An increase of estrogen receptor α protein level regulates BDE-209-mediated blood-testis barrier disruption during spermatogenesis in F1 mice

Abstract

Deca-bromodiphenyl ether (BDE-209) regulates various aspects of spermatogenesis and male fertility through its effect on estrogen receptor α (ERα), but the underlying mechanism remains unclear. Because molecular mechanisms such as remodeling of the blood-testis barrier (BTB) play crucial roles in spermatogenesis, we investigated the disruptive effects of ERα agonists on the BTB in spermatogenesis. In this study, 0, 300, and 500 mg/kg/day of BDE-209 were administered to pregnant adult mice by oral gavage from gestation day 7 to postnatal day 21. SerW3 cells were treated with methylpiperidino pyrazole (MPP) for 30 min before being treated with 50 μg/mL of BDE-209. BDE-209 increases ERα in time- and dose-dependent manners and decreases formin 1 and BTB-associated protein in F1 male mice. Furthermore, BDE-209 impairs the structure and function of the BTB. Activation of ERα signaling could disrupt the BTB, leading to spermatogenesis dysfunction. The results identified the role of ERα in BTB disruption during spermatogenesis and suggested that BTB disruption occurs because of exposure to BDE-209, which could potentially affect spermatogenesis. In conclusion, Sertoli cells seem to be the primary target of BDE-209 in the perinatal period, and this period constitutes a critical window of susceptibility to BDE-209. Also, the SerW3 cell model may not be a particularly useful cell model for studying the function of the cytoskeleton.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Ahmed EA, de Rooij DG (2009) Staging of mouse seminiferous tubule cross-sections. Methods Mol Biol 558:263–277. https://doi.org/10.1007/978-1-60761-103-5_16

  2. Aleksa K, Carnevale A, Goodyer C, Koren G (2012) Detection of polybrominated biphenyl ethers (PBDEs) in pediatric hair as a tool for determining in utero exposure. Forensic Sci Int 218:37–43. https://doi.org/10.1016/j.forsciint.2011.10.003

    Article  CAS  Google Scholar 

  3. Antignac JP, Cariou R, Zalko D, Berrebi A, Cravedi JP, Maume D, Marchand P, Monteau F, Riu A, Andre F, Le Bizec B (2009) Exposure assessment of French women and their newborn to brominated flame retardants: determination of tri- to deca- polybromodiphenylethers (PBDE) in maternal adipose tissue, serum, breast milk and cord serum. Environ Pollut 157:164–173. https://doi.org/10.1016/j.envpol.2008.07.008

    Article  CAS  Google Scholar 

  4. Atanassova N, Mckinnell C, Walker M, Turner KJ, Fisher JS, Morley M, Millar MR, Groome NP, Sharpe RM (1999) Permanent effects of neonatal estrogen exposure in rats on reproductive hormone levels, Sertoli cell number, and the efficiency of spermatogenesis in adulthood pdf. Endocrinology 140:5364–5373

    Article  CAS  Google Scholar 

  5. Brouard V, Guenon I, Bouraima-Lelong H, Delalande C (2016) Differential effects of bisphenol A and estradiol on rat spermatogenesis' establishment. Reprod Toxicol 63:49–61. https://doi.org/10.1016/j.reprotox.2016.05.003

    Article  CAS  Google Scholar 

  6. Bulun SE (2014) Aromatase and estrogen receptor alpha deficiency. Fertil Steril 101:323–329. https://doi.org/10.1016/j.fertnstert.2013.12.022

    Article  CAS  Google Scholar 

  7. Cao H, Wang F, Liang Y, Wang H, Zhang A, Song M (2017) Experimental and computational insights on the recognition mechanism between the estrogen receptor alpha with bisphenol compounds. Arch Toxicol 91:3897–3912. https://doi.org/10.1007/s00204-017-2011-0

    Article  CAS  Google Scholar 

  8. Carbonell A, Perez-Montero S, Climent-Canto P, Reina O, Azorin F (2017) The germline linker histone dBigH1 and the translational regulator bam form a repressor loop essential for male germ stem cell differentiation. Cell Rep 21:3178–3189. https://doi.org/10.1016/j.celrep.2017.11.060

    Article  CAS  Google Scholar 

  9. Carreau S, Hess RA (2010) Oestrogens and spermatogenesis. Philos Trans R Soc Lond Ser B Biol Sci 365:1517–1535. https://doi.org/10.1098/rstb.2009.0235

    Article  CAS  Google Scholar 

  10. Carreau S, Bouraima-Lelong H, Delalande C (2011) Estrogens—new players in spermatogenesis. Reprod Biol 11:174–193. https://doi.org/10.1016/s1642-431x(12)60065-5

    Article  Google Scholar 

  11. Carreau S, Bouraima-Lelong H, Delalande C (2012) Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci 57:31–36. https://doi.org/10.2478/v10039-012-0005-y

    Article  CAS  Google Scholar 

  12. Chauvigne F, Parhi J, Olle J, Cerda J (2017) Dual estrogenic regulation of the nuclear progestin receptor and spermatogonial renewal during gilthead seabream (Sparus aurata) spermatogenesis. Comp Biochem Physiol A Mol Integr Physiol 206:36–46. https://doi.org/10.1016/j.cbpa.2017.01.008

    Article  CAS  Google Scholar 

  13. Chen ZJ, Liu HY, Cheng Z, Man YB, Zhang KS, Wei W, Du J, Wong MH, Wang HS (2014) Polybrominated diphenyl ethers (PBDEs) in human samples of mother-newborn pairs in South China and their placental transfer characteristics. Environ Int 73:77–84. https://doi.org/10.1016/j.envint.2014.07.002

    Article  CAS  Google Scholar 

  14. Chen L, Wang X, Zhang X, Lam PKS, Guo Y, Lam JCW, Zhou B (2017) Transgenerational endocrine disruption and neurotoxicity in zebrafish larvae after parental exposure to binary mixtures of decabromodiphenyl ether (BDE-209) and lead. Environ Pollut 230:96–106. https://doi.org/10.1016/j.envpol.2017.06.053

    Article  CAS  Google Scholar 

  15. Chen J, Li X, Li X, Chen D (2018) The environmental pollutant BDE-209 regulates NO/cGMP signaling through activation of NMDA receptors in neurons. Environ Sci Pollut Res Int 25:3397–3407. https://doi.org/10.1007/s11356-017-0651-5.

    Article  CAS  Google Scholar 

  16. Clarke M, Pearl CA (2014) Alterations in the estrogen environment of the testis contribute to declining sperm production in aging rats. Syst Biol Reprod Med 60:89–97. https://doi.org/10.3109/19396368.2014.885995

    Article  CAS  Google Scholar 

  17. Cooke PS, Nanjappa MK, Ko C, Prins GS, Hess RA (2017) Estrogens in male physiology. Physiol Rev 97:995–1043. https://doi.org/10.1152/physrev.00018.2016

    Article  Google Scholar 

  18. Doyle TJ, Bowman JL, Windell VL, McLean DJ, Kim KH (2013) Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol Reprod 88:112. https://doi.org/10.1095/biolreprod.112.106104.

    Article  Google Scholar 

  19. Du P, Li Z, Du L, Zhang H, Zhou Y, Sun W, Xiao X, He Y, Sun B, Yu Y, Chen D (2015) The effects of PBDE-209 exposure during pregnancy on placental ET-1 and eNOS expression and the birth weight of offspring. Int J Dev Neurosci 43:86–91. https://doi.org/10.1016/j.ijdevneu.2015.03.011

    Article  CAS  Google Scholar 

  20. Dumasia K, Kumar A, Kadam L, Balasinor NH (2015) Effect of estrogen receptor-subtype-specific ligands on fertility in adult male rats. J Endocrinol 225:169–180. https://doi.org/10.1530/JOE-15-0045.

    Article  CAS  Google Scholar 

  21. Dumasia K, Kumar A, Deshpande S, Sonawane S, Balasinor NH (2016) Differential roles of estrogen receptors, ESR1 and ESR2, in adult rat spermatogenesis. Mol Cell Endocrinol 428:89–100. https://doi.org/10.1016/j.mce.2016.03.024

    Article  CAS  Google Scholar 

  22. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB, K KS (1996) Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility pdf. Endocrinology 137(11):4796–4805

    Article  CAS  Google Scholar 

  23. Favareto AP, de Toledo FC, Kempinas Wde G (2011) Paternal treatment with cisplatin impairs reproduction of adult male offspring in rats. Reprod Toxicol 32:425–433. https://doi.org/10.1016/j.reprotox.2011.10.003

    Article  CAS  Google Scholar 

  24. Feng Y, Manka D, Wagner KU, Khan SA (2007) Estrogen receptor-alpha expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. Proc Natl Acad Sci U S A 104:14718–14723. https://doi.org/10.1073/pnas.0706933104

    Article  CAS  Google Scholar 

  25. Fernandes AR, Mortimer D, Rose M, Smith F, Panton S, Garcia-Lopez M (2015) Bromine content and brominated flame retardants in food and animal feed from the UK. Chemosphere 150:472–478. https://doi.org/10.1016/j.chemosphere.2015.12.042

    Article  CAS  Google Scholar 

  26. Fietz D, Ratzenböck C, Hartmann K, Raabe O, Kliesch S, Weidner W, Klug J, Bergmann M (2014) Expression pattern of estrogen receptors α and β and G-protein-coupled estrogen receptor 1 in the human testis. Histochem Cell Biol 142:421–432. https://doi.org/10.1007/s00418-014-1216-z

    Article  CAS  Google Scholar 

  27. Fisher JS, Turner KJ, Brown D, Sharpe RM (1999) Effect of neonatal exposure to estrogenic compounds on development of the excurrent ducts of the rat testis through puberty to adulthood. Environ Health Perspect 107:397–405. https://doi.org/10.1289/ehp.99107397

    Article  CAS  Google Scholar 

  28. Gao Y, Mruk D, Lui W, Lee W, Cheng C (2016) F5-peptide induces aspermatogenesis by disrupting organization of actin- and microtubule-based cytoskeletons in the testis. Oncotarget 7:64203–64220. https://doi.org/10.18632/oncotarget.11887.

    Article  Google Scholar 

  29. Ge LC, Chen ZJ, Liu HY, Zhang KS, Liu H, Huang HB, Zhang G, Wong CK, Giesy JP, Du J, Wang HS (2014) Involvement of activating ERK1/2 through G protein coupled receptor 30 and estrogen receptor alpha/beta in low doses of bisphenol A promoting growth of Sertoli TM4 cells. Toxicol Lett 226:81–89. https://doi.org/10.1016/j.toxlet.2014.01.035

    Article  CAS  Google Scholar 

  30. Grikscheit K, Grosse R (2016) Formins at the junction. Trends Biochem Sci 41:148–159. https://doi.org/10.1016/j.tibs.2015.12.002

    Article  CAS  Google Scholar 

  31. Gunawan A, Kaewmala K, Uddin MJ, Cinar MU, Tesfaye D, Phatsara C, Tholen E, Looft C, Schellander K (2011) Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality. Anim Reprod Sci 128:11–21. https://doi.org/10.1016/j.anireprosci.2011.08.008

    Article  CAS  Google Scholar 

  32. Han Z, Li Y, Zhang S, Song N, Xu H, Dang Y, Liu C, Giesy JP, Yu H (2017) Prenatal transfer of decabromodiphenyl ether (BDE-209) results in disruption of the thyroid system and developmental toxicity in zebrafish offspring. Aquat Toxicol 190:46–52. https://doi.org/10.1016/j.aquatox.2017.06.020

    Article  CAS  Google Scholar 

  33. Hardy ML (2002) The toxicology of the three commercial polybrominated diphenyl oxide (ether) flame retardants. Chemosphere 46:757–777

    Article  CAS  Google Scholar 

  34. Hess RA (2014) Disruption of estrogen receptor signaling and similar pathways in the efferent ductules and initial segment of the epididymis. Spermatogenesis 4:e979103. https://doi.org/10.4161/21565562.2014.979103

    Article  Google Scholar 

  35. Hirahara Y, Matsuda KI, Liu YF, Yamada H, Kawata M, Boggs JM (2013) 17beta-Estradiol and 17alpha-estradiol induce rapid changes in cytoskeletal organization in cultured oligodendrocytes. Neuroscience 235:187–199. https://doi.org/10.1016/j.neuroscience.2012.12.070.

    Article  CAS  Google Scholar 

  36. Johansson N, Viberg H, Fredriksson A, Eriksson P (2008) Neonatal exposure to deca-brominated diphenyl ether (PBDE 209) causes dose-response changes in spontaneous behaviour and cholinergic susceptibility in adult mice. Neurotoxicology 29:911–919. https://doi.org/10.1016/j.neuro.2008.09.008

    Article  CAS  Google Scholar 

  37. Johnson L, Thompson DL Jr, Varner DD (2008) Role of Sertoli cell number and function on regulation of spermatogenesis. Anim Reprod Sci 105:23–51. https://doi.org/10.1016/j.anireprosci.2007.11.029

    Article  CAS  Google Scholar 

  38. Joseph A, Hess RA, Schaeffer DJ, Ko C, Hudgin-Spivey S, Chambon P, Shur BD (2010) Absence of estrogen receptor alpha leads to physiological alterations in the mouse epididymis and consequent defects in sperm function. Biol Reprod 82:948–957. https://doi.org/10.1095/biolreprod.109.079889.

    Article  CAS  Google Scholar 

  39. Katleba KD, Legacki EL, Conley AJ, Berger T (2015) Steroid regulation of early postnatal development in the corpus epididymidis of pigs. J Endocrinol 225:125–134. https://doi.org/10.1530/JOE-15-0001.

    Article  CAS  Google Scholar 

  40. Khalil A, Parker M, Brown SE, Cevik SE, Guo LW, Jensen J, Olmsted A, Portman D, Wu H, Suvorov A (2017) Perinatal exposure to 2,2′,4′4'-tetrabromodiphenyl ether induces testicular toxicity in adult rats. Toxicology 389:21–30. https://doi.org/10.1016/j.tox.2017.07.006

    Article  CAS  Google Scholar 

  41. Kim TH, Lee YJ, Lee E, Kim MS, Kwack SJ, Kim KB, Chung KK, Kang TS, Han SY, Lee J, Lee BM, Kim HS (2009) Effects of gestational exposure to decabromodiphenyl ether on reproductive parameters, thyroid hormone levels, and neuronal development in Sprague-Dawley rats offspring. J Toxicol Environ Health A 72:1296–1303. https://doi.org/10.1080/15287390903320742

    Article  CAS  Google Scholar 

  42. Kojima H, Takeuchi S, Uramaru N, Sugihara K, Yoshida T, Kitamura S (2009) Nuclear hormone receptor activity of polybrominated diphenyl ethers and their hydroxylated and methoxylated metabolites in transactivation assays using Chinese hamster ovary cells. Environ Health Perspect 117:1210–1218. https://doi.org/10.1289/ehp.0900753

    Article  CAS  Google Scholar 

  43. Law RJ, Barry J, Bersuder P, Barber JL, Deaville R, Reid RJ, Jepson PD (2010) Levels and trends of brominated diphenyl ethers in blubber of harbor porpoises (Phocoena phocoena) from the U.K., 1992-2008. Environ Sci Technol 44:4447–4451. https://doi.org/10.1021/es100140q

    Article  CAS  Google Scholar 

  44. Leavy M, Trottmann M, Liedl B, Reese S, Stief C, Freitag B, Baugh J, Spagnoli G, Kolle S (2017) Effects of elevated beta-estradiol levels on the functional morphology of the testis—new insights. Sci Rep 7:39931. https://doi.org/10.1038/srep39931

    Article  CAS  Google Scholar 

  45. Leonetti C, Butt CM, Hoffman K, Miranda ML, Stapleton HM (2016) Concentrations of polybrominated diphenyl ethers (PBDEs) and 2,4,6-tribromophenol in human placental tissues. Environ Int 88:23–29. https://doi.org/10.1016/j.envint.2015.12.002

    Article  CAS  Google Scholar 

  46. Li W, Zhu L, Zha J, Wang Z (2014) Effects of decabromodiphenyl ether (BDE-209) on mRNA transcription of thyroid hormone pathway and spermatogenesis associated genes in Chinese rare minnow (Gobiocypris rarus). Environ Toxicol 29:1–9. https://doi.org/10.1002/tox.20767.

    Article  Google Scholar 

  47. Li N, Mruk DD, Cheng CY (2015) Actin binding proteins in blood-testis barrier function. Curr Opin Endocrinol Diabetes Obes 22:238–247. https://doi.org/10.1097/MED.0000000000000155

    Article  CAS  Google Scholar 

  48. Li J, Dai RX, Chen DJ, Wang CM, Lin HF, Li YR, Tang J, Zhai JX (2016a) Effects of extracellular regulated protein kinases protein and impairment of blood testis barriar stucturein of mice with exposure to decabromodiphenyl ether. Zhonghua Yu Fang Yi Xue Za Zhi 50:1096–1101. https://doi.org/10.3760/cma.j.issn.0253-9624.2016.12.014

    CAS  Article  Google Scholar 

  49. Li N, Mruk DD, Lee WM, Wong CK, Cheng CY (2016b) Is toxicant-induced Sertoli cell injury in vitro a useful model to study molecular mechanisms in spermatogenesis? Semin Cell Dev Biol 59:141–156. https://doi.org/10.1016/j.semcdb.2016.01.003

    Article  CAS  Google Scholar 

  50. Lin J, Zhu J, Li X, Li S, Lan Z, Ko J, Lei Z (2014) Expression of genomic functional estrogen receptor 1 in mouse sertoli cells. Reprod Sci 21:1411–1422. https://doi.org/10.1177/1933719114527355

    Article  CAS  Google Scholar 

  51. Lucas TF, Siu ER, Esteves CA, Monteiro HP, Oliveira CA, Porto CS, Lazari MF (2008) 17beta-estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane, MAPK3/1 phosphorylation and proliferation of cultured immature rat Sertoli cells. Biol Reprod 78:101–114. https://doi.org/10.1095/biolreprod.107.063909

    Article  CAS  Google Scholar 

  52. Lucas TF, Lazari MF, Porto CS (2014) Differential role of the estrogen receptors ESR1 and ESR2 on the regulation of proteins involved with proliferation and differentiation of Sertoli cells from 15-day-old rats. Mol Cell Endocrinol 382:84–96. https://doi.org/10.1016/j.mce.2013.09.015

    Article  CAS  Google Scholar 

  53. MacCalman CD, Getsios S, Farookhi R, Blaschuk OW (1997) Estrogens potentiate the stimulatory effects of follicle-stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology 138:41–48. https://doi.org/10.1210/endo.138.1.4831.

    Article  CAS  Google Scholar 

  54. Mahato D, Goulding EH, Korach KS, E EM (2001) Estrogen receptor-α is required by the supporting somatic cells for spermatogenesis. Mol Cell Endocrinol 178:57–63

    Article  CAS  Google Scholar 

  55. Mi XB, Bao LJ, Wu CC, Wong CS, Zeng EY (2017) Absorption, tissue distribution, metabolism, and elimination of decabrominated diphenyl ether (BDE-209) in rats after multi-dose oral exposure. Chemosphere 186:749–756. https://doi.org/10.1016/j.chemosphere.2017.08.049

    Article  CAS  Google Scholar 

  56. Miyaso H, Nakamura N, Matsuno Y, Kawashiro Y, Komiyama M, Mori C (2012) Postnatal exposure to low-dose decabromodiphenyl ether adversely affects mouse testes by increasing thyrosine phosphorylation level of cortactin. J Toxicol Sci 37:987–999

    Article  CAS  Google Scholar 

  57. Miyaso H, Nakamura N, Naito M, Hirai S, Matsuno Y, Itoh M, Mori C (2014) Early postnatal exposure to a low dose of decabromodiphenyl ether affects expression of androgen and thyroid hormone receptor-alpha and its splicing variants in mouse Sertoli cells. PLoS One 9:e114487. https://doi.org/10.1371/journal.pone.0114487

    Article  CAS  Google Scholar 

  58. Nanjappa MK, Hess RA, Medrano TI, Locker SH, Levin ER, Cooke PS (2016) Membrane-localized estrogen receptor 1 is required for normal male reproductive development and function in mice. Endocrinology 157:2909–2919. https://doi.org/10.1210/en.2016-1085

    Article  CAS  Google Scholar 

  59. Nebel BR, Amarose AP, H EM (1961) Calendar of gametogenic development in the prepuberal male mouse. Science 134:832–833. https://doi.org/10.1126/science.134.3482.832.

    Article  CAS  Google Scholar 

  60. Neuman-Lee LA, Carr J, Vaughn K, French SS (2015) Physiological effects of polybrominated diphenyl ether (PBDE-47) on pregnant gartersnakes and resulting offspring. Gen Comp Endocrinol 219:143–151. https://doi.org/10.1016/j.ygcen.2015.03.011

    Article  CAS  Google Scholar 

  61. O'Shaughnessy PJ (2014) Hormonal control of germ cell development and spermatogenesis. Semin Cell Dev Biol 29:55–65. https://doi.org/10.1016/j.semcdb.2014.02.010

    Article  CAS  Google Scholar 

  62. Qiu L, Zhang X, Zhang X, Zhang Y, Gu J, Chen M, Zhang Z, Wang X, Wang SL (2013) Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice. Toxicol Sci 135:229–240. https://doi.org/10.1093/toxsci/kft129

    Article  CAS  Google Scholar 

  63. Salian S, Doshi T, Vanage G (2009) Neonatal exposure of male rats to Bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology 265:56–67. https://doi.org/10.1016/j.tox.2009.09.012

    Article  CAS  Google Scholar 

  64. Sarkar D, Singh SK (2017) Maternal exposure to polybrominated diphenyl ether (BDE-209) during lactation affects germ cell survival with altered testicular glucose homeostasis and oxidative status through down-regulation of Cx43 and p27Kip1 in prepubertal mice offspring. Toxicology 386:103–119. https://doi.org/10.1016/j.tox.2017.05.016

    Article  CAS  Google Scholar 

  65. Sarkar D, Singh SK (2018) Inhibition of testicular steroidogenesis and impaired differentiation of Sertoli cells in peripubertal mice offspring following maternal exposure to BDE-209 during lactation suppress germ cell proliferation. Toxicol Lett 290:83–96. https://doi.org/10.1016/j.toxlet.2018.03.026

    Article  CAS  Google Scholar 

  66. Sarkar D, Chowdhury JP, Singh SK (2016) Effect of polybrominated diphenyl ether (BDE-209) on testicular steroidogenesis and spermatogenesis through altered thyroid status in adult mice. Gen Comp Endocrinol 239:50–61. https://doi.org/10.1016/j.ygcen.2015.11.009

    Article  CAS  Google Scholar 

  67. Sha J, Wang Y, Lv J, Wang H, Chen H, Qi L, Tang X (2015) Effects of two polybrominated diphenyl ethers (BDE-47, BDE-209) on the swimming behavior, population growth and reproduction of the rotifer Brachionus plicatilis. J Environ Sci (China) 28:54–63. https://doi.org/10.1016/j.jes.2014.07.020

    Article  CAS  Google Scholar 

  68. Shi Z, Jiao Y, Hu Y, Sun Z, Zhou X, Feng J, Li J, Wu Y (2013) Levels of tetrabromobisphenol A, hexabromocyclododecanes and polybrominated diphenyl ethers in human milk from the general population in Beijing, China. Sci Total Environ 452-453:10–18. https://doi.org/10.1016/j.scitotenv.2013.02.038

    Article  CAS  Google Scholar 

  69. Sinkevicius KW, Laine M, Lotan TL, Woloszyn K, Richburg JH, Greene GL (2009) Estrogen-dependent and -independent estrogen receptor-alpha signaling separately regulate male fertility. Endocrinology 150:2898–2905. https://doi.org/10.1210/en.2008-1016

    Article  CAS  Google Scholar 

  70. Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21:214–222. https://doi.org/10.1016/j.tem.2009.12.007

    Article  CAS  Google Scholar 

  71. Su W, Mruk DD, Cheng CY (2013) Regulation of actin dynamics and protein trafficking during spermatogenesis—insights into a complex process. Crit Rev Biochem Mol Biol 48:153–172. https://doi.org/10.3109/10409238.2012.758084

    Article  CAS  Google Scholar 

  72. Suvorov A, Shershebnev A, Wu H, Medvedeva Y, Sergeyev O, Pilsner JR (2018) Perinatal exposure to low dose 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) alters sperm DNA methylation in adult rats. Reprod Toxicol 75:136–143. https://doi.org/10.1016/j.reprotox.2017.10.009

    Article  CAS  Google Scholar 

  73. Toft G, Lenters V, Vermeulen R, Heederik D, Thomsen C, Becher G, Giwercman A, Bizzaro D, Manicardi GC, Spano M, Rylander L, Pedersen HS, Strucinski P, Zviezdai V, Bonde JP (2014) Exposure to polybrominated diphenyl ethers and male reproductive function in Greenland, Poland and Ukraine. Reprod Toxicol 43:1–7. https://doi.org/10.1016/j.reprotox.2013.10.002

    Article  CAS  Google Scholar 

  74. Tseng LH, Lee CW, Pan MH, Tsai SS, Li MH, Chen JR, Lay JJ, Hsu PC (2006) Postnatal exposure of the male mouse to 2,2′,3,3′,4,4′,5,5′,6,6′-decabrominated diphenyl ether: decreased epididymal sperm functions without alterations in DNA content and histology in testis. Toxicology 224:33–43. https://doi.org/10.1016/j.tox.2006.04.003

    Article  CAS  Google Scholar 

  75. Tseng LH, Hsu PC, Lee CW, Tsai SS, Pan MH, Li MH (2013) Developmental exposure to decabrominated diphenyl ether (BDE-209): effects on sperm oxidative stress and chromatin DNA damage in mouse offspring. Environ Toxicol 28:380–309. https://doi.org/10.1002/tox.20729

    Article  CAS  Google Scholar 

  76. Valcarce DG, Vuelta E, Robles V, Herraez MP (2017) Paternal exposure to environmental 17-alpha-ethinylestradiol concentrations modifies testicular transcription, affecting the sperm transcript content and the offspring performance in zebrafish. Aquat Toxicol 193:18–29. https://doi.org/10.1016/j.aquatox.2017.09.025

    Article  CAS  Google Scholar 

  77. Vergouwen R, Huiskamp R, Bas R, Roepers-Gajadien H, Davids J, de Rooij D (1993) Postnatal development of testicular cell populations in mice. Jreprodfertil 99:479–485. https://doi.org/10.1530/jrf.0.0990479

    CAS  Article  Google Scholar 

  78. Viberg H, Fredriksson A, Eriksson P (2007) Changes in spontaneous behaviour and altered response to nicotine in the adult rat, after neonatal exposure to the brominated flame retardant, decabrominated diphenyl ether (PBDE 209). Neurotoxicology 28:136–142. https://doi.org/10.1016/j.neuro.2006.08.006

    Article  CAS  Google Scholar 

  79. Wakui S, Shirai M, Motohashi M, Mutou T, Oyama N, Wempe MF, Takahashi H, Inomata T, Ikegami M, Endou H, Asari M (2014) Effects of in utero exposure to di(n-butyl) phthalate for estrogen receptors alpha, beta, and androgen receptor of Leydig cell on rats. Toxicol Pathol 42:877–887. https://doi.org/10.1177/0192623313502879

    Article  CAS  Google Scholar 

  80. Wan HT, Mruk DD, Wong CK, Cheng CY (2014) Perfluorooctanesulfonate (PFOS) perturbs male rat Sertoli cell blood-testis barrier function by affecting F-actin organization via p-FAK-Tyr(407): an in vitro study. Endocrinology 155:249–262. https://doi.org/10.1210/en.2013-1657

    Article  CAS  Google Scholar 

  81. Wan X, Ru Y, Chu C, Ni Z, Zhou Y, Wang S, Zhou Z, Zhang Y (2016) Bisphenol A accelerates capacitation-associated protein tyrosine phosphorylation of rat sperm by activating protein kinase A. Acta Biochim Biophys Sin Shanghai 48:573–580. https://doi.org/10.1093/abbs/gmw039

    Article  CAS  Google Scholar 

  82. Wang C, Yang L, Wang S, Zhang Z, Yu Y, Wang M, Cromie M, Gao W, Wang SL (2016) The classic EDCs, phthalate esters and organochlorines, in relation to abnormal sperm quality: a systematic review with meta-analysis. Sci Rep 6:19982. https://doi.org/10.1038/srep19982

    Article  CAS  Google Scholar 

  83. Wong RL, Walker CL (2013) Molecular pathways: environmental estrogens activate nongenomic signaling to developmentally reprogram the epigenome. Clin Cancer Res 19:3732–3737. https://doi.org/10.1158/1078-0432.CCR-13-0021

    Article  CAS  Google Scholar 

  84. Xiao X, Mruk DD, Tang EI, Wong CK, Lee WM, John CM, Turek PJ, Silvestrini B, Cheng CY (2014) Environmental toxicants perturb human Sertoli cell adhesive function via changes in F-actin organization mediated by actin regulatory proteins. Hum Reprod 29:1279–1291. https://doi.org/10.1093/humrep/deu011

    Article  CAS  Google Scholar 

  85. Zhang W, Cai Y, Sheng G, Chen D, Fu J (2011) Tissue distribution of decabrominated diphenyl ether (BDE-209) and its metabolites in sucking rat pups after prenatal and/or postnatal exposure. Toxicology 283:49–54. https://doi.org/10.1016/j.tox.2011.02.003

    Article  CAS  Google Scholar 

  86. Zhang X, Zhang K, Yang D, Ma L, Lei B, Zhang X, Zhou J, Fang X, Yu Y (2014) Polybrominated biphenyl ethers in breast milk and infant formula from Shanghai, China: temporal trends, daily intake, and risk assessment. Sci Total Environ 497-498:508–515. https://doi.org/10.1016/j.scitotenv.2014.08.034

    Article  CAS  Google Scholar 

  87. Zhang J, Wang Y, Zhou B, Sun KM, Tang X (2016) Reproductive effects of two polybrominated diphenyl ethers on the rotifer Brachionus plicatilis. Bull Environ Contam Toxicol 97:198–202. https://doi.org/10.1007/s00128-016-1832-5

    Article  CAS  Google Scholar 

  88. Zhao W, Cheng J, Gu J, Liu Y, Fujimura M, Wang W (2014) Assessment of neurotoxic effects and brain region distribution in rat offspring prenatally co-exposed to low doses of BDE-99 and methylmercury. Chemosphere 112:170–176. https://doi.org/10.1016/j.chemosphere.2014.04.011

    Article  CAS  Google Scholar 

  89. Zhou YJ, Xie X, Chen LM, Liang C, Wan Q, Chen GY, Tian Y (2013) Effect of maternal BDE-209 exposure on sexual development in male offspring rats. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 31:581–584

    CAS  Google Scholar 

Download references

Author information

Affiliations

Author notes

  1. Jinxia Zhai and Xiya Geng are Co-first authors

    Authors

    Corresponding author

    Correspondence to Jinxia Zhai.

    Additional information

    Responsible editor: Philippe Garrigues

    Electronic supplementary material

    ESM 1

    (DOCX 67 kb)

    Rights and permissions

    Reprints and Permissions

    About this article

    Verify currency and authenticity via CrossMark

    Cite this article

    Zhai, J., Geng, X., Ding, T. et al. An increase of estrogen receptor α protein level regulates BDE-209-mediated blood-testis barrier disruption during spermatogenesis in F1 mice. Environ Sci Pollut Res 26, 4801–4820 (2019). https://doi.org/10.1007/s11356-018-3784-2

    Download citation

    Keywords

    • BDE-209
    • MPP
    • Estrogen receptor α
    • Spermatogenesis
    • Reproductive and developmental toxicology