Archives of Toxicology

, Volume 92, Issue 6, pp 2013–2025 | Cite as

Corticosteroid-binding globulin, induced in testicular Leydig cells by perfluorooctanoic acid, promotes steroid hormone synthesis

Molecular Toxicology
  • 118 Downloads

Abstract

Perfluorooctanoic acid (PFOA) is an abundant perfluoroalkyl substance widely applied in industrial and consumer products. It is a ubiquitous environmental pollutant and suspected endocrine disruptor. Corticosteroid-binding globulin (CBG) is a monomeric glycoprotein that can bind specifically to anti-inflammatory steroids, such as glucocorticoids and progesterone, in circulation. Our previous proteomic profile analysis revealed that CBG levels increased in testes after PFOA treatment. In the present study, we verified its increase in mouse testes following oral exposure to PFOA (0, 1.25 and 5 mg/kg/day for 28 days) by immunohistochemical analysis and Western blotting. In addition, RNA fluorescence in situ hybridization (FISH) confirmed that testicular CBG was specifically expressed in Leydig cells. Serum CBG levels in all three PFOA groups also increased, accompanied by increased corticosterone in the 5 and 20 mg/kg/day groups and decreased adrenocorticotropic hormone in the 20 mg/kg/day group. Thus, the influence of PFOA on blood CBG may change free steroid hormone concentrations, thereby serving as an endocrine disruptor. A stimulation effect of PFOA on CBG was also observed in vitro using the Leydig tumor mLTC-1 cell line. Overexpression of CBG in mLTC-1 cells increased progesterone release in culture media. In addition, CBG-induced proteins involved in steroidogenesis in mLTC-1 cells, including steroidogenic acute regulatory protein (StAR), cytochrome P450 cholesterol side-chain cleavage enzyme (CYP11A1), 17α-hydroxylase/17,20 lyase (CYP17A1), and 3β-hydroxysteroid dehydrogenase (3β-HSD), which may be the mechanism behind increased progesterone. Furthermore, the production and release of CBG in mLTC-1 cells were also induced by luteinizing hormone, though this mechanism requires further exploration.

Keywords

Perfluorooctanoic acid Progesterone Leydig cell Corticosteroid-binding globulin 

Abbreviations

CYP17A1

17α-Hydroxylase/17,20 lyase

3β-HSD

3β-Hydroxysteroid dehydrogenase

ACTH

Adrenocorticotropic hormone

CBG

Corticosteroid-binding globulin

CRH

Corticotrophin-releasing hormone

CYP11A1

Cytochrome P450 cholesterol side-chain cleavage enzyme

HPA

Hypothalamic–pituitary–adrenal

LH

Luteinizing hormone

ORF

Open reading frame

PFASs

Perfluoroalkyl substances

PFOA

Perfluorooctanoate

RCL

Reactive center loop

StAR

Steroidogenic acute regulatory protein

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31320103915, 21737004, and 21377128). We thank Prof. Geoffrey L. Hammond from the Departments of Cellular and Physiological Sciences and Obstetrics and Gynaecology, University of British Columbia, Canada, for providing CBG antibodies.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdou HS, Bergeron F, Tremblay JJ (2014) A cell-autonomous molecular cascade initiated by AMP-activated protein kinase represses steroidogenesis. Mol Cell Biol 34(23):4257–4271.  https://doi.org/10.1128/Mcb.00734-14 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Averina M, Brox J, Huber S, Furberg AS (2018) Perfluoroalkyl substances in adolescents in northern Norway: lifestyle and dietary predictors. The Tromso study, Fit Futures 1. Environ Int 114:123–130.  https://doi.org/10.1016/j.envint.2018.02.031 CrossRefPubMedGoogle Scholar
  3. Avvakumov GV, Hammond GL (1994) Glycosylation of human corticosteroid-binding globulin—differential processing and significance of carbohydrate chains at individual sites. Biochemistry 33(19):5759–5765.  https://doi.org/10.1021/bi00185a012 CrossRefPubMedGoogle Scholar
  4. Avvakumov GV, Strelchyonok OA (1987) Properties and serum levels of pregnancy-associated variant of human transcortin. Biochim Biophys Acta 925(1):11–16.  https://doi.org/10.1016/0304-4165(87)90142-5 CrossRefPubMedGoogle Scholar
  5. Avvakumov GV, Warmelsrodenhiser S, Hammond GL (1993) Glycosylation of human corticosteroid-binding globulin at asparagine-238 is necessary for steroid binding. J Biol Chem 268(2):862–866PubMedGoogle Scholar
  6. Barry V, Winquist A, Steenland K (2013) Perfluorooctanoic acid (PFOA) exposures and incident cancers among adults living near a chemical plant. Environ Health Perspect 121(11–12):1313–1318.  https://doi.org/10.1289/ehp.1306615 PubMedPubMedCentralGoogle Scholar
  7. Benassayag C, Souski I, Mignot TM et al (2001) Corticosteroid-binding globulin status at the fetomaternal interface during human term pregnancy. Biol Reprod 64(3):812–821.  https://doi.org/10.1095/biolreprod64.3.812 CrossRefPubMedGoogle Scholar
  8. Biegel LB, Liu RC, Hurtt ME, Cook JC (1995) Effects of ammonium perfluorooctanoate on Leydig cell function: in vitro, in vivo, and ex vivo studies. Toxicol Appl Pharmacol 134(1):18–25.  https://doi.org/10.1006/taap.1995.1164 CrossRefPubMedGoogle Scholar
  9. Biegel LB, Hurtt ME, Frame SR, O’Connor JC, Cook JC (2001) Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicol Sci 60(1):44–55.  https://doi.org/10.1093/toxsci/60.1.44 CrossRefPubMedGoogle Scholar
  10. Brunner E, Baima J, Vieira TC, Vieira JGH, Abucham J (2003) Hereditary corticosteroid-binding globulin deficiency due to a missense mutation (Asp367Asn, CBG Lyon) in a Brazilian kindred. Clin Endocrinol 58(6):756–762.  https://doi.org/10.1046/j.1365-2265.2003.01783.x CrossRefGoogle Scholar
  11. Butenhoff JL, Gaylor DW, Moore JA et al (2004) Characterization of risk for general population exposure to perfluorooctanoate. Regul Toxicol Pharmacol 39(3):363–380.  https://doi.org/10.1016/j.yrtph.2004.03.003 CrossRefPubMedGoogle Scholar
  12. Calafat AM, Wong LY, Kuklenyik Z, Reidy JA, Needham LL (2007) Polyfluoroalkyl chemicals in the U.S. population: data from the National Health and Nutrition Examination Survey (NHANES) 2003–2004 and comparisons with NHANES 1999–2000. Environ Health Perspect 115(11):1596–1602.  https://doi.org/10.1289/ehp.10598 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Caldwell JD, Jirikowski GF (2014) Sex hormone binding globulin and corticosteroid binding globulin as major effectors of steroid action. Steroids 81:13–16.  https://doi.org/10.1016/j.steroids.2013.11.010 CrossRefPubMedGoogle Scholar
  14. Castiglioni S, Valsecchi S, Polesello S et al (2015) Sources and fate of perfluorinated compounds in the aqueous environment and in drinking water of a highly urbanized and industrialized area in Italy. J Hazard Mater 282:51–60.  https://doi.org/10.1016/j.jhazmat.2014.06.007 CrossRefPubMedGoogle Scholar
  15. Dallman MF, Pecoraro NC, La Fleur SE et al (2006) Glucocorticoids, chronic stress, and obesity. Prog Brain Res 153:75–105.  https://doi.org/10.1016/S0079-6123(06)53004-3 CrossRefPubMedGoogle Scholar
  16. Emptoz-Bonneton A, Cousin P, Seguchi K et al (2000) Novel human corticosteroid-binding globulin variant with low cortisol-binding affinity. J Clin Endocr Metab 85(1):361–367.  https://doi.org/10.1210/jc.85.1.361 PubMedGoogle Scholar
  17. Feldman D, Mondon CE, Horner JA, Weiser JN (1979) Glucocorticoid and estrogen regulation of corticosteroid-binding globulin production by rat-liver. Am J Physiol 237(6):E493–E499.  https://doi.org/10.1152/ajpendo.1979.237.6.E493 PubMedGoogle Scholar
  18. Fernandez-Real JM, Grasa M, Casamitjana R, Pugeat M, Barret C, Ricart W (1999) Plasma total and glycosylated corticosteroid-binding globulin levels are associated with insulin secretion. J Clin Endocr Metab 84(9):3192–3196.  https://doi.org/10.1210/jc.84.9.3192 CrossRefPubMedGoogle Scholar
  19. Fernandez-Real JM, Grasa M, Casamitjana R, Ricart W (2000) The insulin resistance syndrome and the binding capacity of cortisol binding globulin (CBG) in men and women. Clin Endocrinol 52(1):93–99.  https://doi.org/10.1046/j.1365-2265.2000.00864.x CrossRefGoogle Scholar
  20. Fernandez-Real JM, Pugeat M, Emptoz-Bonneton A, Ricart W (2001) Study of the effect of changing glucose, insulin, and insulin-like growth factor-I levels on serum corticosteroid binding globulin in lean, obese, and obese subjects with glucose intolerance. Metab Clin Exp 50(10):1248–1252.  https://doi.org/10.1053/meta.2001.25647 CrossRefPubMedGoogle Scholar
  21. Fernandez-Real J, Pugeat M, Grasa M et al (2002) Serum corticosteroid-binding globulin (CBG) concentration and insulin resistance syndrome: a population study. J Clin Endocrinol 87(10):4686–4690.  https://doi.org/10.1210/jc.2001-011843 CrossRefGoogle Scholar
  22. Fernandez-Real JM, Pugeat M, Lopez-Bermejo A, Bornet H, Ricart W (2005) Corticosteroid-binding globulin affects the relationship between circulating adiponectin and cortisol in men and women. Metab Clin Exp 54(5):584–589.  https://doi.org/10.1016/j.metabol.2004.11.015 CrossRefPubMedGoogle Scholar
  23. Fleshner M, Deak T, Spencer RL, Laudenslager ML, Watkins LR, Maier SF (1995) A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136(12):5336–5342.  https://doi.org/10.1210/en.136.12.5336 CrossRefPubMedGoogle Scholar
  24. Gagliardi L, Ho JT, Torpy DJ (2010) Corticosteroid-binding globulin: the clinical significance of altered levels and heritable mutations. Mol Cell Endocrinol 316(1):24–34.  https://doi.org/10.1016/j.mce.2009.07.015 CrossRefPubMedGoogle Scholar
  25. Garrel DR (1996) Corticosteroid-binding globulin during inflammation and burn injury: nutritional modulation and clinical implications. Horm Res 45(3–5):245–251.  https://doi.org/10.1159/000184796 CrossRefPubMedGoogle Scholar
  26. Gulfo J, Ledda A, Gea-Sorli S et al (2016) New roles for corticosteroid binding globulin and opposite expression profiles in lung and liver. PloS One 11(1):e0146497.  https://doi.org/10.1371/journal.pone.0146497 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hammond GL (1990) Molecular-properties of corticosteroid binding globulin and the sex-steroid binding-proteins. Endocr Rev 11(1):65–79.  https://doi.org/10.1210/edrv-11-1-65 CrossRefPubMedGoogle Scholar
  28. Hammond GL, Smith CL, Goping IS et al (1987) Primary structure of human corticosteroid binding globulin, deduced from hepatic and pulmonary cdnas, exhibits homology with serine protease inhibitors. Proc Natl Acad Sci USA 84(15):5153–5157.  https://doi.org/10.1073/pnas.84.15.5153 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hammond GL, Smith CL, Underhill DA (1991) Molecular studies of corticosteroid binding globulin structure, biosynthesis and function. J Steroid Biochem 40(4–6):755–762.  https://doi.org/10.1016/0960-0760(91)90300-T CrossRefGoogle Scholar
  30. Hampl R, Kubatova J, Starka L (2016) Steroids and endocrine disruptors—history, recent state of art and open questions. J Steroid Biochem 155:217–223.  https://doi.org/10.1016/j.jsbmb.2014.04.013 CrossRefGoogle Scholar
  31. Henley DE, Lightman SL (2011) New insights into corticosteroid-binding globulin and glucocorticoid delivery. Neuroscience 180:1–8.  https://doi.org/10.1016/j.neuroscience.2011.02.053 CrossRefPubMedGoogle Scholar
  32. Hill LA, Vassiliadi DA, Simard M et al (2012) Two different corticosteroid-binding globulin variants that lack cortisol-binding activity in a Greek woman. J Clin Endocr Metab 97(11):4260–4267.  https://doi.org/10.1210/jc.2012-2467 CrossRefPubMedGoogle Scholar
  33. Hoke RA, Ferrell BD, Ryan T et al (2015) Aquatic hazard, bioaccumulation and screening risk assessment for 6:2 fluorotelomer sulfonate. Chemosphere 128:258–265.  https://doi.org/10.1016/j.chemosphere.2015.01.033 CrossRefPubMedGoogle Scholar
  34. Hryb DJ, Khan MS, Romas NA, Rosner W (1986) Specific binding of human corticosteroid-binding globulin to cell-membranes. Proc Natl Acad Sci USA 83(10):3253–3256.  https://doi.org/10.1073/pnas.83.10.3253 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Joensen UN, Bossi R, Leffers H, Jensen AA, Skakkebaek NE, Jorgensen N (2009) Do perfluoroalkyl compounds impair human semen quality? Environ Health Perspect 117(6):923–927.  https://doi.org/10.1289/ehp.0800517 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kennedy GL Jr, Butenhoff JL, Olsen GW et al (2004) The toxicology of perfluorooctanoate. Crit Rev Toxicol 34(4):351–384.  https://doi.org/10.1080/10408440490464705 CrossRefPubMedGoogle Scholar
  37. Kim JM, Ghosh SR, Weil AC, Zirkin BR (2001) Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinology 142(9):3809–3816.  https://doi.org/10.1210/endo.142.9.8375 CrossRefPubMedGoogle Scholar
  38. Klaunig JE, Hocevar BA, Kamendulis LM (2012) Mode of action analysis of perfluorooctanoic acid (PFOA) tumorigenicity and human relevance. Reprod Toxicol 33(4):410–418.  https://doi.org/10.1016/j.reprotox.2011.10.014 CrossRefPubMedGoogle Scholar
  39. Klieber MA, Underhill C, Hammond GL, Muller YA (2007) Corticosteroid-binding globulin, a structural basis for steroid transport and proteinase-triggered release. J Biol Chem 282(40):29594–29603.  https://doi.org/10.1074/jbc.M705014200 CrossRefPubMedGoogle Scholar
  40. Kumsta R, Entringer S, Hellhammer DH, Wust S (2007) Cortisol and ACTH responses to psychosocial stress are modulated by corticosteroid binding globulin levels. Psychoneuroendocrinology 32(8–10):1153–1157.  https://doi.org/10.1016/j.psyneuen.2007.08.007 CrossRefPubMedGoogle Scholar
  41. Lau C, Butenhoff JL, Rogers JM (2004) The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol Appl Pharmacol 198(2):231–241.  https://doi.org/10.1016/j.taap.2003.11.031 CrossRefPubMedGoogle Scholar
  42. Lau C, Anitole K, Hodes C, Lai D, Pfahles-Hutchens A, Seed J (2007) Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci 99(2):366–394.  https://doi.org/10.1093/toxsci/kfm128 CrossRefPubMedGoogle Scholar
  43. Lewis JG, Elder PA (2011) Corticosteroid-binding globulin reactive centre loop antibodies recognise only the intact natured protein: elastase cleaved and uncleaved CBG may coexist in circulation. J Steroid Biochem 127(3–5):289–294.  https://doi.org/10.1016/j.jsbmb.2011.08.006 CrossRefGoogle Scholar
  44. Lewis JG, Lewis MG, Elder PA (2003) An enzyme-linked immunosorbent assay for corticosteroid-binding globulin using monoclonal and polyclonal antibodies: decline in CBG following synthetic ACTH. Clin Chim Acta 328(1–2):121–128.  https://doi.org/10.1016/S0009-8981(02)00417-5 CrossRefPubMedGoogle Scholar
  45. Lin HY, Muller YA, Hammond GL (2010) Molecular and structural basis of steroid hormone binding and release from corticosteroid-binding globulin. Mol Cell Endocrinol 316(1):3–12.  https://doi.org/10.1016/j.mce.2009.06.015 CrossRefPubMedGoogle Scholar
  46. Lin HY, Underhill C, Lei JH et al (2012) High frequency of SERPINA6 polymorphisms that reduce plasma corticosteroid-binding globulin activity in chinese subjects. J Clin Endocr Metab 97(4):E678–E686.  https://doi.org/10.1210/jc.2011-3141 CrossRefPubMedGoogle Scholar
  47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(− Delta Delta C) method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  48. Mattos GE, Heinzmann JM, Norkowski S et al (2013) Corticosteroid-binding globulin contributes to the neuroendocrine phenotype of mice selected for extremes in stress reactivity. J Endocrinol 219(3):217–229.  https://doi.org/10.1530/Joe-13-0255 CrossRefPubMedGoogle Scholar
  49. Mendel CM (1989) The free hormone hypothesis—a physiologically based mathematical-model. Endocr Rev 10(3):232–274.  https://doi.org/10.1210/edrv-10-3-232 CrossRefPubMedGoogle Scholar
  50. Misao R, Hori M, Ichigo S, Fujimoto J, Tamaya T (1994) Corticosteroid-binding globulin mRNA levels in human uterine endometrium. Steroids 59(10):603–607.  https://doi.org/10.1016/0039-128X(94)90055-8 CrossRefPubMedGoogle Scholar
  51. Neufeld JH, Breen L, Hauger R (1994) Extreme posture elevates corticosterone in a forced ambulation model of chronic stress in rats. Pharmacol Biochem Behav 47(2):233–240.  https://doi.org/10.1016/0091-3057(94)90005-1 CrossRefPubMedGoogle Scholar
  52. Olsen GW, Zobel LR (2007) Assessment of lipid, hepatic, and thyroid parameters with serum perfluorooctanoate (PFOA) concentrations in fluorochemical production workers. Int Arch Occup Environ Health 81(2):231–246.  https://doi.org/10.1007/s00420-007-0213-0 CrossRefPubMedGoogle Scholar
  53. Olsen GW, Burris JM, Ehresman DJ et al (2007) Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect 115(9):1298 – 305.  https://doi.org/10.1289/ehp.10009 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Olsen GW, Butenhoff JL, Zobel LR (2009) Perfluoroalkyl chemicals and human fetal development: an epidemiologic review with clinical and toxicological perspectives. Reprod Toxicol 27(3–4):212–230.  https://doi.org/10.1016/j.reprotox.2009.02.001 CrossRefPubMedGoogle Scholar
  55. Payne AH, Youngblood GL (1995) Regulation of expression of steroidogenic enzymes in Leydig-cells. Biol Reprod 52(2):217–225.  https://doi.org/10.1095/biolreprod52.2.217 CrossRefPubMedGoogle Scholar
  56. Pemberton PA, Stein PE, Pepys MB, Potter JM, Carrell RW (1988) Hormone binding globulins undergo serpin conformational change in inflammation. Nature 336(6196):257–258.  https://doi.org/10.1038/336257a0 CrossRefPubMedGoogle Scholar
  57. Perogamvros I, Underhill C, Henley DE et al (2010) Novel corticosteroid-binding globulin variant that lacks steroid binding activity. J Clin Endocr Metab 95(10):E142–E150.  https://doi.org/10.1210/jc.2010-0746 CrossRefPubMedGoogle Scholar
  58. Petersen HH, Andreassen TK, Breiderhoff T et al (2006) Hyporesponsiveness to glucocorticoids in mice genetically deficient for the corticosteroid binding globulin. Mol Cell Biol 26(19):7236–7245.  https://doi.org/10.1128/Mcb.00400-06 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Prevedouros K, Cousins IT, Buck RC, Korzeniowski SH (2006) Sources, fate and transport of perfluorocarboxylates. Environ Sci Technol 40(1):32–44.  https://doi.org/10.1021/es0512475 CrossRefPubMedGoogle Scholar
  60. Qian XX, Droste SK, Gutierrez-Mecinas M et al (2011) A rapid release of corticosteroid-binding globulin from the liver restrains the glucocorticoid hormone response to acute stress. Endocrinology 152(10):3738–3748.  https://doi.org/10.1210/en.2011-1008 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Raymer JH, Michael LC, Studabaker WB et al (2012) Concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) and their associations with human semen quality measurements. Reprod Toxicol 33(4):419–427.  https://doi.org/10.1016/j.reprotox.2011.05.024 CrossRefPubMedGoogle Scholar
  62. Rebois RV (1982) Establishment of gonadotropin-responsive murine Leydig tumor-cell line. J Cell Biol 94(1):70–76.  https://doi.org/10.1083/jcb.94.1.70 CrossRefPubMedGoogle Scholar
  63. Richard EM, Helbling JC, Tridon C et al (2010) Plasma transcortin influences endocrine and behavioral stress responses in mice. Endocrinology 151(2):649–659.  https://doi.org/10.1210/en.2009-0862 CrossRefPubMedGoogle Scholar
  64. Robinson PA, Langley MS, Hammond GL (1985) A solid-phase radioimmunoassay for human corticosteroid binding globulin. J Endocrinol 104(2):259–267.  https://doi.org/10.1677/joe.0.1040259 CrossRefPubMedGoogle Scholar
  65. Savu L, Zouaghi H, Carli A, Nunez EA (1981) Serum depletion of corticosteroid binding activities, an early marker of human septic shock. Biochem Biophys Res Commun 102(1):411–419.  https://doi.org/10.1016/0006-291x(81)91536-9 CrossRefPubMedGoogle Scholar
  66. Shi Z, Zhang H, Liu Y, Xu M, Dai J (2007) Alterations in gene expression and testosterone synthesis in the testes of male rats exposed to perfluorododecanoic acid. Toxicol Sci 98(1):206–215.  https://doi.org/10.1093/toxsci/kfm070 CrossRefPubMedGoogle Scholar
  67. Sinha Hikim AP, Rajavashisth TB, Sinha Hikim I et al (1997) Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol Reprod 57(5):1193–1201.  https://doi.org/10.1095/biolreprod57.5.1193 CrossRefPubMedGoogle Scholar
  68. Smith CL, Hammond GL (1992) Hormonal-regulation of corticosteroid-binding globulin biosynthesis in the male-rat. Endocrinology 130(4):2245–2251.  https://doi.org/10.1210/en.130.4.2245 PubMedGoogle Scholar
  69. Spencer RL, Miller AH, Moday H et al (1996) Chronic social stress produces reductions in available splenic type II corticosteroid receptor binding and plasma corticosteroid binding globulin levels. Psychoneuroendocrinology 21(1):95–109.  https://doi.org/10.1016/0306-4530(95)00020-8 CrossRefPubMedGoogle Scholar
  70. Sumer-Bayraktar Z, Kolarich D, Campbell MP, Ali S, Packer NH, Thaysen-Andersen M (2011) N-glycans modulate the function of human corticosteroid-binding globulin. Mol Cell Proteom 10(8)  https://doi.org/10.1074/mcp.M111.009100
  71. Torpy DJ, Bachmann AW, Grice JE et al (2001) Familial corticosteroid-binding globulin deficiency due to a novel null mutation: association with fatigue and relative hypotension. J Clin Endocr Metab 86(8):3692–3700.  https://doi.org/10.1210/jc.86.8.3692 CrossRefPubMedGoogle Scholar
  72. Tucker DK, Macon MB, Strynar MJ, Dagnino S, Andersen E, Fenton SE (2015) The mammary gland is a sensitive pubertal target in CD-1 and C57Bl/6 mice following perinatal perfluorooctanoic acid (PFOA) exposure. Reprod Toxicol 54:26–36.  https://doi.org/10.1016/j.reprotox.2014.12.002 CrossRefPubMedGoogle Scholar
  73. US EPA UEPA (2016) PFOA Stewardship ProgramGoogle Scholar
  74. Verhoog N, Allie-Reid F, Berghe WV et al (2014) Inhibition of corticosteroid-binding globulin gene expression by glucocorticoids involves C/EBP beta. PloS one 9(10):e110702.  https://doi.org/10.1371/journal.pone.0110702 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Vested A, Ramlau-Hansen CH, Olsen SF et al (2013) Associations of in utero exposure to perfluorinated alkyl acids with human semen quality and reproductive hormones in adult men. Environ Health Perspect 121(4):453–458.  https://doi.org/10.1289/ehp.1205118 458e1-5PubMedPubMedCentralGoogle Scholar
  76. Wang N, Szostek B, Buck RC, Folsom PW, Sulecki LM, Gannon JT (2009) 8-2 Fluorotelomer alcohol aerobic soil biodegradation: pathways, metabolites, and metabolite yields. Chemosphere 75(8):1089–1096.  https://doi.org/10.1016/j.chemosphere.2009.01.033 CrossRefPubMedGoogle Scholar
  77. Wang J, Yan S, Zhang W, Zhang H, Dai J (2015) Integrated proteomic and miRNA transcriptional analysis reveals the hepatotoxicity mechanism of PFNA exposure in mice. J Proteome Res 14(1):330–341.  https://doi.org/10.1021/pr500641b CrossRefPubMedGoogle Scholar
  78. White SS, Calafat AM, Kuklenyik Z et al (2007) Gestational PFOA exposure of mice is associated with altered mammary gland development in dams and female offspring. Toxicol Sci 96(1):133–144.  https://doi.org/10.1093/toxsci/kfl177 CrossRefPubMedGoogle Scholar
  79. White SS, Fenton SE, Hines EP (2011) Endocrine disrupting properties of perfluorooctanoic acid. J Steroid Biochem Mol Biol 127(1–2):16–26.  https://doi.org/10.1016/j.jsbmb.2011.03.011 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Willach S, Brauch HJ, Lange FT (2016) Contribution of selected perfluoroalkyl and polyfluoroalkyl substances to the adsorbable organically bound fluorine in German rivers and in a highly contaminated groundwater. Chemosphere 145:342–350.  https://doi.org/10.1016/j.chemosphere.2015.11.113 CrossRefPubMedGoogle Scholar
  81. Willnow TE, Nykjaer A (2010) Cellular uptake of steroid carrier proteins—mechanisms and implications. Mol Cell Endocrinol 316(1):93–102.  https://doi.org/10.1016/j.mce.2009.07.021 CrossRefPubMedGoogle Scholar
  82. Yan S, Wang J, Zhang W, Dai J (2014) Circulating microRNA profiles altered in mice after 28 d exposure to perfluorooctanoic acid. Toxicol Lett 224(1):24–31.  https://doi.org/10.1016/j.toxlet.2013.10.017 CrossRefPubMedGoogle Scholar
  83. Young KA, Nelson RJ (2001) Mediation of seasonal testicular regression by apoptosis. Reproduction 122(5):677–685.  https://doi.org/10.1530/rep.0.1220677 CrossRefPubMedGoogle Scholar
  84. Zhang H, Lu Y, Luo B, Yan S, Guo X, Dai J (2014) Proteomic analysis of mouse testis reveals perfluorooctanoic acid-induced reproductive dysfunction via direct disturbance of testicular steroidogenic machinery. J Proteome Res 13(7):3370–3385.  https://doi.org/10.1021/pr500228d CrossRefPubMedGoogle Scholar
  85. Zhao B, Chu Y, Hardy DO, Li XK, Ge RS (2010) Inhibition of 3beta- and 17beta-hydroxysteroid dehydrogenase activities in rat Leydig cells by perfluorooctane acid. J Steroid Biochem Mol Biol 118(1–2):13–17.  https://doi.org/10.1016/j.jsbmb.2009.09.010 CrossRefPubMedGoogle Scholar
  86. Zhao W, Cui RN, Wang JH, Dai JY (2017) Inhibition effects of perfluoroalkyl acids on progesterone production in mLTC-1. J Environ Sci 56:272–280.  https://doi.org/10.1016/j.jes.2016.08.026 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Animal Ecology and Conservation Biology, Institute of ZoologyChinese Academy of SciencesBeijingPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations