Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
권호 표지
DOI QR코드

DOI QR Code

Adverse Effect of Nonylphenol on the Reproductive System in F1 Male Mice: A Subchronic Low-Dose Exposure Model

  • Kim, Yong-Bin (Dept. of Biotechnology, Sangmyung University) ;
  • Cheon, Yong-Pil (Division of Developmental Biology and Physiology, School of Biological Sciences and Chemistry, Sungshin University) ;
  • Lee, Sung-Ho (Dept. of Biotechnology, Sangmyung University)
  • Received : 2019.04.09
  • Accepted : 2019.05.02
  • Published : 2019.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Nonylphenols (NPs) are widely used industrial materials, and are considered as potent endocrine disrupting chemical. Present study was undertaken to clarify the effect of subchronic low-dose NP exposure to F1 generation male mice. Mice were divided into 2 groups; (1) CON, control animals and (2) NP-50 ($50{\mu}g/L$), animals were treated with NP via drinking water. NP exposures were continuously conducted from parental pre-mating period until the postnatal day (PND) 55 of F1 offsprings. Mice were sacrificed on PND 55 and the tissue weights were measured. The initial body weights (at PND 21) and terminal body weights (PND 55) of the NP-50 animals were significantly lower than those of control animals (p<0.05). NP exposure induced a significant increase in the absolute weight of the testes (p<0.05). Conversely, the NP exposure caused significant decrease in the absolute weights of the epididymis (p<0.01), prostate (p<0.05) and seminal vesicle (p<0.05). Histopathological studies revealed that NP-treated animals exerted decreased seminiferous tubule diameters, reduced luminal area, and lower number of germ cells. Also some sloughing morphologies in the tubules were observed. In the caudal epididymis, fewer mature sperms and swollen epithelial cells were found in the NP-treated group. Our results confirmed that the subchronic low-dose NP exposure altered some male parameters and induced histopathological abnormalities in testis and epididymis of F1 mice. Since the NP dose used in this study is close to the average human daily NP exposure, our results could provide practically meaningful understanding of adverse effect of EDC in human.

Keywords

References

  1. 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. https://doi.org/10.1016/j.scitotenv.2018.04.079
  2. Aly HA, Domenech O, Banjar ZM (2012) Effect of nonylphenol on male reproduction: Analysis of rat epididymal biochemical markers and antioxidant defense enzymes. Toxicol Appl Pharmacol 261:134-141. https://doi.org/10.1016/j.taap.2012.02.015
  3. Cha S, Baek JW, Ji HJ, Choi JH, Kim C, Lee MY, Hwang YJ, Yang E, Lee SH, Jung HI, Cheon YP (2017) Disturbing effects of chronic low-dose 4-nonylphenol exposing on gonadal weight and reproductive outcome over one-generation. Dev Reprod 21:121-130. https://doi.org/10.12717/DR.2017.21.2.121
  4. Chitra KC, Latchoumycandane C, Mathur PP (2002) Effect of nonylphenol on the antioxidant system in epididymal sperm of rats. Arch Toxicol 76:545-551. https://doi.org/10.1007/s00204-002-0372-4
  5. Cunny HC, Mayes BA, Rosica KA, Trutter JA, Van Miller JP (1999) Subchronic toxicity (90-day) study with para-nonylphenol in rats. Regul Toxicol Pharmacol 26:72-178.
  6. de Jager C, Bornman MS, van der Horst G (1999) The effect of p-nonylphenol, an environmental toxicant with oestrogenic properties, on fertility potential in adult male rats. Andrologia 31:99-106.
  7. de Weert J, de la Cal A, van den Berg H, Murk A, Langenhoff A, Rijnaarts H, Grotenhuis T (2008) Bioavailability and biodegradation of nonylphenol in sediment determined with chemical and bioanalysis. Environ Toxicol Chem 27:778-785. https://doi.org/10.1897/07-367.1
  8. Di QN, Cao WX, Xu R, Lu L, Xu Q, Wang XB (2018) Chronic low-dose exposure of nonylphenol alters energy homeostasis in the reproductive system of female rats. Toxicol Appl Pharmacol 348:67-75. https://doi.org/10.1016/j.taap.2018.04.007
  9. Duan P, Hu C, Butler HJ, Quan C, Chen W, Huang W, Tang S, Zhou W, Yuan M, Shi Y, Martin FL, Yang K (2016) Effects of 4-nonylphenol on spermatogenesis and induction of testicular apoptosis through oxidative stress-related pathways. Reprod Toxicol 62:27-38. https://doi.org/10.1016/j.reprotox.2016.04.016
  10. Fourie MH, Bornman MS, Viljoen E (2001) Epididymal markers in rats exposed to the xenoestrogen p-nonylphenol: No biochemical effects at low dosages. Andrologia 33:305-310. https://doi.org/10.1046/j.1439-0272.2001.00442.x
  11. Gong Y, Wu J, Huang Y, Shen S, Han X (2009) Nonylphenol induces apoptosis in rat testicular Sertoli cells via endoplasmic reticulum stress. Toxicol Lett 186:84-95. https://doi.org/10.1016/j.toxlet.2009.01.010
  12. Guenther K, Heinke V, Thiele B, Kleist E, Prast H, Raecker T (2002) Endocrine disrupting nonylphenols are ubiquitous in food. Environ Sci Technol 36:1676-1680. https://doi.org/10.1021/es010199v
  13. Hu Y, Wang R, Xiang Z, Qian W, Han X, Li D (2014) Antagonistic effects of a mixture of low-dose nonylphenol and di-n-butyl phthalate (monobutyl phthalate) on the Sertoli cells and serum reproductive hormones in prepubertal male rats in vitro and in vivo. PLOS ONE 9:e93425. https://doi.org/10.1371/journal.pone.0093425
  14. Huang SL, Tuan NN, Lee K (2016) Occurrence, human intake and biodegradation of estrogen-like nonylphenols and octylphenols. Curr Drug Metab 17:293-302. https://doi.org/10.2174/1389200217666151210124821
  15. 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. https://doi.org/10.1186/1477-7827-1-30
  16. Lu WC, Wang AQ, Chen XL, Yang G, Lin Y, Chen YO, Hong CJ, Tian HL (2014) 90d Exposure to nonylphenol has adverse effects on the spermatogenesis and sperm maturation of adult male rats. Biomed Environ Sci 27:907-911. https://doi.org/10.3967/bes2014.128
  17. Mao W, Song Y, Sui H, Cao P, Liu Z (2019) Analysis of individual and combined estrogenic effects of bisphenol, nonylphenol and diethylstilbestrol in immature rats with mathematical models. Environ Health Prev Med. 24:32. https://doi.org/10.1186/s12199-019-0789-5
  18. Mehranjani MS, Noorafshan A, Momeni HR, Abnosi MH, Mahmoodi M, Anvari M, Hoseini SM (2009) Stereological study of the effects of vitamin E on testis structure in rats treated with para-nonylphenol. Asian J Androl 11:508-516. https://doi.org/10.1038/aja.2009.29
  19. Melnick R, Lucier G, Wolfe M, Hall R, Stancel G, Prins G, Gallo M, Reuhl K, Ho SM, Brown T, Moore J, Leakey J, Haseman J, Kohn M (2002) Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review. Environ Health Perspect 110:427-431. https://doi.org/10.1289/ehp.02110427
  20. Muller S, Schmid P, Schlatter C (1998) Pharmacokinetic behavior of 4-nonylphenol in humans. Environ Toxicol Pharmacol 5:257-265. https://doi.org/10.1016/S1382-6689(98)00009-X
  21. Muncke J (2009) Exposure to endocrine disrupting compounds via the food chain: Is packaging a relevant source? Sci Total Environ 407:4549-4559. https://doi.org/10.1016/j.scitotenv.2009.05.006
  22. Nagao T, Wada K, Marumo H, Yoshimura S, Ono H (2001) Reproductive effects of nonylphenol in rats after gavage administration: A two-generation study. Reprod Toxicol 15:293-315. https://doi.org/10.1016/S0890-6238(01)00123-X
  23. Noorimotlagh Z, Haghighi NJ, Ahmadimoghadam M, Rahim F (2017) An updated systematic review on the possible effect of nonylphenol on male fertility. Environ Sci Pollut Res Int 24:3298-3314. https://doi.org/10.1007/s11356-016-7960-y
  24. 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. https://doi.org/10.1016/j.ecoenv.2018.04.023
  25. Patino-Garcia D, Cruz-Fernandes L, Bunay J, Palomino J, Moreno RD (2018) Reproductive alterations in chronically exposed female mice to environmentally relevant doses of a mixture of phthalates and alkylphenols. Endocrinology 159:1050-1061. https://doi.org/10.1210/en.2017-00614
  26. Sato T, Saito H, Uchiyama T, Fujimoto Y, Katase T, Kai O (2009) Effects of synthetic para-nonylphenol isomers administered chronically throughout pregnancy and lactation on reproductive system of mouse pups. Arch Toxicol 83:1097-1108. https://doi.org/10.1007/s00204-009-0464-5
  27. Soto AM, Justicia H, Wray JW, Sonnenschein C (1991) p-Nonyl-phenol: An estrogenic xenobiotic released from "modified" polystyrene. Environ Health Perspect 92:167-173. https://doi.org/10.1289/ehp.9192167
  28. Uguz C, Varisli O, Agca C, Agca Y (2009) Effects of nonylphenol on motility and subcellular elements of epididymal rat sperm. Reprod Toxicol 28:542-549. https://doi.org/10.1016/j.reprotox.2009.06.007
  29. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: Low-dose effects and nonmonotonic dose responses. Endocr Rev 33:378-455. https://doi.org/10.1210/er.2011-1050
  30. Yu J, Yang J, Luo Y, Mengxue Y, Li W, Yang Y, He L, Xu J (2018) The adverse effects of chronic low-dose exposure to nonylphenol on type 2 diabetes mellitus in high sucrose-high fat diet-treated rats. Islets 10:1-9. https://doi.org/10.1080/19382014.2017.1404211