Environmental levels of oestrogenic and antiandrogenic compounds feminize digit ratios in male rats and their unexposed male progeny

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1768, 2013, Pages

  Auger, Jacques ^a   Le Denmat, Dominique ^b   Berges, Raymond ^c   Doridot, Ludivine ^d   Salmon, Benjamin ^b   Canivenc Lavier, Marie Chantal ^c   Eustache, Florence ^d,e  

^a Port Royal Hospital   (France)

^b and Plateforme d'Imagerie du Vivant   (France)

^c CNRS   (France)

^d INSERM   (France)

^e HÔPITAL JEAN VERDIER   (France)

Author keywords

2D: 4D; Bisphenol A; Endocrine disruptor; Endocrine active substance; Genistein; Vinclozolin

Indexed keywords

ADULT; BIOMARKER; ENDOCRINE DISRUPTOR; IMAGE ANALYSIS; PREGNANCY; RODENT; SEXUAL DIMORPHISM; X-RAY;

RATTUS; RATTUS NORVEGICUS; RODENTIA;

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; ESTROGEN; PHENOL DERIVATIVE;

ANATOMY AND HISTOLOGY; ANIMAL; DRUG EFFECTS; EMBRYO DEVELOPMENT; EMBRYOLOGY; ENVIRONMENTAL EXPOSURE; FEMALE; LIMB; MALE; RAT; SEXUAL DEVELOPMENT; TOXICITY; WISTAR RAT;

ANIMALS; BENZHYDRYL COMPOUNDS; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ESTROGENS, NON-STEROIDAL; EXTREMITIES; FEMALE; MALE; PHENOLS; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

EID: 84898198855     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1532     Document Type: Article

References (55)

1. Galis F, Ten Broek CM, Van Dongen S, Wijnaendts LC. 2010 Sexual dimorphism in the prenatal digit ratio (2D: 4D). Arch. Sex. Behav. 39, 57-62. (doi:10.1007/s10508-009-9485-7)
2. Lutchmaya S, Baron-Cohen S, Raggatt P, Knickmeyer R, Manning JT. 2004 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum. Dev. 77, 23-28. (doi:10.1016/j.earlhumdev.2003.12.002)
3. Manning JT, Bundred PE. 2000 The ratio of 2nd to 4th digit length: a new predictor of disease predisposition? Med. Hypotheses 54, 855-857. (doi:10.1054/mehy.1999.0000)
4. Manning JT, Baron-Cohen S, Wheelwright S, Sanders G. 2001 The 2nd to 4th digit ratio and autism. Dev. Med. Child Neurol. 43, 160-164. (doi:10.1111/j.1469-8749.2001.tb00181.x)
5. Rahman AA et al. 2011 Hand pattern indicates prostate cancer risk. Br. J. Cancer 104, 175-177. (doi:10.1038/sj.bjc.6605986)
6. Manning JT, Scutt D, Wilson J, Lewis-Jones DI. 1998 The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum. Reprod. 13, 3000-3004. (doi:10.1093/humrep/13.11.3000)
7. Auger J, Eustache F. 2011 Second to fourth digit ratios, male genital development and reproductive health: a clinical study among fertile men and testis cancer patients. Int. J. Androl. 34, e49-e58. (doi:10.1111/j.1365-2605.2010.01124.x)
8. Breedlove SM. 2010 Minireview: organizational hypothesis: instances of the fingerpost. Endocrinology 151, 4116-4122. (doi:10.1210/en. 2010-0041)
9. Brown WM, Finn CJ, Breedlove SM. 2002 Sexual dimorphism in digit-length ratios of laboratory mice. Anat. Rec. 267, 231-234. (doi:10.1002/ar. 10108)
10. Roney JR, Whitham JC, Leoni M, Bellem A, Wielebnowski N, Maestripieri D. 2004 Relative digit lengths and testosterone levels in Guinea baboons. Horm. Behav. 45, 285-290. (doi:10.1016/j.yhbeh. 2003.12.008)
11. Zheng Z, Cohn MJ. 2011 Developmental basis of sexually dimorphic digit ratios. Proc. Natl Acad. Sci. USA 108, 16 289-16 294. (doi:10.1073/pnas. 1108312108)
12. Farabollini F, Porrini S, Dessi-Fulgherit F. 1999 Perinatal exposure to the estrogenic pollutant bisphenol A affects behavior in male and female rats. Pharmacol. Biochem. Behav. 64, 687-694. (doi:10.1016/S0091-3057(99)00136-7)
13. Salian S, Doshi T, Vanage G. 2009 Perinatal exposure of rats to bisphenol A affects the fertility of male offspring. Life Sci. 85, 742-752. (doi:10.1016/j.lfs. 2009.10.004)
14. Hsieh MH, Breyer BN, Eisenberg ML, Baskin LS. 2008 Associations among hypospadias, cryptorchidism, anogenital distance, and endocrine disruption. Curr. Urol. Rep. 9, 137-142. (doi:10.1007/s11934-008-0025-0)
15. Eustache F, Mondon F, Canivenc-Lavier MC, Lesaffre C, Fulla Y, Berges R, Cravedi JP, Vaiman D, Auger J. 2009 Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility. Environ. Health Perspect. 117, 1272-1279. (doi:10. 1289/ehp.0800158)
16. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. 2008 Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health Perspect. 116, 39-44. (doi:10.1289/ehp. 10753)
17. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. 2007 Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139-177. (doi:10.1016/j. reprotox.2007.07.010)
18. Hotchkiss AK, Lambright CS, Ostby JS, Parks-Saldutti L, Vandenbergh JG, Gray Jr LE. 2007 Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague- Dawley rats. Toxicol. Sci. 96, 335-345. (doi:10. 1093/toxsci/kfm002)
19. Lakind JS, Naiman DQ. 2011 Daily intake of bisphenol A and potential sources of exposure: 2005-2006 National Health and Nutrition Examination Survey. J. Expo. Sci. Environ. Epidemiol. 21, 272-279. (doi:10.1038/jes.2010.9)
20. Tanaka K, Sasaki S, Murakami K, Okubo H, Takahashi Y, Miyake Y. 2008 Relationship between soy and isoflavone intake and periodontal disease: the Freshmen in Dietetic Courses Study II. BMC Pub. Health 8, 39. (doi:10.1186/1471-2458-8-39)
21. US EPA 2003 Fed reg. vinclozolin; notice of filing a pesticide petition to establish a tolerance for a certain pesticide chemical in or on food, pp. 14628-14635. See https://www.federalregister.gov/articles/2003/03/26/03-7246/.
22. Leblanc JC, Malmauret L, Guerin T, Bordet F, Boursier B, Verger P. 2000 Estimation of the dietary intake of pesticide residues, lead, cadmium, arsenic and radionuclides in France. Food Addit. Contam. 17, 925-932. (doi:10.1080/026520300750038108)
23. European Food Safety Authority 2008 Reasoned opinion of EFSA prepared by PRAPeR on MRLs of concern for the active substance vinclozolin. EFSA Sci. Rep. 166, 1-36. (doi:10.2903/j.efsa. 2008.166r)
24. Hass U, Scholze M, Christiansen S, Dalgaard M, Vinggaard AM, Axelstad M, Metzdorff SB, Kortenkamp A. 2007 Combined exposure to antiandrogens exacerbates disruption of sexual differentiation in the rat. Environ. Health Perspect. 115(Suppl. 1), 122-128. (doi:10.1289/ehp.9360)
25. Marois G. 1968 Action of progesterone, testosterone and estradiol on the anogenital distance and somatic sexual differentiation in rats. Biol. Med. 57, 44-90.
26. Talarovicová A, Krsková L, Blazeková J. 2009 Testosterone enhancement during pregnancy influences the 2D: 4D ratio and open field motor activity of rat siblings in adulthood. Horm. Behav. 55, 235-239. (doi:10.1016/j.yhbeh.2008.10.010)
27. McMechan AP, O'Leary-Moore SK, Morrison SD, Hannigan JH. 2004 Effects of prenatal alcohol exposure on forepaw digit length and digit ratios in rats. Dev. Psychobiol. 45, 251-258. (doi:10.1002/ dev.20035)
28. Manning JT. 2011 Resolving the role of prenatal sex steroids in the development of digit ratio. Proc. Natl Acad. Sci. USA 108, 16 143-16 144. (doi:10.1073/ pnas.1108312108)
29. Manning JT, Fink B. 2008 Digit ratio (2D: 4D), dominance, reproductive success, asymmetry, and sociosexuality in the BBC Internet Study. Am. J. Hum. Biol. 20, 451-461. (doi:10.1002/ajhb.20767)
30. Manno FA. 2008 Measurement of the digit lengths and the anogenital distance in mice. Physiol. Behav. 93, 364-368. (doi:10.1016/j.physbeh.2007.09.011)
31. McFadden D, Shubel E. 2002 Relative lengths of fingers and toes in human males and females. Horm. Behav. 42, 492-500. (doi:10.1006/hbeh. 2002.1833)
32. Kyriakidis I, Papaioannidou P. 2008 Epidemiologic study of the sexually dimorphic second to fourth digit ratio (2D: 4D) and other finger ratios in Greek population. Coll. Antropol. 32, 1093-1098.
33. Voracek M. 2009 Comparative study of digit ratios (2D: 4D and other) and novel measures of relative finger length: testing magnitude and consistency of sex differences across samples. Percept. Mot. Skills 108, 83-93. (doi:10.2466/pms.108.1.83-93)
34. Hauser H, Gandelman R. 1983 Contiguity to males in utero affects avoidance responding in adult female mice. Science 220, 437-438. (doi:10.1126/ science.6836288)
35. Morley-Fletcher S, Palanza P, Parolaro D, Vigano D, Laviola G. 2003 Intrauterine position has long-term influence on brain mu-opioid receptor density and behaviour in mice. Psychoneuroendocrinology 28, 386-400. (doi:10.1016/S0306-4530(02)00030-6)
36. Knickmeyer RC, Woolson S, Hamer RM, Konneker T, Gilmore JH. 2011 2D: 4D ratios in the first 2 years of life: stability and relation to testosterone exposure and sensitivity. Horm. Behav. 60, 256-263. (doi:10.1016/j.yhbeh.2011.05.009)
37. Rosenberg Zand RS, Jenkins DJ, Diamandis EP. 2000 Genistein: a potent natural antiandrogen. Clin. Chem. 46, 887-888.
38. Wang H, Li J, Gao Y, Xu Y, Pan Y, Tsuji I, Sun ZJ, Li XM. 2010 Xeno-oestrogens and phyto-oestrogens are alternative ligands for the androgen receptor. Asian J. Androl. 12, 535-547. (doi:10.1038/aja.2010.14)
39. Xu LC, Sun H, Chen JF, Bian Q, Qian J, Song L, Wang XR. 2005 Evaluation of androgen receptor transcriptional activities of bisphenol A, octylphenol and nonylphenol in vitro. Toxicology 216, 197-203. (doi:10.1016/j.tox.2005.08.006)
40. Lee HJ, Chattopadhyay S, Gong EY, Ahn RS, Lee K. 2003 Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol. Sci. 75, 40-46. (doi:10.1093/toxsci/kfg150)
41. Molina-Molina JM et al. 2006 Steroid receptor profiling of vinclozolin and its primary metabolites. Toxicol. Appl. Pharmacol. 216, 44-54. (doi:10. 1016/j.taap.2006.04.005)
42. Xiao Y, Liu R, Xing L, Xu Y, Shang L, Hao W. 2011 Combined developmental toxicity of bisphenol A and genistein in micromass cultures of rat embryonic limb bud and midbrain cells. Toxicol. In Vitro 25, 153-159. (doi:10.1016/j.tiv.2010.10.010)
43. Rowas SA, Haddad R, Gawri R, Al Ma'awi AA, Chalifour LE, Antoniou J, Mwale F. 2012 Effect of in utero exposure to diethylstilbestrol on lumbar and femoral bone, articular cartilage, and the intervertebral disc in male and female adult mice progeny with and without swimming exercise. Arthritis Res. Ther. 14, R17. (doi:10.1186/ar3696)
44. Dean A, Sharpe RM. 2013 Anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders. J. Clin. Endocrinol. Metab. 98, 2230-2238. (doi:10.1210/jc.2012-4057)
45. Hurd PL, Bailey AA, Gongal PA, Yan RH, Greer JJ, Pagliardini S. 2008 Intrauterine position effects on anogenital distance and digit ratio in male and female mice. Arch. Sex. Behav. 37, 9-18. (doi:10. 1007/s10508-007-9259-z)
46. van den Driesche S, Scott HM, MacLeod DJ, Fisken M, Walker M, Sharpe RM. 2011 Relative importance of prenatal and postnatal androgen action in determining growth of the penis and anogenital distance in the rat before, during and after puberty. Int. J. Androl. 34, e578-e586. (doi:10.1111/j.1365-2605.2011.01175.x)
47. Kurebayashi H, Nagatsuka S, Nemoto H, Noguchi H, Ohno Y. 2005 Disposition of low doses of 14Cbisphenol A in male, female, pregnant, fetal, and neonatal rats. Arch. Toxicol. 79, 243-252. (doi:10. 1007/s00204-004-0628-2)
48. Doerge DR, Vanlandingham M, Twaddle NC, Delclos KB. 2010 Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol. Lett. 199, 372-376. (doi:10.1016/j.toxlet.2010.09.022)
49. Jirtle RL, Skinner MK. 2007 Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8, 253-262. (doi:10.1038/ nrg2045)
50. Lange UC, Schneider R. 2010 What an epigenome remembers. Bioessays 32, 659-668. (doi:10.1002/ bies.201000030)
51. Reik W. 2007 Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432. (doi:10.1038/ nature05918)
52. Salian S, Doshi T, Vanage G. 2009 Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to bisphenol A. Life Sci. 85, 11-18. (doi:10.1016/j.lfs.2009.04.005)
53. Salian S, Doshi T, Vanage G. 2011 Perinatal exposure of rats to bisphenol A affects fertility of male offspring: an overview. Reprod. Toxicol. 31, 359-362. (doi:10.1016/j.reprotox.2010.10.008)
54. Lilley T, Laaksonen T, Huitu O, Helle S. 2009 Digit length ratio (2D/4D): comparing measurements from X-rays and photographs in field voles (Microtus agrestis). Behav. Ecol. Sociobiol. 63, 1539-1547. (doi:10.1016/j.physbeh.2009.11.015)
55. Yan RH, Malisch JL, Hannon RM, Hurd PL, Garland Jr T. 2008 Selective breeding for a behavioural trait changes digit ratio. PLoS ONE 3, e3216. (doi:10. 1371/journal.pone.0003216)