publishing.
  • Georgieva E, Ivanova D, Zhelev Z, Bakalova R, Gulubova M, Aoki I. 2017. Mitochondrial dysfunction and redox imbalance as a diagnostic marker of “free radical diseases”. Anticancer Res. 37:5373–5381.
  • Gobe G, Crane D. 2010. Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett. 198:49–55.
  • Goldring CEP, Kitteringham NR, Elsby R, Randle LE, Clement YN, Williams DP, McMahon M, Hayes JD, Itoh K, Yamamoto M, et al. 2004. Activation of hepatic Nrf2 in vivo by acetaminophen in CD‐1 mice. Hepatology. 39:1267–1276.
  • Halden RU. 2010. Plastics and health risks. Annu Rev Public Health. 31:179–194.
  • Hassani M, Ghassemi-Barghi N, Modanloo M, Mohammadpour A, Shokrzadeh M. 2019. Cytotoxic effects of duloxetine on MKN45 and NIH3T3 cell lines and genotoxic effects on human peripheral blood lymphocytes. Arq Gastroenterol. 56:372–376.
  • Heidari R, Jafari F, Khodaei F, Shirazi Yeganeh B, Niknahad H. 2018. Mechanism of Valproic acid‐induced Fanconi syndrome involves mitochondrial dysfunction and oxidative stress in rat kidney. Nephrology. 23:351–361.
  • Heudorf U, Mersch-Sundermann V, Angerer J. 2007. Phthalates: toxicology and exposure. Int J Hyg Environ Health. 210:623–634.
  • Holmström KM, Kostov RV, Dinkova-Kostova AT. 2016. The multifaceted role of Nrf2 in mitochondrial function. Curr Opin Toxicol. 1:80–91.
  • Hong GL, Liu JM, Zhao GJ, Wang L, Liang G, Wu B, Li MF, Qiu QM, Lu ZQ. 2013. The reversal of paraquat-induced mitochondria-mediated apoptosis by cycloartenyl ferulate, the important role of Nrf2 pathway. Exp Cell Res. 319:2845–2855.
  • Júnior HVN, Fonteles MMDF, Mendes DE Freitas R. 2009. Acute seizure activity promotes lipid peroxidation, increased nitrite levels and adaptive pathways against oxidative stress in the frontal cortex and striatum. Oxid Med Cell Longevity. 2:130–137.
  • Kamijo Y, Hora K, Nakajima T, Kono K, Takahashi K, Ito Y, Higuchi M, Kiyosawa K, Shigematsu H, Gonzalez FJ, et al. 2007. Peroxisome Proliferator–Activated Receptor α Protects against Glomerulonephritis Induced by Long-Term Exposure to the Plasticizer Di-(2-Ethylhexyl) Phthalate. JASN. 18:176–188.,
  • KEMI. 2008. Bis (2-Ethylhexyl) phthalate (DEHP).
  • Li PC, Li XN, Du ZH, Wang H, Yu ZR, Li JL. 2018. Di (2-ethyl hexyl) phthalate (DEHP)-induced kidney injury in quail (Coturnix japonica) via inhibiting HSF1/HSF3-dependent heat shock response. Chemosphere. 209:981–988.
  • Liu N, Jiang L, Sun X, Yao X, Zhai X, Liu X, Wu X, Bai Y, Wang S, Yang G. 2017. Mono-(2-ethylhexyl) phthalate induced ROS-dependent autophagic cell death in human vascular endothelial cells. Toxicol in Vitro. 44:49–56.
  • Li J, Zhang J, Yadav MP, Li X. 2019. Biodegradability and biodegradation pathway of di-(2-ethylhexyl) phthalate by Burkholderia pyrrocinia B1213. Chemosphere. 225:443–450.
  • LO D, Wang YT, Wu MC. 2014. Hepatoprotective effect of silymarin on di (2-ethylhexyl) phthalate (DEHP) induced injury in liver FL83B cells. Environ Toxicol Pharmacol. 38:112–118.
  • Luo Y, Li XN, Zhao Y, Du ZH, Li JL. 2019. DEHP triggers cerebral mitochondrial dysfunction and oxidative stress in quail (Coturnix japonica) via modulating mitochondrial dynamics and biogenesis and activating Nrf2-mediated defense response. Chemosphere. 224:626–633.
  • Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, Missiroli S, Patergnani S, Poletti F, et al. 2012. Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct. 2012:1–17.
  • Martinou JC, Youle RJ. 2011. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell. 21:92–101.
  • Nabae K, Doi Y, Takahashi S, Ichihara T, Toda C, Ueda K, Okamoto Y, Kojima N, Tamano S, Shirai T. 2006. Toxicity of di (2-ethylhexyl) phthalate (DEHP) and di (2-ethylhexyl) adipate (DEHA) under conditions of renal dysfunction induced with folic acid in rats: enhancement of male reproductive toxicity of DEHP is associated with an increase of the mono-derivative. Reprod Toxicol. 22:411–417.
  • Niknahad H, Jamshidzadeh A, Heidari R, Hosseini Z, Mobini K, Khodaei F, Ommati MM, Abdoli N, Keshavarz N, Bazyari M, et al. 2016. Paradoxical effect of methimazole on liver mitochondria: in vitro and in vivo. Toxicol Lett. 259:108–115.
  • Potočnjak I, Broznić D, Kindl M, Kropek M, Vladimir-Knežević S, Domitrović R. 2017. Stevia and stevioside protect against cisplatin nephrotoxicity through inhibition of ERK1/2, STAT3, and NF-κB activation. Food Chem Toxicol. 107:215–225.
  • Praveena SM, Teh SW, Rajendran RK, Kannan N, Lin CC, Abdullah R, Kumar S. 2018. Recent updates on phthalate exposure and human health: a special focus on liver toxicity and stem cell regeneration. Environ Sci Pollut Res. 25:11333–11342.
  • Rafael-Vázquez L, García-Trejo S, Aztatzi-Aguilar O, Bazán-Perkins B, Quintanilla-Vega B. 2018. Exposure to diethylhexyl phthalate (DEHP) and monoethylhexyl phthalate (MEHP) promotes the loss of alveolar epithelial phenotype of A549 cells. Toxicol Lett. 294:135–144.
  • Rajesh P, Sathish S, Srinivasan C, Selvaraj J, Balasubramanian K. 2013. Diethyl hexyl phthalate (DEHP) is associated with insulin resistance in adipose tissue of male rat: protective role of antioxidant vitamins (C & E). J Cell Biochem. 114:558–569.
  • Redza-Dutordoir M, Averill-Bates DA. 2016. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 1863:2977–2992.
  • Rosado-Berrios CA, Vélez C, Zayas B. 2011. Mitochondrial permeability and toxicity of diethylhexyl and monoethylhexyl phthalates on TK6 human lymphoblasts cells. Toxicol In Vitro. 25:2010–2016.
  • Rowdhwal SSS, Chen J. 2018. Toxic effects of di-2-ethylhexyl phthalate: an overview. BioMed Res Int. 2018: 1750368.
  • Schiffer TA, Christensen M, Gustafsson H, Palm F. 2018. The effect of inactin on kidney mitochondrial function and production of reactive oxygen species. PLoS One. 13:e0207728.
  • Sedlak J, Lindsay RH. 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 25:192–205.
  • Shokrzadeh M, Dashti A, Aghajanshakeri S, Pourabbas B. 2019a. Prevention Effects of Foeniculum vulgare (Fennel) Hydroalcoholic Extract for Threatened Abortion by Misoprostol Induction in Experimental Mice. Int J Trad Nat Med. 9:1–16.
  • Shokrzadeh M, Ghassemi-Barghi N. 2018a. Antioxidant and genoprotective effects of amifostine against irinotecan toxicity in human hepatoma cells. Int J Cancer Res Ther. 3:1–5.
  • Shokrzadeh M, Ghassemi-Barghi N. 2018b. Melatonin loading chitosan-tripolyphosphate nanoparticles: application in attenuating etoposide-induced genotoxicity in HepG2 cells. Pharmacology. 102:74–80.
  • Shokrzadeh M, Mohammadpour A, Modanloo M, Hassani M, Barghi NG, Niroomand P. 2019b. Cytotoxic effects of aripiprazole on MKN45 and NIH3T3 cell lines and genotoxic effects on human peripheral blood lymphocytes. Arq Gastroenterol. 56:155–159.
  • Sun Y, Shen J, Zeng L, Yang D, Shao S, Wang J, Wei J, Xiong J, Chen J. 2018. Role of autophagy in di-2-ethylhexyl phthalate (DEHP)-induced apoptosis in mouse Leydig cells. Environ Pollut. 243:563–572.
  • Tang X, Wu S, Shen L, Wei Y, Cao X, Wang Y, Long C, Zhou Y, Li D, Huang F, et al. 2018. Di‐(2‐ethylhexyl) phthalate (DEHP)‐induced testicular toxicity through Nrf2‐mediated Notch1 signaling pathway in Sprague–Dawley rats. Environ Toxicol. 33:720–728.,
  • Wang W, Craig ZR, Basavarajappa MS, Gupta RK, Flaws JA. 2012a. Di (2-ethylhexyl) phthalate inhibits growth of mouse ovarian antral follicles through an oxidative stress pathway. Toxicol Appl Pharmacol. 258:288–295.
  • Wang W, Craig ZR, Basavarajappa MS, Hafner KS, Flaws JA. 2012b. Mono-(2-ethylhexyl) phthalate induces oxidative stress and inhibits growth of mouse ovarian antral follicles. Biol Reprod. 87:152.
  • Wang F, Gao F, Lan M, Yuan H, Huang Y, Liu J. 2009. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol In Vitro. 23:808–815.
  • Wang X, Jiang L, Ge L, Chen M, Yang G, Ji F, Zhong L, Guan Y, Liu X. 2015. Oxidative DNA damage induced by di-(2-ethylhexyl) phthalate in HEK-293 cell line. Environ Toxicol Pharmacol. 39:1099–1106.
  • Wang B, Liu F, Dong J, You M, Fu Y, Li C, Lu Y, Chen J. 2018a. Maternal exposure to environmental DEHP exacerbated OVA-induced asthmatic responses in rat offspring. Sci Total Environ. 615:253–261.
  • Wang Z, Shao M, Liu Y. 2017. Promotion of Wilms’ tumor cells migration and invasion by mono-2-ethyhexyl phthalate (MEHP) via activation of NF-κB signals. Chem Biol Interact. 270:1–8.
  • Wang Y, Wang T, Ban Y, Shen C, Shen Q, Chai X, Zhao W, Wei J. 2018b. Di-(2-ethylhexyl) phthalate exposure modulates antioxidant enzyme activity and gene expression in juvenile and adult Daphnia magna. Arch Environ Contam Toxicol. 75:145–156.
  • Ward JM, Diwan BA, Ohshima M, Hu H, Schuller HM, Rice JM. 1986. Tumor-initiating and promoting activities of di (2-ethylhexyl) phthalate in vivo and in vitro. Environ Health Perspect. 65:279.
  • Wei Z, Song L, Wei J, Chen T, Chen J, Lin Y, Xia W, Xu B, Li X, Chen X, et al. 2012. Maternal exposure to di-(2-ethylhexyl) phthalate alters kidney development through the renin–angiotensin system in offspring. Toxicol Lett. 212:212–221.,
  • Wu CT, Wang CC, Huang LC, Liu SH, Chiang CK. 2018. Plasticizer di-(2-ethylhexyl) phthalate induces epithelial-to-mesenchymal transition and renal fibrosis in vitro and in vivo. Toxicol Sci. 164:363–374.
  • Yang Y, Liu H, Liu F, Dong Z. 2014. Mitochondrial dysregulation and protection in cisplatin nephrotoxicity. Arch Toxicol. 88:1249–1256.
  • Zhang S, Fu J, Zhou Z. 2004. In vitro effect of manganese chloride exposure on reactive oxygen species generation and respiratory chain complexes activities of mitochondria isolated from rat brain. Toxicol In Vitro. 18:71–77.
  • Zhang F, Xu Z, Gao J, Xu B, Deng Y. 2008. In vitro effect of manganese chloride exposure on energy metabolism and oxidative damage of mitochondria isolated from rat brain. Environ Toxicol Pharmacol. 26:232–236.
  • Zhang G, Yang W, Jiang F, Zou P, Zeng Y, Ling X, Zhou Z, Cao J, Ao L. 2019a. PERK regulates Nrf2/ARE antioxidant pathway against dibutyl phthalate-induced mitochondrial damage and apoptosis dependent of reactive oxygen species in mouse spermatocyte-derived cells. Toxicol Lett. 308:24–33.
  • Zhang Q, Zhao Y, Talukder M, Han Y, Zhang C, Li XN, Li JL. 2019b. Di (2-ethylhexyl) phthalate induced hepatotoxicity in quail (Coturnix japonica) via modulating the mitochondrial unfolded protein response and NRF2 mediated antioxidant defense. Sci Total Environ. 651:885–894.
  • Zhao Y, Du ZH, Talukder M, Lin J, Li XN, Zhang C, Li JL. 2018b. Crosstalk between unfolded protein response and Nrf2-mediated antioxidant defense in Di-(2-ethylhexyl) phthalate-induced renal injury in quail (Coturnix japonica). Environ Pollut. 242:1871–1879.
  • Zhao Y, Fan JH, Luo Y, Talukder M, Li XN, Zuo YZ, Li JL. 2019. Di-(2-ethylhexyl) phthalate (DEHP)-induced hepatotoxicity in quail (Coturnix japonica) via suppression of the heat shock response. Chemosphere. 228:685–693.
  • Zhao J, Ren S, Liu C, Huo L, Liu Z, Zhai L. 2018a. Di-(2-Ethylhexyl) Phthalate Increases Obesity-Induced Damage to the Male Reproductive System in Mice. Oxid Med Cell Longevity. 2018:1–12.
  • Zhong Q, Putt DA, Xu F, Lash LH. 2008. Hepatic mitochondrial transport of glutathione: studies in isolated rat liver mitochondria and H4IIE rat hepatoma cells. Arch Biochem Biophys. 474:119–127.
  • Zorova LD, Popkov VA, Plotnikov EY, Silachev DN, Pevzner IB, Jankauskas SS, Babenko VA, Zorov SD, Balakireva AV, Juhaszova M, et al. 2018. Mitochondrial membrane potential. Anal Biochem. 552:50–59.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.