Effects of n-butylparaben on steroidogenesis and spermatogenesis through changed E2 levels in male rat offspring

Environmental Toxicology and Pharmacology

Volumn 37, Issue 2, 2014, Pages 705-717

  Zhang, Linyuan ^a   Dong, Li ^a   Ding, Sijin ^a   Qiao, Peihuan ^a   Wang, Chong ^a   Zhang, Ming ^a   Zhang, Lixia ^a   Du, Qingcheng ^a   Li, Yimin ^a   Tang, Ning ^a   Chang, Bing ^a  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Endocrine disrupting chemicals; Oestrogene; Parabens; Reproduction; Testosterone

Indexed keywords

BUTYL PARABEN; ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE; TESTOSTERONE; 4 HYDROXYBENZOIC ACID ESTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOGENITAL DISTANCE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; EPIDIDYMIS; ESTRADIOL BLOOD LEVEL; FEMALE; FOLLITROPIN BLOOD LEVEL; GESTATIONAL AGE; LUTEINIZING HORMONE BLOOD LEVEL; MALE; MALE GENITAL SYSTEM; NONHUMAN; PERINATAL PERIOD; PREPUTIAL GLAND; PRIORITY JOURNAL; PROGENY; RAT; REPRODUCTIVE TOXICITY; SEMINAL VESICLE; SPERMATOGENESIS; SPERMATOZOON COUNT; STEROIDOGENESIS; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL; ANIMAL; BLOOD; DRUG EFFECTS; FETOMATERNAL TRANSFUSION; ORGAN SIZE; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE; TESTIS; TOXICITY; WISTAR RAT;

ANIMALS; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; LUTEINIZING HORMONE; MALE; MATERNAL-FETAL EXCHANGE; ORGAN SIZE; PARABENS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, WISTAR; SPERM COUNT; SPERMATOGENESIS; TESTIS; TESTOSTERONE;

EID: 84895426786     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2014.01.016     Document Type: Article

References (87)

1. Atanassova N., McKinnell C., Walker M., Turner K., Fisher J., Morley M., Millar M., Groome N., Sharpe R. Permanent effects of neonatal estrogen exposure in rats on reproductive hormone levels, Sertoli cell number, and the efficiency of spermatogenesis in adulthood. Endocrinology 1999, 140:5364-5373.
2. Atanassova N.N., Walker M., McKinnell C., Fisher J.S., Sharpe R.M. Evidence that androgens and oestrogens, as well as follicle-stimulating hormone, can alter Sertoli cell number in the neonatal rat. J. Endocrinol. 2005, 184:107-117.
3. 2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology 2011, 152:562-1571.
4. Bethea C.L., Fahrenbach W.H., Sprangers S.A., Freesh F. Immunocytochemical localization of progestin receptors in monkey hypothalamus: effect of estrogen and progestin. Endocrinology 1992, 130:895-905.
5. Boberg J., Taxvig C., Christiansen S., Hass U. Update on Uptake, Distribution, Metabolism and Excretion (ADME) and Endocrine Disrupting Activity of Parabens 2009, http://www.mst.dk/NR/rdonlyres/1D32086E-65A4-4B2C-B74F-6A6C6753DBB7/0/Updateonuptakedistributionmetabolismandexcretion_ADME_.pdf.
6. Boberg J., Taxvig C., Christiansen S., Hass U. Possible endocrine disrupting effects of parabens and their metabolites. Reprod. Toxicol. 2010, 30(2):301-312.
7. Berger T., Conley A.J., Van Klompenberg M., Roser J.F., Hovey R.C. Increased testicular Sertoli cell population induced by an estrogen receptor antagonist. Mol. Cell. Endocrinol. 2013, 366(1):53-58.
8. Carreau S., Bouraima-Lelong H., Delalande C. Estrogens: new players in spermatogenesis. Reprod. Biol. 2011, 11:174-193.
9. Chen J., Ahn K.C., Gee N.A., Gee S.J., Hammock B.D., Lasley B.L. Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicol. Appl. Pharmacol. 2007, 221(3):278-284.
10. Christiansen S., Scholze M., Dalgaard M., Vinggaard A.M., Axelstad M., Kortenkamp A., Hass U. Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ. Health Perspect. 2009, 117:1839-1846.
11. Cook J.C., Johnson L., O'Connor J.C., Biegel L.B., Krams C.H., Frame S.R., Hurtt M.E. Effects of dietary 17β-estradiol exposure on serum hormone concentrations and testicular parameters in male Crl: CD BR rats. Toxicological Sciences 1998, 44:155-168.
12. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20:358-417.
13. Darbre P.D., Aljarrah A., Miller W.R., Coldham N.G., Sauer M.J., Pope G.S. Concentrations of parabens in human breast tumours. J. Appl. Toxicol. 2004, 24:5-13.
14. Daston G.P. Developmental toxicity evaluation of butylparaben in Sprague-Dawley rats. Birth Defects Res. B: Dev. Reprod. Toxicol. 2004, 71(4):296-302.
15. DeGroot L.J. Endocrinology 1995, W.B. Saunders Company, Philadelphia, PA. third ed.
16. Eddy E.M., Washburn T.F., Bunch D.O., Goulding E.H., Gladen B.C., Lubahn D.B., Korach K.S. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 1996, 137:4796-4805.
17. EFSA Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the commission related to parahydroxybenzoates (E214-219). EFSA J. 2004, 83:1-26.
18. El-Kashoury A.A., Salama A.F., Selim A.I., Mohamed R.A. Animal model study of reproductive toxicity of the chronic exposure of dicofol. Life Sci. J. 2009, 6:1-18.
19. El Hussein S., Muret P., Berard M., Makki S., Humbert P. Assessment of principal parabens used in cosmetics after their passage through human epidermis-dermis layers (ex-vivo study). Exp. Dermatol. 2007, 16:830-836.
20. Fisher J.S., Turner K.J., Brown D., Sharpe R.M. Effect of neonatal exposure to estrogenic compounds on development of the excurrent ducts of the rat testis through puberty to adulthood. Environ. Health Perspect. 1999, 107:397-405.
21. Gill W.B., Schumacher G.F., Bibbo M., Straus F.H., Schoenberg H.W. Association of diethylstilbestrol exposure in utero with cryptorchidism, testicular hypoplasia and semen abnormalities. J. Urol. 1979, 122:36-39.
22. Goyal H., Braden T., Mansour M., Williams C., Kamaleldin A., Srivastava K. Diethylstilbestrol-treated adult rats with altered epididymal sperm numbers and sperm motility parameters, but without alterations in sperm production and sperm morphology. Biol. Reprod. 2001, 64:927-934.
23. Goyal H., Robateau A., Braden T., Williams C., Srivastava K., Ali K. Neonatal estrogen exposure of male rats alters reproductive functions at adulthood. Biol. Reprod. 2003, 68:2081-2091.
24. Gray L.E., Ostby J.S., Kelce W.R. A dose-response analysis of the reproductive effects of a single gestational dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin in male Long Evans Hooded rat offspring. Toxicol. Appl. Pharmacol. 1997, 146:11-20.
25. Griswold M.D. The central role of Sertoli cells in spermatogenesis. Semin. Cell Dev. Biol. 1998, 9:411-416.
26. Haave M., Bernhard A., Jellestad F.K., Heegaard E., Brattelid T., Lundebye A.K. Long-term effects of environmentally relevant doses of 2,2',4,4',5,5'-hexachlorobiphenyl (PCB153) on neurobehavioural development, health and spontaneous behaviour in maternally exposed mice. Behav. Brain Funct. 2011, 7:3.
27. Heikinheimo O., Mahony M.C., Gordon K., Hsiu J.G., Hodgen G.D., Gibbons W.E. Estrogen and progesterone receptor mRNA are expressed in distinct pattern in male primate reproductive organs. J. Assist. Reprod. Genet. 1995, 12:198-204.
28. Hess R.A. Oestrogen in fluid transport in efferent ducts of the male reproductive tract. Rev. Reprod. 2000, 5:84-92.
29. Hess R.A. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 2003, 1:52.
30. Hess R.A., Bunick D., Lee K.H., Bahr J., Taylor J.A., Korach K.S., Lubahn D.B. A role for oestrogens in the male reproductive system. Nature 1997, 390:509-512.
31. Hoberman A.M., Schreur D.K., Leazer T., Daston G.P., Carthew P., Re T., Loretz L., Mann P. Lack of effect of butylparaben and methylparaben on the reproductive system in male rats. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:123-133.
32. Holson R.R., Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol. Teratol. 1992, 14:221-228.
33. Janjua N.R., Frederiksen H., Skakkebaek N.E., Wulf H.C., Andersson A.M. Urinary excretion of phthalates and paraben after repeated whole-body topical application in humans. Int. J. Androl. 2008, 31:118-130.
34. Janjua N.R., Mortensen G.K., Andersson A.M., Kongshoj B., Skakkebaek N.E., Wulf H.C. Systemic uptake of diethyl phthalate, dibutyl phthalate, and butyl paraben following whole-body topical application and reproductive and thyroid hormone levels in humans. Environ. Sci. Technol. 2007, 41:5564-5570.
35. Jayle M.F., Scholler R., Sfikakis A., Heron M. Excretion of phenol steroids and 17-ketosteroids after the administration of chorionic gonadotropins to men. Clin. Chim. Acta 1962, 7:212-220.
36. Jensen T.K., Toppari J., Keiding N., Skakkebaek N.E. Do environmental estrogens contribute to the decline in male reproductive health?. Clin. Chem. 1995, 41:1896-1901.
37. Kang K.S., Che J.H., Ryu D.Y., Kim T.W., Li G.X., Lee Y.S. Decreased sperm number and motile activity on the F1 offspring maternally exposed to butyl p-hydroxybenzoic acid (butyl paraben). J. Vet. Med. Sci. 2002, 64:227-235.
38. Kleymenova E., Swanson C., Boekelheide K., Gaido K.W. Exposure in utero to di (n-butyl) phthalate alters the vimentin cytoskeleton of fetal rat Sertoli cells and disrupts Sertoli cell-gonocyte contact. Biol. Reprod. 2005, 73:482-490.
39. Knobil E., Neill J.D. The Physiology of Reproduction 1994, New York Raven Press, NY. second ed.
40. Korach K.S. Insights from the study of animals lacking functional estrogen receptor. Science 1994, 266:1524-1527.
41. Lau C., Klinefelter G., Cameron A.M. Reproductive development and functions in the rat after repeated maternal deprivation stress. Fundam. Appl. Toxicol. 1996, 30:298-301.
42. Lee K.H., Hess R.A., Bahr J.M., Lubahn D.B., Taylor J., Bunick D. Estrogen receptor alpha has a functional role in the mouse rete testis and efferent ductules. Biol. Reprod. 2000, 63:1873-1880.
43. Lemini C., Jaimez R., Avila M.E., Franco Y., Larrea F., Lemus A.E. In vivo and in vitro estrogen bioactivities of alkyl parabens. Toxicol. Ind. Health 2003, 19:69-79.
44. Li X., Nokkala E., Yan W., Streng T., Saarinen N., Wärri A., Huhtaniemi I., Santti R., Mäkelä S., Poutanen M. Altered structure and function of reproductive organs in transgenic male mice overexpressing human aromatase. Endocrinology 2001, 142:2435-2442.
45. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. PNAS 1993, 90:11162-11166.
46. Luetjens C.M., Didolkar A., Kliesch S., Paulus W., Jeibmann A., Bocker W., Nieschlag E., Simoni M. Tissue expression of the nuclear progesterone receptor in male non-human primates and men. J. Endocrinol. 2006, 189:529-539.
47. McLachlan J.A., Newbold R.R., Bullock B. Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol. Science 1975, 190:991-992.
48. McLachlan J.A., Newbold R.R., Burow M.E., Li S.F. From malformations to molecular mechanisms in the male: three decades of research on endocrine disrupters. APMIS 2001, 109:263-272.
49. Meachem S., Von Schonfeldt V., Schlatt S. Spermatogonia: stem cells with a great perspective. Reproduction 2001, 121:825-834.
50. Nakamura D., Yanagiba Y., Duan Z., Ito Y., Okamura A., Asaeda N., Tagawa Y., Li C., Taya K., Zhang S.-Y. Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicol. Lett. 2010, 194:16-25.
51. O'Connor J.C., Frame S.R., Ladics G.S. Evaluation of a 15-day screening assay using intact male rats for identifying antiandrogens. Toxicol. Sci. 2002, 69:92-108.
52. O'Donnell L., Meachem S.J., Stanton P.G., McLachlan R.I. Chapter 21-Endocrine regulation of spermatogenesis. Knobil and Neill's Physiology of Reproduction 2006, 1:1039-1044. Academic Press, SanDiego. third ed.
53. O'donnell L., Robertson K.M., Jones M.E., Simpson E.R. Estrogen and spermatogenesis. Endocr. Rev. 2001, 22:289-318.
54. Oishi S. Effects of butylparaben on the male reproductive system in rats. Toxicol. Ind. Health 2001, 17:31-39.
55. Oishi S. Effects of propyl paraben on the male reproductive system. Food Chem. Toxicol. 2002, 40:1807-1813.
56. Oishi S. Effects of butyl paraben on the male reproductive system in mice. Arch. Toxicol. 2002, 76:423-429.
57. Page S.T., Amory J.K., Bremner W.J. Advances in male contraception. Endocr. Rev. 2008, 29:465-493.
58. Piegorsch W.W., Haseman J.K. Statistical methods for analyzing developmental toxicity data. Teratog. Carcinog. Mutagen. 1991, 11:115-133.
59. Prusakiewicz J.J., Harville H.M., Zhang Y., Ackermann C., Voorman R.L. Parabens inhibit human skin estrogen sulfotransferase activity: possible link to paraben estrogenic effects. Toxicology 2007, 232:248-256.
60. Quignot N., Arnaud M., Robidel F., Lecomte A., Tournier M., Cren-Olivé C., Barouki R., Lemazurier E. Characterization of endocrine-disrupting chemicals based on hormonal balance disruption in male and female adult rats. Reprod. Toxicol. 2012, 33:339-352.
61. Robertson K.M., O'Donnell L., Jones M.E., Meachem S.J., Boon W.C., Fisher C.R., Graves K.H., McLachlan R.I., Simpson E.R. Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. PNAS 1999, 96:7986-7991.
62. Routledge E.J., Parker J., Odum J., Ashby J., Sumpter J.P. Some alkyl hydroxy benzoate preservatives (parabens) are estrogenic. Toxicol. Appl. Pharmacol. 1998, 153:12-19.
63. Satoh K., Nonaka R., Ohyama K., Nagai F. Androgenic and antiandrogenic effects of alkylphenols and parabens assessed using the reporter gene assay with stably transfected CHO-K1 cells (AR-EcoScreen System). J. Health Sci. 2005, 51(5):557-568.
64. SCCP Extended opinion on parabens, underarm cosmetics and breast cancer. SCCP/0874/05. European Commission, Health and Consumer Protection Directorate-General 2005, Scientific Committee on Consumer Products, http://ec.europa.eu/health/ph_risk/committees/04_sccp/docs/sccp_o_00d.pdf.
65. Scott H.M., Mason J.I., Sharpe R.M. Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr. Rev. 2009, 30:883-925.
66. Sharpe R.M. The roles of oestrogen in the male. Trends Endocrinol. Metab. 1998, 9:371-377.
67. Sharpe R.M. The 'oestrogen hypothesis'-where do we stand now?. Int. J. Androl. 2003, 26:2-15.
68. Sharpe R., Atanassova N., McKinnell C., Parte P., Turner K., Fisher J., Kerr J., Groome N., Macpherson S., Millar M. Abnormalities in functional development of the Sertoli cells in rats treated neonatally with diethylstilbestrol: a possible role for estrogens in Sertoli cell development. Biol. Reprod. 1998, 59:1084-1094.
69. Sharpe R.M., Fisher J.S., Millar M.M., Jobling S., Sumpter J.P. Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ. Health Perspect. 1995, 103:1136-1143.
70. Sharpe R.M., Skakkebaek N.E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract?. Lancet 1993, 13:1392-1395.
71. Shaw J., deCatanzaro D. Estrogenicity of parabens revisited: impact of parabens on early pregnancy and an uterotrophic assay in mice. Reprod. Toxicol. 2009, 28(1):26-31.
72. Soni M.G., Carabin I.G., Burdock G.A. Safety assessment of esters of p-hydroxybenzoic acid (parabens). Food Chem. Toxicol. 2005, 43:985-1015.
73. Stoker T.E., Laws S.C., Guidici D.L., Cooper R.L. The effect of atrazine on puberty in male wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol. Sci. 2000, 58:50-59.
74. Swerdloff R. What is the relationship among the various endocrine components of the male reproductive system? Hypothalamic-pituitary-testicular axis, feedback loops. Handbook of Andrology 2010, 2-1-2-4. Allen Press Inc., Lawrence. B. Robaire, P. Chan (Eds.).
75. Strohsnitter W.C., Noller K.L., Hoover R.N., Robboy S.J., Palmer J.R., Titus-Ernstoff L., Kaufman R.H., Adam E., Herbst A.L., Hatch E.E. Cancer risk in men exposed in utero to diethylstilbestrol. J. Natl. Cancer Inst. 2001, 93:545-551.
76. Taxvig C., Vinggaard A.M., Hass U., Axelstad M., Boberg J., Hansen P.R., Frederiksen H., Nellemann C. Do parabens have the ability to interfere with steroidogenesis?. Toxicol. Sci. 2008, 106:206-213.
77. Toyama Y., Ohkawa M., Oku R., Maekawa M., Yuasa S. Neonatally administered diethylstilbestrol retards the development of the blood-testis barrier in the rat. J. Androl. 2001, 22:413.
78. Victor-Costa A.B., Bandeira S.M.C., Oliveira A.G., Mahecha G.A.B., Oliveira C.A. Changes in testicular morphology and steroidogenesis in adult rats exposed to atrazine. Reprod. Toxicol. 2010, 29:323-331.
79. Welsh M., Saunders P.T.K., Fisken M., Scott H.M., Hutchison G.R., Smith L.B., Sharpe R.M. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J. Clin. Invest. 2008, 118:1479-1490.
80. Williams K., McKinnell C., Saunders P., Walker M., Fisher J., Turner K., Atanassova N., Sharpe R. Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. APMIS 2001, 109:S493-S504.
81. Ye L., Su Z.J., Ge R.S. Inhibitors of Testosterone Biosynthetic and Metabolic Activation Enzymes. Molecules 2011, 16:9983-10001.
82. Ye X., Bishop A.M., Reidy J.A., Needham L.L., Calafat A.M. Parabens as urinary biomarkers of exposure in humans. Environ. Health Perspect. 2006, 114:1843-1846.
83. Ye X., Tao L.J., Needham L.L., Calafat A.M. Automated on-line column-switching HPLC- MS/MS method for measuring environmental phenols and parabens in serum. Talanta 2008, 76:865-871.
84. Zhang F.P., Pakarainen T., Zhu F., Poutanen M., Huhtaniemi I. Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 2004, 145:1453-1463.
85. Zhang Q., Bai Q., Yuan Y., Liu P., Qiao J. Assessment of seminal estradiol and testosterone levels as predictors of human spermatogenesis. J. Androl. 2010, 31:215.
86. Zirkin B.R. What compounds mediate communication within the testis? Where and how are male-associated hormones produced? Integration of the hypothalamus, pituitary and testis. Handbook of Andrology 2010, 4-1-4-4. Allen Press Inc., Lawrence. B. Robaire, P. Chan (Eds.).
87. Zondek B. Mass excretion of oestrogenic hormone in the urine of the stallion. Nature 1934, 133:209-221.