Enhanced Kidney Damage Induced by Increasing Nonylphenol Doses: Impact on Autophagy-Related Proteins and Proinflammatory Cytokines in Rats

References

• Acir, I.H., 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. 
   Google Scholar
• Alekhya Sita, G.J., Gowthami, M., Srikanth, G., Krishna, M.M., Rama Sireesha, K., Sajjarao, M., Nagarjuna, K., Nagarjuna, M., Chinnaboina, G.K., Mishra, A., SreeHarsha, N., 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.
   Google Scholar
•  Alers, S., Loffler, A.S., 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, 2-11.
   Google Scholar
• Alişan Suna, P., Cengiz, Ö., 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): 63-76.
   Google Scholar
• Azmat, R., Ijaz, M.U., Ehsan, N., Afsar, T., Almajwal, A., Amor, H., Alruwaili, N.W., 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.
   Google Scholar
• Bachmann, S., Mundel, P., 1994. Nitric oxide in the kidney: synthesis, localization, and function. Am J Kidney Dis. 24,112-129.
   Google Scholar
• Baran, M., Yay, A., Onder, G.O., Canturk Tan, F., Yalcin, B., Balcioglu, E., Yıldız, O.G., 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. 
   Google Scholar
• Bonventre, J.V., Yang, L., 2011. Cellular pathophysiology of ischemic acute kidney injury. J. Clin. Invest. 121(11), 4210-21. 
   Google Scholar
• Boyacioglu, M., Gules, O., Sahiner, H.S., 2021. Protective Effect of Sodium Selenite on 4-Nonylphenol-Induced Hepatotoxicity and Nephrotoxicity in Rats. Biol. Trace Elem. Res. 199, 3001-3012.
   Google Scholar
• Cachofeiro, V., Fortepiani, L.A., Navarro-Cid, J., Lahera, V., García-Estañ, J., 2002. Renal dysfunction after chronic blockade of nitric oxide synthesis. Antioxid. Redox Signal. 4(6), 885-91.
   Google Scholar
• 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.
   Google Scholar
• Conde, E., Giménez-Moyano, S., Martín-Gómez, L, Rodríguez, M., Edurne Ramos, M., Aguado-Fraile, E., Blanco-Sanchez, I., Saiz, A., García-Bermejo, M.L., 2017. HIF-1α induction during reperfusion avoids maladaptive repair after renal ischemia/reperfusion involving miR127-3p. Sci. Rep. 7, 41099.
   Google Scholar
• Cui, J., Jin, S., Wang, R.F., 2016. The BECN1-USP19 axis plays a role in the crosstalk between autophagy and antiviral immune responses. Autophagy. 12(7), 1210-1. 
   Google Scholar
• Dong, G.K., Zhang, X.T., Ma, L.Q., Li, N., Ma, C.L., Cong, B., Gu, Z.Y., 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), 250-2, 256.
   Google Scholar
• Duan, P., Hu, C., Quan, C., Yu, T., Huang, W., Chen, W., Tang, S., Shi, Y., Martin, F.L., 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.
   Google Scholar
• 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
   Google Scholar
• Filomeni, G., De Zio, D., Cecconi. F., 2015. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 22, 377-388.
   Google Scholar
• Genderen, A.M., 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.
   Google Scholar
• Goktepe, O., Balcioglu, E., Baran, M., Cengiz Mat, O., Alisan Suna, P., Bolat, D., Yalcın, B., Yay, A., 2023a. Protective effects of melatonin on female rat ovary treated with nonylphenol. Biotech. Histochem. 98(1), 13-19.
   Google Scholar
• Goktepe, O., Onder, G.O., Cetindag, E., Bitgen, N., Cengiz Mat, O., Alisan Suna, P., Tufan, E., Yalcın, B., Baran, M., Oz Gergin, O., Yay, A., 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. 
   Google Scholar
• Guan, S.Y., Leng, R.X., Tao, J.H., Li, X.P., Ye, D.Q., Olsen, N., Zheng, S.G., Pan, H.F., 2017. Hypoxia-inducible factor-1α: a promising therapeutic target for autoimmune diseases. Expert Opin. Ther. Targets. 21(7), 715-723. 
   Google Scholar
• Han, K.H., Lim, J.M., Kim, W.Y., Kim, H., Madsen, K.M., Kim, J., 2005. Expression of endothelial nitric oxide synthase in developing rat kidney. Am. J. Physiol. Renal Physiol. 288(4), F694-702. 
   Google Scholar
• Han, X.D., Tu, Z.G., Gong, Y., Shen, S.N., Wang X.Y., Kang L.N., Hou, Y.Y., Chen, J.X., 2004. The toxic effects of nonylphenol on the reproductive system of male rats. Reprod. Toxicol. 19, 215-221.
   Google Scholar
• He, C., Levine B., 2010. The Beclin 1 interactome. Curr. Opin. Cell Biol. 2, 140-9. 
   Google Scholar
• Heeringa, P., Van Goor, H., Itoh-Lindstrom, Y., Maeda, N., Falk, R.J., Assmann, K.J., Kallenberg, C.G., Jennette, J.C., 2000. Lack of endothelial nitric oxide synthase aggravates murine accelerated anti-glomerular basement membrane glomerulonephritis. Am. J. Pathol. 156(3), 879-88. 
   Google Scholar
• 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.
   Google Scholar
• Hurley, J.H., Young, L.N., 2017. Mechanisms of autophagy initiation. Annu. Rev. Biochem.  86, 225-244.
   Google Scholar
• Ijaz, M.U., 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. 
   Google Scholar
• 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.
   Google Scholar
• Kang, R., Zeh, H.J., Lotze, M.T., Tang, D., 2011. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18(4), 571-80. 
   Google Scholar
• Khandia, R., Dadar, M., Munjal, A., Dhama, K., Karthik, K., Tiwari, R., Yatoo, M.I., Iqbal, H.M.N., Singh, K.P., Joshi, S.K., Chaicumpa, W., 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. 
   Google Scholar
• Kim, J., Kim, Y.C., Fang, C., Russell, R.C., Kim, J.H., 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.
   Google Scholar
• 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. 
   Google Scholar
• Kotb, A.M.,  Abd-Elkareem, M.N., Abou Khalil, S., Sayed A.E.D.H.,  2018. Protective effect of Nigella sativa on 4-nonylphenol-induced nephrotoxicity in Clarias gariepinus (Burchell, 1822). Sci. Total Environ., 619, 692-699.
   Google Scholar
• 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), 3319-25. 
   Google Scholar
• Kruger,P., Saffarzadeh, M., Weber, A.N., 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.
   Google Scholar
• 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: 30.
   Google Scholar
• Lee, J., Giordano, S., Zhang, J., 2012. Autophagy, mitochondria and oxidative stress: Cross-talk and redox signalling. Biochem. J.  441, 523-540.
   Google Scholar
• 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), 1472-86. 
   Google Scholar
• 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.
   Google Scholar
• Locatelli, A.G., Cenci, S., 2022. Autophagy and longevity: Evolutionary hints from hyper-longevous mammals. Front. Endocrinol. (Lausanne) 13, 1085522.
   Google Scholar
• Lu, I.C., Chao, H.R., Mansor, W.N., Peng, C.W., Hsu, Y.C., Yu, T.Y., Chang, W.H., Fu, L.M., 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.  
   Google Scholar
• Mahfoudh-Boussaid, A., Zaouali, M.A., Hadj-Ayed, K., Miled, A.H., 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. 
   Google Scholar
• Mao, Z., Zheng, X.F., Zhang, Y.Q., Tao, X.X., Li, Y., Wang, W., 2012. Occurrence and biodegradation of nonylphenol in the environment. Int. J. Mol. Sci. 13, 491-505.
   Google Scholar
• Mei, Y., Glover, K., Su, M., Sinha, S.C., 2016. Conformational flexibility of BECN1: Essential to its key role in autophagy and beyond. Protein Sci. 10: 1767-85.
   Google Scholar
• Mizushima, N., 2004. Methods for monitoring autophagy. Int. J. Biochem. Cell. Biol. 36(12): 2491-502. 
   Google Scholar
• Mizushima, N., Levine, B., Cuervo, A.M., Klionsky, D.J., 2008. Autophagy fights disease through cellular self-digestion. Nature. 451, 1069-1075.
   Google Scholar
• Mogensen, C.E., 2003. Microalbuminuria and hypertension with focus on type 1 and type 2 diabetes. J. Intern. Med. 254(1), 45-66.
   Google Scholar
• Mount, P.F., Power, D.A., 2006. Nitric oxide in the kidney: functions and regulation of synthesis. Acta Physiol. (Oxf). 187(4), 433-46.
   Google Scholar
• Noorimotlagh, Z., Mirzaee, S.A., 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.
   Google Scholar
• Onder GO, Goktepe O, Karaman E, Karakas E, Mat OC, Bolat D, Okur E, Tan FC, Balcioglu E, Baran M, Ermis M, Yay A., 2023. Nonylphenol Exposure-Induced Oocyte Quality Deterioration Could be Reversed by Boric Acid Supplementation in Rats. Biol Trace Elem Res. 201(9): 4518-4529.
   Google Scholar
• Ozbek, E., 2012. Induction of oxidative stress in kidney. Int. J. Nephrol. 2012, 465897. 
   Google Scholar
• Park, M.H., Gutiérrez-García, A.K., 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, 935-942.
   Google Scholar
• 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.
   Google Scholar
• Pirozzi, C., Lama, A., Annunziata, C., Cavaliere, G., Ruiz-Fernandez, C., Monnolo, A., Comella, F., Gualillo, O., Stornaiuolo, M., Mollica, M.P., Raso, G.M., Ferrante, M.C., Meli, R., 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.
   Google Scholar
• Priego, A.R., Parra, E.G., Mas, S., Morgado-Pascual, J.L., 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. 
   Google Scholar
• Ratliff, B.B., Abdulmahdi, W.,  Pawar, R., Wolin, M.S., 2016. Oxidant mechanisms in renal injury and disease. Antioxid. Redox. Signal. 25(3), 119-146.
   Google Scholar
• Rehman, A., Tahir, A., Ehsan, N., Ijaz, M.U., Afsar, T., Almajwal, A., Alruwaili, N.W., 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.
   Google Scholar
• Sarkar, C., Zhao, Z., Aungst, S., Sabirzhanov, B., Faden, A.I., Lipinski, M.M., 2014. Impaired autophagy flux is associated with neuronal cell death after traumatic brain injury. Autophagy. 10(12), 2208-22.
   Google Scholar
• 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.
   Google Scholar
• Scherz-Shouval, R., Elazar, Z., 2011. Regulation of autophagy by ROS: Physiology and pathology. Trends Biochem. Sci.  36, 30-38.
   Google Scholar
• Schindler, K., Bondeva, T., Schindler, C., Claus, R.A., 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), 1100-13.
   Google Scholar
• Schmutzler, C., Hamann, I., Hofmann, P.J., Kovacs, G., Stemmler, L., Mentrup, B., Schomburg, L., Ambrugger, P., Grüters, A., Seidlova-Wuttke, D., Jarry, H., Wuttke, W., Köhrle, J., 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. 
   Google Scholar
• Schug T.T., Abagyan, R., Blumberg, B., Collins, T.J., Crews, D., DeFur, P.L., Dickerson, S.M., Edwards, T.M., Gore, A.C., Guillette, L.J., Hayes, T., Heindel, J.J., Moores, A., Patisaul, H.B., Tal, T.L., Thayer, K.A., Vandenberg, L.N., Warner, J., Watson, C.S., Saal, F.S., Zoeller, R.T., O'Brien, K.P., Myers J.P., 2013. Designing endocrine disruption out of the next generation of chemicals. Green Chem. 15, 181-198. 
   Google Scholar
• 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.
   Google Scholar
• 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. 
   Google Scholar
• Shrivastava, S., Bhanja Chowdhury, J., Steele, R., Ray, R., Ray, R.B., 2012. Hepatitis C virus upregulates Beclin1 for induction of autophagy and activates mTOR signaling. J. Virol. 86 (16), 8705-12. 
   Google Scholar
• Singh, A.P., Singh, N., Pathak, D., Bedi, P.M.S., 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.
   Google Scholar
• Sinniah, R., Khan, T.N., 1999. Renal tubular basement membrane changes in tubulointerstitial damage in patients with glomerular diseases. Ultrastruct. Pathol. 23(6), 359-368.
   Google Scholar
• Tang, C., Livingston, M.J., Liu, Z., Dong, Z., 2020. Autophagy in kidney homeostasis and disease. Nat. Rev. Nephrol. 16(9), 489-508.
   Google Scholar
• Tsai, H.J., Wu, P.Y., Huang, J.C., Chen, S.C., 2021. Environmental pollution and chronic kidney disease. Int. J. Med. Sci. 18(5), 1121-1129.
   Google Scholar
• Urriola-Muñoz, P., Li, X., Maretzky, T., McIlwain, D.R., Mak, T.W., Reyes, J.G., Blobel, C.P., Moreno, R.D., 2018. The xenoestrogens biphenol-A and nonylphenol differentially regulate metalloprotease-mediated shedding of EGFR ligands. J. Cell. Physiol. 233, 2247-2256.
   Google Scholar
• Wang, Z., Schley, G., Türkoglu, G., Burzlaff, N., Amann, K.U., Willam, C., Eckardt, K.U., Bernhardt, W.M., 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), 929-36. 
   Google Scholar
• 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. 
   Google Scholar
• Xia, W., Jiang, Y., Li, Y., Wan, Y., Liu, J., Ma, Y., Mao, Z., Chang, H., Li, G., Xu, B., Chen, X., Xu, S., 2014. Early-life exposure to bisphenol a induces liver injury in rats involvement of mitochondria-mediated apoptosis. PLoS One. 9(2), 1-9. 
   Google Scholar
• Yalcin, B., Yay, A.H., Tan, F.C., Özdamar, S., Yildiz, O.G., 2023. Investigation of the anti-oxidative and anti-inflammatory effects of melatonin on experimental liver damage by radiation. Pathol Res Pract. 246: 154477. 
   Google Scholar
• Zhang, X., Flaws, J.A., Spinella, M.J., Irudayaraj, J., 2023. The relationship between typical environmental endocrine disruptors and kidney disease. Toxics. 11(1), 1-21.
   Google Scholar
• Zhang, Y., Wang, T., Lan, M., Zang, X.W., Li, Y.L., Cui, X.S., Kim, N.H., Sun, S.C., 2018. Melatonin protects oocytes from MEHP exposure-induced meiosis defects in porcine. Biol Reprod. 98(3), 286-298.
   Google Scholar