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Research Article

Enhanced kidney damage induced by increasing nonylphenol doses: impact on autophagy-related proteins and proinflammatory cytokines in rats

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Received 01 Feb 2024, Accepted 05 May 2024, Published online: 15 Jul 2024

References

  • Acir IH, Guenther K. 2018. Endocrine-disrupting metabolites of alkylphenol ethoxylates -a critical review of analytical methods, environmental occurrences, toxicity, and regulation. Sci Total Environ. 635:1530–1546. doi: 10.1016/j.scitotenv.2018.04.079.
  • Alekhya Sita GJ, Gowthami M, Srikanth G, Krishna MM, Rama Sireesha K, Sajjarao M, Nagarjuna K, Nagarjuna M, Chinnaboina GK, Mishra A, et al. 2019. Protective role of luteolin against bisphenol A-induced renal toxicity through suppressing oxidative stress, inflammation, and upregulating Nrf2/ARE/HO-1 pathway. IUBMB Life. 71(7):1041–1047. doi: 10.1002/iub.2066.
  • Alers S, Löffler AS, Wesselborg S, Stork B. 2012. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol. 32(1):2–11., doi: 10.1128/MCB.06159-11.
  • Suna PA, Cengiz O, Ceyhan A, Atay E, Ertekin T, Nisari M, Yay A., 2021. The protective role of curcumin against toxic effect of nonylphenol on bone development. Hum Exp Toxicol. 40(12_suppl):S63–S76. doi: 10.1177/09603271211030548.
  • Azmat R, Ijaz MU, Ehsan N, Afsar T, Almajwal A, Amor H, Alruwaili NW, Razak S. 2023. Diosmetin alleviates nonylphenol-induced liver damage by improving biochemical, inflammatory, apoptotic and histological profile in rats. J. King Saud Univ. Sci. 35(1):1–5.
  • Bachmann S, Mundel P. 1994. Nitric oxide in the kidney: synthesis, localization, and function. Am J Kidney Dis. 24(1):112–129. doi: 10.1016/s0272-6386(12)80170-3.
  • Baran M, Yay A, Onder GO, Canturk Tan F, Yalcin B, Balcioglu E, Yıldız OG. 2022. Hepatotoxicity and renal toxicity induced by radiation and the protective effect of quercetin in male albino rats. Int J Radiat Biol. 98(9):1473–1483. doi: 10.1080/09553002.2022.2033339.
  • Bonventre JV, Yang L. 2011. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 121(11):4210–4221. doi: 10.1172/JCI45161.
  • Boyacioglu M, Gules O, Sahiner HS. 2021. Protective Effect of Sodium Selenite on 4-Nonylphenol-Induced Hepatotoxicity and Nephrotoxicity in Rats. Biol Trace Elem Res. 199(8):3001–3012. doi: 10.1007/s12011-020-02418-y.
  • Cachofeiro V, Fortepiani LA, Navarro-Cid J, Lahera V, García-Estañ J. 2002. Renal dysfunction after chronic blockade of nitric oxide synthesis. Antioxid. Redox Signal. 4(6):885–891.
  • Che X, Fang Y, You M, Xu Y, Wang Y. 2020. Exposure to nonylphenol in early life increases pro-inflammatory cytokines in the prefrontal cortex: involvement of gut-brain communication. Chem Biol Interact. 323:109076. doi: 10.1016/j.cbi.2020.109076.
  • Conde E, Giménez-Moyano S, Martín-Gómez L, Rodríguez M, Edurne Ramos M, Aguado-Fraile E, Blanco-Sanchez I, Saiz A, García-Bermejo ML. 2017. HIF-1α induction during reperfusion avoids maladaptive repair after renal ischemia/reperfusion involving miR127-3p. Sci Rep. 7(1):41099. doi: 10.1038/srep41099.
  • Cui J, Jin S, Wang RF. 2016. The BECN1-USP19 axis plays a role in the crosstalk between autophagy and antiviral immune responses. Autophagy. 12(7):1210–1211. doi: 10.1080/15548627.2016.1173801.
  • Dong GK, Zhang XT, Ma LQ, Li N, Ma CL, Cong B, Gu ZY. 2014. Nitric oxide mediated TNF-α, IL-1β gene expression in liver induced by crush injury of rat’s soft tissues. Fa Yi Xue Za Zhi. 30(4):250–252, 256.
  • Duan P, Hu C, Quan C, Yu T, Huang W, Chen W, Tang S, Shi Y, Martin FL, Yang K. 2017. 4-Nonylphenol induces autophagy and attenuates mTOR-p70S6K/4EBP1 signaling by modulating AMPK activation in Sertoli cells. Toxicol Lett. 267:21–31.
  • Feng M, Yin H, Peng H, Liu Z, Lu G, Dang Z. 2017. Hexavalent chromium induced oxidative stress and apoptosis in Pycnoporus sanguineus. Environ Pollut. 228:128–139. doi: 10.1016/j.envpol.2017.05.012.
  • Filomeni G, De Zio D, Cecconi F. 2015. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 22(3):377–388. doi: 10.1038/cdd.2014.150.
  • Genderen AM, Jansen J, Cheng C, Vermonden T, Masereeuw R. 2018. Renal tubular and vascular basement membranes and their mimicry in engineering vascularized kidney tubules. Adv. Healthc. Mater. 7(19):e1800529.
  • Goktepe O, Balcioglu E, Baran M, Cengiz O, Ceyhan A, Suna PA, Bolat D, Yalcin B, Yay A., 2023a. Protective effects of melatonin on female rat ovary treated with nonylphenol. Biotech Histochem. 98(1):13–19.
  • Goktepe O, Onder GO, Cetindag E, Bitgen N, Cengiz Mat O, Alisan Suna P, Tufan E, Yalcın B, Baran M, Oz Gergin O, et al. 2023b. The effect of different doses of nonylphenol on the blood-testicular barrier integrity, hormone level, and DNA damage in the testes of rats. Food Chem Toxicol. 177:113816. doi: 10.1016/j.fct.2023.113816.
  • Guan SY, Leng RX, Tao JH, Li XP, Ye DQ, Olsen N, Zheng SG, Pan HF. 2017. Hypoxia-inducible factor-1α: a promising therapeutic target for autoimmune diseases. Expert Opin. Ther. Targets. 21(7):715–723.
  • Han KH, Lim JM, Kim WY, Kim H, Madsen KM, Kim J. 2005. Expression of endothelial nitric oxide synthase in developing rat kidney. Am. J. Physiol. Renal Physiol. 288(4):F694–702.
  • Han XD, Tu ZG, Gong Y, Shen SN, Wang XY, Kang LN, Hou YY, Chen JX. 2004. The toxic effects of nonylphenol on the reproductive system of male rats. Reprod Toxicol. 19(2):215–221. doi: 10.1016/j.reprotox.2004.06.014.
  • He C, Levine B. 2010. The Beclin 1 interactome. Curr Opin Cell Biol. 22(2):140–149. doi: 10.1016/j.ceb.2010.01.001.
  • Heeringa P, Van Goor H, Itoh-Lindstrom Y, Maeda N, Falk RJ, Assmann KJ, Kallenberg CG, Jennette JC. 2000. Lack of endothelial nitric oxide synthase aggravates murine accelerated anti-glomerular basement membrane glomerulonephritis. Am. J. Pathol. 156(3):879–888.
  • Huang W, Quan C, Duan P, Tang S, Chen W, Yang K. 2016. Nonylphenol induced apoptosis and autophagy involving the Akt/mTOR pathway in prepubertal Sprague-Dawley male rats in vivo and in vitro. Toxicology. 373:41–53. doi: 10.1016/j.tox.2016.11.006.
  • Hurley JH, Young LN. 2017. Mechanisms of autophagy initiation. Annu Rev Biochem. 86(1):225–244. doi: 10.1146/annurev-biochem-061516-044820.
  • Ijaz MU, Tahir A, Samad A, Anwar H. 2021. Nobiletin ameliorates nonylphenol-induced testicular damage by improving biochemical, steroidogenic, hormonal, spermatogenic, apoptotic and histological profile. Hum Exp Toxicol. 40(3):403–416. doi: 10.1177/0960327120950007.
  • Jubendradass R, D’Cruz S, Rani S, Mathur P. 2012. Nonylphenol induces apoptosis via mitochondria and Fas-L-mediated pathways in the liver of adult male rat. Regul Toxicol Pharmacol. 62(3):405–411. doi: 10.1016/j.yrtph.2012.01.004.
  • Kang R, Zeh HJ, Lotze MT, Tang D. 2011. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18(4):571–580. doi: 10.1038/cdd.2010.191.
  • Khandia R, Dadar M, Munjal A, Dhama K, Karthik K, Tiwari R, Yatoo MI, Iqbal HMN, Singh KP, Joshi SK, et al. 2019. A comprehensive review of autophagy and ıts various roles in ınfectious, non-ınfectious, and lifestyle diseases: current knowledge and prospects for disease prevention, novel drug design, and therapy. Cells. 8(7):674. doi: 10.3390/cells8070674.
  • Kim J, Kim YC, Fang C, Russell RC, Kim JH, Fan W, Liu R, Zhong Q, Guan KL. 2013. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell. 152(1–2):290–303. doi: 10.1016/j.cell.2012.12.016.
  • Korkmaz A, Aydoğan M, Kolankaya D, Barlas N. 2011. Vitamin C coadministration augments bisphenol A, nonylphenol, and octylphenol induced oxidative damage on kidney of rats. Environ Toxicol. 26(4):325–337. doi: 10.1002/tox.20556.
  • Kotb AM, Abd-Elkareem MN, Abou Khalil S, Sayed AEDH. 2018. Protective effect of Nigella sativa on 4-nonylphenol-induced nephrotoxicity in Clarias gariepinus (Burchell, 1822). Sci Total Environ. 619-620:692–699. doi: 10.1016/j.scitotenv.2017.11.131.
  • Kroening S, Neubauer E, Wessel J, Wiesener M, Goppelt-Struebe M. 2009. Hypoxia interferes with connective tissue growth factor (CTGF) gene expression in human proximal tubular cell lines. Nephrol. Dial. Transplant. 24(11):3319–3325.
  • Kruger P, Saffarzadeh M, Weber AN, Rieber N, Radsak M, Von Bernuth H, Benarafa C, Roos D, Skokowa J, Hartl D. 2015. Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog. 11(3):e1004651. doi: 10.1371/journal.ppat.1004651.
  • Kyselova V, Peknicova J, Buckiova D, Boubelik M. 2003. Effects of p-nonylphenol and resveratrol on body and organ weight and in vivo fertility of outbred CD-1 mice. Reprod Biol Endocrinol. 1(1):30. doi: 10.1186/1477-7827-1-30.
  • Lee J, Giordano S, Zhang J. 2012. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J. 441(2):523–540. doi: 10.1042/BJ20111451.
  • Li H, Peng X, Wang Y, Cao S, Xiong L, Fan J, Wang Y, Zhuang S, Yu X, Mao H. 2016. Atg5-mediated autophagy deficiency in proximal tubules promotes cell cycle G2/M arrest and renal fibrosis. Autophagy. 12(9):1472–1486. doi: 10.1080/15548627.2016.1190071.
  • Lin K, Wang Y, Gong J, Tan Y, Deng T, Wei N. 2020. Protective effects of total flavonoids from Alpinia officinarum rhizoma against ethanol-induced gastric ulcer in vivo and in vitro. Pharm. Biol. 58(1):854–862.
  • Locatelli AG, Cenci S. 2022. Autophagy and longevity: evolutionary hints from hyper-longevous mammals. Front Endocrinol (Lausanne). 13:1085522. doi: 10.3389/fendo.2022.1085522.
  • Lu IC, Chao HR, Mansor WN, Peng CW, Hsu YC, Yu TY, Chang WH, Fu LM. 2021. Levels of phthalates, bisphenol-a, nonylphenol, and microplastics in fish in the estuaries of northern Taiwan and the ımpact on human health. Toxics. 9(10):246. doi: 10.3390/toxics9100246.
  • Mahfoudh-Boussaid A, Zaouali MA, Hadj-Ayed K, Miled AH, Saidane-Mosbahi D, Rosello-Catafau J, Ben Abdennebi H. 2012. Ischemic preconditioning reduces endoplasmic reticulum stress and upregulates hypoxia inducible factor-1α in ischemic kidney: the role of nitric oxide. J Biomed Sci. 19(1):7. doi: 10.1186/1423-0127-19-7.
  • Mao Z, Zheng XF, Zhang YQ, Tao XX, Li Y, Wang W. 2012. Occurrence and biodegradation of nonylphenol in the environment. Int. J. Mol. Sci. 13:491–505.
  • Mei Y, Glover K, Su M, Sinha SC. 2016. Conformational flexibility of BECN1: essential to its key role in autophagy and beyond. Protein Sci. 25(10):1767–1785. doi: 10.1002/pro.2984.
  • Mizushima N. 2004. Methods for monitoring autophagy. Int J Biochem Cell Biol. 36(12):2491–2502. doi: 10.1016/j.biocel.2004.02.005.
  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ. 2008. Autophagy fights disease through cellular self-digestion. Nature. 451(7182):1069–1075. doi: 10.1038/nature06639.
  • Mogensen CE. 2003. Microalbuminuria and hypertension with focus on type 1 and type 2 diabetes. J Intern Med. 254(1):45–66.
  • Mount PF, Power DA. 2006. Nitric oxide in the kidney: functions and regulation of synthesis. Acta Physiol. 187(4):433–446.
  • Noorimotlagh Z, Mirzaee SA, Ahmadi M, Jaafarzadeh N, Rahim F. 2018. The possible DNA damage induced by environmental organic compounds: the case of nonylphenol. Ecotoxicol Environ Saf. 158:171–181. doi: 10.1016/j.ecoenv.2018.04.023.
  • Onder GO, Goktepe O, Karaman E, Karakas E, Mat OC, Bolat D, Okur E, Tan FC, Balcioglu E, Baran M, et al. 2023. Nonylphenol exposure-induced oocyte quality deterioration could be reversed by boric acid supplementation in rats. Biol Trace Elem Res. 201(9):4518–4529. doi: 10.1007/s12011-023-03657-5.
  • Ozbek E. 2012. Induction of oxidative stress in kidney. Int. J. Nephrol. 2012:465897.
  • Park MH, Gutiérrez-García AK, Choudhury M. 2019. Mono-(2-ethylhexyl) phthalate aggravates inflammatory response via sirtuin regulation and inflammasome activation in RAW 264.7 cells. Chem Res Toxicol. 32(5):935–942. doi: 10.1021/acs.chemrestox.9b00101.
  • Peng X, Wang Y, Li H, Fan J, Shen J, Yu X, Zhou Y, Mao H. 2019. Atg5-mediated autophagy suppresses NF-kappaB signaling to limit epithelial inflammatory response to kidney injury. Cell Death Dis. 10(4):253. doi: 10.1038/s41419-019-1483-7.
  • Pirozzi C, Lama A, Annunziata C, Cavaliere G, Ruiz-Fernandez C, Monnolo A, Comella F, Gualillo O, Stornaiuolo M, Mollica MP, et al. 2020. Oral bisphenol A worsens liver immune-metabolic and mitochondrial dysfunction induced by high-fat diet in adult mice: cross-talk between oxidative stress and inflammasome pathway. Antioxidants. 9(12):1201. doi: 10.3390/antiox9121201.
  • Priego AR, Parra EG, Mas S, Morgado-Pascual JL, Ruiz-Ortega M, Rayego-Mateos S. 2021. Bisphenol A modulates autophagy and exacerbates chronic kidney damage in mice. Int. J. Mol. Sci. 22(13):7189.
  • Ratliff BB, Abdulmahdi W, Pawar R, Wolin MS. 2016. Oxidant mechanisms in renal injury and disease. Antioxid. Redox. Signal. 25(3):119–146.
  • Rehman A, Tahir A, Ehsan N, Ijaz MU, Afsar T, Almajwal A, Alruwaili NW, Hasan Z, Amor H, Razak S. 2022. Protective effects of aucubin against nonylphenol-induced liver toxicity by improving biochemical, inflammatory and histopathological indices. J. King Saud Univ. Sci. 34(4):102033.
  • Sarkar C, Zhao Z, Aungst S, Sabirzhanov B, Faden AI, Lipinski MM. 2014. Impaired autophagy flux is associated with neuronal cell death after traumatic brain injury. Autophagy. 10(12):2208–2222. doi: 10.4161/15548627.2014.981787.
  • Satoh M, Fujimoto S, Haruna Y, Arakawa S, Horike H, Komai N, Sasaki T, Tsujioka K, Makino H, Kashihara N. 2005. NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy. Am J Physiol Renal Physiol. 288(6):F1144–52.
  • Scherz-Shouval R, Elazar Z. 2011. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 36(1):30–38. doi: 10.1016/j.tibs.2010.07.007.
  • Schindler K, Bondeva T, Schindler C, Claus RA, Franke S, Wolf G. 2016. Preconditioned suppression of prolyl-hydroxylases attenuates renal injury but increases mortality in septic murine models. Nephrol Dial Transplant. 31(7):1100–1113. doi: 10.1093/ndt/gfv442.
  • Schmutzler C, Hamann I, Hofmann PJ, Kovacs G, Stemmler L, Mentrup B, Schomburg L, Ambrugger P, Grüters A, Seidlova-Wuttke D, et al. 2004. Endocrine active compounds affect thyrotropin and thyroid hormone levels in serum as well as endpoints of thyroid hormone action in liver, heart and kidney. Toxicology. 205(1–2):95–102. doi: 10.1016/j.tox.2004.06.041.
  • Schug TT, Abagyan R, Blumberg B, Collins TJ, Crews D, DeFur PL, Dickerson SM, Edwards TM, Gore AC, Guillette LJ, et al. 2013. Designing endocrine disruption out of the next generation of chemicals. Green Chem. 15(1):181–198. doi: 10.1039/C2GC35055F.
  • Sharma M, Chadha P. 2016. Study on DNA damaging effects of 4-nonylphenol using erythrocytes from peripheral circulation, gill and kidney of fish Channapunctatus. J. Environ. Biol. 37:313–318.
  • Shi R, Liu Z, Liu T. 2021. The antagonistic effect of bisphenol A and nonylphenol on liver and kidney injury in rats. Immunopharmacol. Immunotoxicol. 43(5):527–535.
  • Shrivastava S, Bhanja Chowdhury J, Steele R, Ray R, Ray RB. 2012. Hepatitis C virus upregulates Beclin1 for induction of autophagy and activates mTOR signaling. J Virol. 86(16):8705–8712. doi: 10.1128/JVI.00616-12.
  • Singh AP, Singh N, Pathak D, Bedi PMS. 2019. Estradiol attenuates ischemia reperfusion-induced acute kidney injury through PPAR-γ stimulated eNOS activation in rats. Mol Cell Biochem. 453(1–2):1–9. doi: 10.1007/s11010-018-3427-4.
  • Sinniah R, Khan TN. 1999. Renal tubular basement membrane changes in tubulointerstitial damage in patients with glomerular diseases. Ultrastruct. Pathol. 23(6):359–368.
  • Tang C, Livingston MJ, Liu Z, Dong Z. 2020. Autophagy in kidney homeostasis and disease. Nat Rev Nephrol. 16(9):489–508. doi: 10.1038/s41581-020-0309-2.
  • Tsai HJ, Wu PY, Huang JC, Chen SC. 2021. Environmental pollution and chronic kidney disease. Int J Med Sci. 18(5):1121–1129. doi: 10.7150/ijms.51594.
  • Urriola-Muñoz P, Li X, Maretzky T, McIlwain DR, Mak TW, Reyes JG, Blobel CP, Moreno RD. 2018. The xenoestrogens biphenol-A and nonylphenol differentially regulate metalloprotease-mediated shedding of EGFR ligands. J Cell Physiol. 233(3):2247–2256. doi: 10.1002/jcp.26097.
  • Wang Z, Schley G, Türkoglu G, Burzlaff N, Amann KU, Willam C, Eckardt KU, Bernhardt WM. 2012. The protective effect of prolyl-hydroxylase inhibition against renal ischaemia requires application prior to ischaemia but is superior to EPO treatment. Nephrol. Dial. Transplant. 27(3):929–936.
  • Wu M, Xu H, Shen Y, Qiu W, Yang M. 2011. Oxidative stress in zebrafish embryos induced by short-term exposure to bisphenol A, nonylphenol, and their mixture. Environ Toxicol Chem. 30(10):2335–2341.
  • Xia W, Jiang Y, Li Y, Wan Y, Liu J, Ma Y, Mao Z, Chang H, Li G, Xu B, et al. 2014. Early-life exposure to bisphenol a induces liver injury in rats involvement of mitochondria-mediated apoptosis. PLOS One. 9(2):e90443. doi: 10.1371/journal.pone.0090443.
  • Yalcin B, Yay AH, Tan FC, Özdamar S, Yildiz OG. 2023. Investigation of the anti-oxidative and anti-inflammatory effects of melatonin on experimental liver damage by radiation. Pathol Res Pract. 246:154477. doi: 10.1016/j.prp.2023.154477.
  • Zhang X, Flaws JA, Spinella MJ, Irudayaraj J. 2023. The relationship between typical environmental endocrine disruptors and kidney disease. Toxics. 11(1):1–21. doi: 10.3390/toxics11010032.
  • Zhang Y, Wang T, Lan M, Zang XW, Li YL, Cui XS, Kim NH, Sun SC. 2018. Melatonin protects oocytes from MEHP exposure-induced meiosis defects in porcine. Biol Reprod. 98(3):286–298. doi: 10.1093/biolre/iox185.

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