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Journal of Endocrinological Investigation

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01-01-2017 | Original Article

Lactational exposure effect of polychlorinated biphenyl on rat Sertoli cell markers and functional regulators in prepuberal and puberal F₁ offspring

Authors: E. Sugantha Priya, T. Sathish Kumar, S. Balaji, S. Bavithra, P. Raja Singh, D. Sakthivel, B. Ravi Sankar, J. Arunakaran

Published in: Journal of Endocrinological Investigation | Issue 1/2017

Abstract

Purpose

Polychlorinated biphenyls (PCBs) are persistent and bioaccumulative environmental toxicants acting as endocrine disruptors. Many researches evidenced that PCBs affect the male reproductive system in adult rats and it can transfer from mother to offspring through milk. We investigated whether the lactational exposure to PCBs affects the Sertoli cell function in F₁ offspring.

Methods

Dams were orally treated with different doses of PCB—Aroclor 1254 (1, 2 and 5 mg/kg bw/day, respectively) from postpartum day 1–20. Male offspring rats were killed on PND 21 and PND 60. Testes were used both for histological study and to isolate Sertoli cell. Serum and testicular interstitial fluid (TIF) levels of testosterone, ABP and estradiol were analyzed by ELISA method. The mRNA and protein expressions of follicle-stimulating hormone (FSHR), androgen-binding protein (ABP), Inhibinβ, androgen receptor (AR) and estrogen receptor (ERβ) were studied using real-time PCR and immunoblotting, respectively.

Results

The testicular architecture was altered in PCB-treated groups of both prepuberal and puberal rats. Testosterone, estradiol and androgen-binding protein levels were altered in both serum and TIF in PCB treated groups. The gene expression level of FSHR, ABP, ERβ and AR was decreased in a dose-dependent manner, whereas Inhibinβ gene expression level was increased in PCB-treated groups.

Conclusion

Lactational exposure to PCB affects both the histoarchitecture of testis, Sertoli cell maker and functional regulators in both prepuberal and puberal F₁ male progeny.

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Cai JL, Sun LB, Guo ZZ, Jiang XM, Zheng GC, Qiu HL, Sha AG, Wang CG, Ren JZ, Zuo ZH (2015) Decrease in prosaposin in spermatozoon is associated with polychlorinated biphenyl exposure. Int J Clin Exp Pathol 8(3):2436–2448PubMedPubMedCentral

Bergkvist C, Berglund M, Glynn A, Wolk A, Akesson A (2015) Dietary exposure to polychlorinated biphenyls and risk of myocardial infarction—a population-based prospective cohort study. Int J Cardiol 183:242–248. doi:10.1016/j.ijcard.2015.01.055 CrossRefPubMed

Bavithra S, Priya ES, Selvakumar K, Krishnamoorthy G, Arunakaran J (2015) Effect of melatonin on glutamate: BDNF signaling in the cerebral cortex of polychlorinated biphenyls (PCBs)—exposed adult male rats. Neurochem Res 40(9):858–1869. doi:10.1007/s11064-015-1677-z CrossRef

Parent AS, Franssen D, Fudvoye J, Gérard A, Bourguignon JP (2015) Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: revision of human observations and mechanistic insight from rodents. Front Neuroendocrinol 38:12–36. doi:10.1016/j.yfrne.2014.12.004 CrossRefPubMed

Paoli D, Giannandrea F, Gallo M, Turci R, Cattaruzza MS, Lombardo F, Lenzi A, Gandini L (2015) Exposure to polychlorinated biphenyls and hexachlorobenzene, semen quality and testicular cancer risk. J Endocrinol Invest 38(7):745–752. doi:10.1007/s40618-015-0251-5 CrossRefPubMed

Anbalagan J, Kanagaraj P, Srinivasan N, Aruldhas M, Arunakaran J (2003) Effect of polychlorinated biphenyl, Aroclor 1254 on rat epididymis. Indian J Med Res 118:236–242PubMed

Venkataraman P, Sridhar M, Dhanamma S, Vijayababu M, Arunkumar A, Srinivasan N, Arunakaran J (2004) Effects of vitamin supplementation on PCB (Aroclor 1254)-induced changes in ventral prostatic androgen and estrogen receptors. Endocr Res 30(3):469–480CrossRefPubMed

Krishnamoorthy G, Murugesan P, Muthuvel R, Gunadharini DN, Vijayababu MR, Arunkumar A, Venkataraman P, Aruldhas MM, Arunakaran J (2005) Effect of Aroclor 1254 on Sertoli cellular antioxidant system, androgen binding protein and lactate in adult rat in vitro. Toxicology 212(2–3):195–205CrossRefPubMed

Krishnamoorthy G, Venkataraman P, Arunkumar A, Vignesh R, Aruldhas M, Arunakaran J (2007) Ameliorative effect of vitamins (α-tocopherol and ascorbic acid) on PCB (Aroclor 1254) induced oxidative stress in rat epididymal sperm. Reprod Toxicol 23(2):239–245CrossRefPubMed

10.

Murugesan P, Muthusamy T, Balasubramanian K, Arunakaran J (2007) Effects of vitamins C and E on steroidogenic enzymes mRNA expression in polychlorinated biphenyl (Aroclor 1254) exposed adult rat Leydig cells. Toxicology 232(3):170–182CrossRefPubMed

11.

Murugesan P, Muthusamy T, Balasubramanian K, Arunakaran J (2008) Polychlorinated biphenyl (Aroclor 1254) inhibits testosterone biosynthesis and antioxidant enzymes in cultured rat Leydig cells. Reprod Toxicol 25(4):447–454. doi:10.1016/j.reprotox.2008.04.003 CrossRefPubMed

12.

Elumalai P, Krishnamoorthy G, Selvakumar K, Arunkumar R, Venkataraman P, Arunakaran J (2009) Studies on the protective role of lycopene against polychlorinated biphenyls (Aroclor 1254)-induced changes in StAR protein and cytochrome P450 scc enzyme expression on Leydig cells of adult rats. Reprod Toxicol 27(1):41–45. doi:10.1016/j.reprotox.2008.11.053 CrossRefPubMed

13.

Selvakumar K, Banu LS, Krishnamoorthy G, Venkataraman P, Elumalai P, Arunakaran J (2011) Differential expression of androgen and estrogen receptors in PCB (Aroclor 1254)-exposed rat ventral prostate: impact of alpha-tocopherol. Exp Toxicol Pathol 63(1–2):105–112. doi:10.1016/j.etp.2009.10.003 CrossRefPubMed

14.

Venkataraman P, Selvakumar K, Krishnamoorthy G, Muthusami S, Rameshkumar R, Prakash S, Arunakaran J (2010) Effect of melatonin on PCB (Aroclor 1254) induced neuronal damage and changes in Cu/Zn superoxide dismutase and glutathione peroxidase-4 mRNA expression in cerebral cortex, cerebellum and hippocampus of adult rats. Neurosci Res 66(2):189–197. doi:10.1016/j.neures.2009.10.015 CrossRefPubMed

15.

Selvakumar K, Bavithra S, Ganesh L, Krishnamoorthy G, Venkataraman P, Arunakaran J (2013) Polychlorinated biphenyls induced oxidative stress mediated neurodegeneration in hippocampus and behavioral changes of adult rats: anxiolytic-like effects of quercetin. Toxicol Lett 222(1):45–54. doi:10.1016/j.toxlet.2013.06.237 CrossRefPubMed

16.

Mruk DD, Cheng CY (2004) Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25(5):747–806CrossRefPubMed

17.

Choi MS, Park HJ, Oh JH, Lee EH, Park SM, Yoon S (2014) Nonylphenol-induced apoptotic cell death in mouse TM4 Sertoli cells via the generation of reactive oxygen species and activation of the ERK signaling pathway. J Appl Toxicol 34(6):628–636. doi:10.1002/jat.2886 CrossRefPubMed

18.

Sharpe RM, Cooper I (1983) Testicular interstitial fluid as a monitor for changes in the intratesticular environment in the rat. J Reprod Fertil 69(1):125–135CrossRefPubMed

19.

Majumdar SS, Tsuruta J, Griswold MD, Bartke A (1995) Isolation and culture of Sertoli cells from the testes of adult Siberian hamsters: analysis of proteins synthesized and secreted by Sertoli cells cultured from hamsters raised in a long or a short photoperiod. Biol Reprod 52(3):658–666CrossRefPubMed

20.

Raychoudhury S, Thompson EW, Blackshaw A, Irving M (1993) Sertoli cells as paracrine modulators of DNA synthesis in rat peritubular myoid cells in culture. J Reprod Fertil 99(2):513–518CrossRefPubMed

21.

Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1(2):581–585CrossRefPubMed

22.

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2^−ΔΔCT method. Methods 25(4):402–408CrossRefPubMed

23.

Edwards LJ, Coulter CL, Symonds ME, McMillen IC (2001) Prenatal undernutrition, glucocorticoids and the programming of adult hypertension. Clin Exp Pharmacol Phys 28(11):938–941CrossRef

24.

Hany J, Lilienthal H, Sarasin A, Roth-Härer A, Fastabend A, Dunemann L, Lichtensteiger W, Winneke G (1999) Developmental exposure of rats to a reconstituted PCB mixture or Aroclor 1254: effects on organ weights, aromatase activity, sex hormone levels, and sweet preference behavior. Toxicol Appl Pharmacol 158(3):231–243CrossRefPubMed

25.

Sekaran S, Balaganapathy P, Parsanathan R, Elangovan S, Gunashekar J, Bhat FA, Jagadeesan A (2015) Lactational exposure of phthalate causes long-term disruption in testicular architecture by altering tight junctional and apoptotic protein expression in Sertoli cells of first filial generation pubertal Wistar rats. Hum Exp Toxicol 34:575–590. doi:10.1177/0960327114555926 CrossRefPubMed

26.

O’shaughnessy PJ, Monteiro A, Abel M (2012) Testicular development in mice lacking receptors for follicle stimulating hormone and androgen. PLoS ONE 7:e35136. doi:10.1371/journal.pone.0035136 CrossRefPubMedPubMedCentral

27.

Meachem SJ, Nieschlag E, Simoni M (2001) Inhibin B in male reproduction pathophysiology and clinical relevance. Eur J Endocrinol 145(5):561–571CrossRefPubMed

28.

Delbes G, Levacher C, Habert R (2006) Estrogen effects on fetal and neonatal testicular development. Reproduction 132(4):527–538CrossRefPubMed

Title: Lactational exposure effect of polychlorinated biphenyl on rat Sertoli cell markers and functional regulators in prepuberal and puberal F1 offspring
Authors: E. Sugantha Priya
T. Sathish Kumar
S. Balaji
S. Bavithra
P. Raja Singh
D. Sakthivel
B. Ravi Sankar
J. Arunakaran
Publication date: 01-01-2017
Publisher: Springer International Publishing
Published in: Journal of Endocrinological Investigation / Issue 1/2017
Electronic ISSN: 1720-8386
DOI: https://doi.org/10.1007/s40618-016-0539-0

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