A review of studies on androgen and estrogen exposure in fish early life stages: Effects on gene and hormonal control of sexual differentiation

Journal of Applied Toxicology

Volumn 31, Issue 5, 2011, Pages 379-398

  Leet, Jessica K ^a   Gall, Heather E ^b   Sepúlveda, Maria S ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Cyp19; Dmrt1; Endocrine disrupting chemicals; Foxl2; Gene expression; Hormones; Sex determination; Sex differentiation; Sox9; Teleosts

Indexed keywords

17ALPHA TRENBOLONE; AMH PROTEIN; ANDROGEN; ANDROSTANOLONE; ANDROSTENEDIONE; ANDROSTERONE; AROMATASE; CELL NUCLEUS RECEPTOR; DMRT1 PROTEIN; DMY PROTEIN; ESTRADIOL; ESTRIOL; ESTROGEN; ESTRONE; FOLLISTATIN; FORK HEAD TRANSCRIPTION FACTOR 2; GLYCOPROTEIN; GROWTH DIFFERENTIATION FACTOR 9; INHA PROTEIN; NR5A1 PROTEIN; NUCLEAR RECEPTOR DAX 1; OVO11 PROTEIN; PAX2A PROTEIN; PROTEIN; SSB4 PROTEIN; TESTOSTERONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX9; TRENBOLONE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CONCENTRATION (PARAMETERS); DEVELOPMENTAL STAGE; ENVIRONMENTAL EXPOSURE; GENE CONTROL; HORMONAL REGULATION; MOLECULAR MECHANICS; NONHUMAN; ORYZIAS; PIMEPHALES PROMELAS; PRIORITY JOURNAL; RAINBOW TROUT; REVIEW; SEX DETERMINATION; SEX DIFFERENTIATION; TELEOST; WATER CONTAMINATION; ZEBRA FISH;

ANDROGENS; ANIMALS; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL MONITORING; ESTROGENS; FEMALE; FISHES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MALE; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; WATER POLLUTANTS, CHEMICAL;

PISCES; TELEOSTEI; VERTEBRATA;

EID: 79960746241     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1682     Document Type: Review

References (156)

1. Alfaqih MA, Brunelli JP, Drew RE, Thorgaard GH. 2009. Mapping of five candidate sex-determining loci in rainbow trout (Oncorhynchus mykiss). BMC Genet. 10: 2; doi: 10.1186/1471-2156-10-2.
2. Angus RA, Stanko J, Jenkins RL, Watson RD. 2005. Effects of 17α-ethynylestradiol on sexual development of male western mosquitofish (Gambusia affinis). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 140(3-4): 330-339; doi: 10.1016/j.cca.2005.03.008.
3. Ankley GT, Jensen KM, Makynen EA, Kahl MD, Korte JJ, Hornung MW, Henry TR, Denny JS, Leino RL, Wilson VS, Cardon MC, Hartig PC, Gray LE. 2003. Effects of the androgenic growth promoter 17-beta-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ. Toxicol. Chem. 22(6): 1350-1360; doi: 10.1002/etc.5620220623.
4. Arango NA, Lovell-Badge R, Behringer RR. 1999. Targeted mutagenesis of the endogenous mouse MIS gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 99: 409-419; doi: 10.1016/S0092-8674(00)81527-5.
5. Arcand-Hoy LD, Benson WH. 1998. Fish reproduction: an ecologically relevant indicator of endocrine disruption. Environ. Toxicol. Chem. 17(1): 49-57; doi: 10.1002/etc.5620170108.
6. Baroiller JF, D'Cotta H. 2001. Environment and sex determination in farmed fish. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130(4): 399-409; doi: 10.1016/S1532-0456(01)00267-8.
7. Baron D, Guiguen Y. 2003. Gene expression during gonadal sex differentiation in rainbow trout (Oncorhynchus mykiss): from candidate genes studies to high throughout genomic approach. Fish Physiol. Biochem. 28: 119-123; doi: 10.1023/B:FISH.0000030496.21741.6c.
8. Baron D, Cocquet J, Xia XH, Fellous M, Guiguen Y, Veitia RA. 2004. An evolutionary and functional analysis of FOXL2 in rainbow trout gonad differentiation. J. Mol. Endocrinol. 33(3): 705-715; doi: 10.1677/jme.1.01566.
9. Baron D, Houlgatte R, Fostier A, Guiguen Y. 2005. Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol. Reprod. 73(5): 959-966; doi: 10.1095/biolreprod.105.041830.
10. Baron D, Houlgatte R, Fostier A, Guiguen Y. 2008. Expression profiling of candidate genes during ovary-to-testis trans-differentiation in rainbow trout masculinized by androgens. Gen. Comp. Endocrinol. 156(2): 369-378; doi: 10.1016/j.ygcen.2008.01.016.
11. Baronti C, Curini R, D'Ascenzo G, Corcia AD, Gentilli A, Samperi R. 2000. Monitoring natural and synthetic estrogens at activated sludge sewage treatment plants and in a receiving water. Environ. Sci. Technol. 40: 2181-2189; doi: 10.1021/es001359q.
12. Behringer RR, Cate RL, Froelick GJ, Palmiter RD, Brinster RL. 1990. Abnormal sexual development in transgenic mice chronically expressing mullerian inhibiting substance. Nature 345: 167-170; doi: 10.1038/345167a0.
13. Blázquez M, Piferrer F. 2004. Cloning, sequence analysis, tissue distribution, and sex-specific expression of the neural form of P450 aromatase in juvenile sea bass (Dicentrarchus labrax). Mol. Cell. Endocrinol. 219(1-2): 83-94; doi: 10.1016/j.mce.2004.01.006.
14. Bogers R, De Vries-Buitenweg S, Van Gils M, Baltussen E, Hargreaves A, van de Waart B, De Roode D, Legler J, Murk A. 2006a. Development of chronic tests for endocrine active chemicals. Part 2: an extended fish early-life stage test with an androgenic chemical in the fathead minnow (Pimephales promelas). Aquat. Toxicol. 80(2): 119-130; doi: 10.1016/j.aquatox.2006.07.020.
15. Bogers R, Esther M, Jeanette D, Daphne FDR, Albertinka JM, Bart Van Der B, Juliette L. 2006b. Estrogenic endpoints in fish early life-stage tests: luciferase and vitellogenin induction in estrogen-responsive transgenic zebrafish. Environ. Toxicol. Chem. 25(1): 241-247; doi: 10.1897/05-234R.1.
16. Bollig F, Mehringer R, Perner B, Hartung C, Schafer M, Schartl M, Volff JN, Winkler C, Englert C. 2006. Identification and comparative expression analysis of a second WT1 gene in zebrafish. Dev. Dyn. 235(2): 554-561; doi: 10.1002/dvdy.20645.
17. Borch T, Davis JG, Yang Y, Young RB. 2009. Occurrence of steroid sex hormones in the Cache la Poudre River, and pathways for their removal in the environment. Completion Report no. 216. Colorado Water Institute; 61.
18. Boudreau M, Simon CC, Deborah LM, Céline HB, Joanne LP, Glen JvdK. 2004. Utility of morphological abnormalities during early-life development of the estuarine mummichog, Fundulus heteroclitus, as an indicator of estrogenic and antiestrogenic endocrine disruption. Environ. Toxicol. Chem. 23(2): 415-425; doi: 10.1897/03-50.
19. Brion F, Tyler CR, Palazzi X, Laillet B, Porcher JM, Garric J, Flammarion P. 2004. Impacts of 17β-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat. Toxicol. 68(3): 193-217; doi: 10.1016/j.aquatox.2004.01.022.
20. Callard GV, Tchoudakova A. 1997. Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish. J. Steroid Biochem. Mol. Biol. 61(3-6): 387-392; doi: 10.1016/S0960-0760(97)80037-4.
21. Callard GV, Tchoudakova AV, Kishida M, Wood E. 2001. Differential tissue distribution, developmental programming, estrogen regulation and promoter characteristics of cyp19 genes in teleost fish. J. Steroid Biochem. Mol. Biol. 79(1-5): 305-314; doi: 10.1016/S0960-0760(01)00147-9.
22. Chai C, Chan WK. 2000. Developmental expression of a novel FTZ-f1 homologue, FF1b (Nr5a4), in the zebrafish Danio rerio. Mech. Dev. 91: 421-426; doi: 10.1016/S0925-4773(99)00312-3.
23. Chang X, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y. 2005. Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 141(2): 101-115; doi: 10.1016/j.ygcen.2004.11.020.
24. Chen TS, Chen TC, Yeh KJ, Chao HR, Liaw ET, Hsieh CY, Chen KC, Hsieh LT, Yeh YL. 2010. High estrogen concentrations in receiving river discharge from a concentrated livestock feedlot. Sci. Total Environ. 408: 3223-3230; doi: 10.1016/j.scitotenv.2010.03.054.
25. Chiang EF-L, Yan Y-L, Guiguen Y, Postlethwait J, Chung B-c. 2001a. Two Cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain. Mol. Biol. Evol. 18(4): 542-550.
26. Chiang EF-L, Yan Y-L, Tong S-K, Hsiao P-H, Guiguen Y, Postlethwait J, Chung B-C. 2001b. Characterization of duplicated zebrafish cyp19 genes. J. Exp. Zool. 290(7): 709-714; doi: 10.1002/jez.1121.
27. Chimchirian RF, Suri RP, Fu H. 2007. Free synthetic and natural estrogen hormones in influent and effluent of three municipal wastewater treatment plants. Water Environ. Res. 79(9): 969-974; doi: 10.2175/106143007X175843.
28. Cocquet J, Baere ED, Gareil M, Pannetier M, Xia X, Fellous M, Veitia RA. 2003. Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res. 101: 206-211; doi: 10.1159/000074338.
29. Conover DO, Kynard BE. 1981. Environmental sex determination: interaction of temperature and genotype in a fish. Science 213(4507): 577-579; doi: 10.1126/science.213.4507.577.
30. Cyr DG, Eales JG. 1996. Interrelationships between thyroidal and reproductive endocrine systems in fish. Rev. Fish Biol. 6(2): 165-200; doi: 10.1007/bf00182342.
31. D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller J-F. 2001. Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol. Reprod. Dev. 59(3): 265-276; doi: 10.1002/mrd.1031.
32. Devlin RH, Nagahama Y. 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208(3-4): 191-364; doi: 10.1016/S0044-8486(02)00057-1.
33. Devlin RH, McNeil BK, Groves TDD, Donaldson EM. 1991. Isolation of a Y-chromosomal DNA probe capable of determining genetic sex in chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci. 48(9): 1606-1612; doi: 10.1139/f91-190.
34. Duong CN, Ra JS, Cho J, Kim SD, Choi HK, Park J, Kim KW, Inam E, Kim SD. 2010. Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78: 286-293.
35. Durhan EJ, Lambright CS, Makynen EA, Lazorchak J, Hartig PC, Wilson VS, Gray LE, Ankley GT. 2006. Identification of metabolites of trenbolone acetate in androgen runoff from a beef feedlot. Environ. Health Perspect. 114(1): 65-68.
36. Fenske M, Segner H. 2004. Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat. Toxicol. 67(2): 105-126; doi: 10.1016/j.aquatox.2003.10.008.
37. Fenske M, Gerd M, Christoph S, Helmut S. 2005. An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish, Danio rerio. Environ. Toxicol. Chem. 24(5): 1088-1098; doi: 10.1897/04-096R1.1.
38. Filby AL, Thorpe KL, Tyler CR. 2006. Multiple molecular effect pathways of an environmental oestrogen in fish. J. Mol. Endocrinol. 37(1): 121-134; doi: 10.1677/jme.1.01997.
39. Filby AL, Thorpe KL, Maack G, Tyler CR. 2007. Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquat. Toxicol. 81(2): 219-231; doi: 10.1016/j.aquatox.2006.12.003.
40. Gall HE, Jafvert CT, Jenkinson B. 2010. Integrating hydrograph modeling with real-time flow monitoring to generate hydrograph-specific sampling schemes. J. Hydrol. 393(3-4): 331-340; doi: 10.1016/j.jhydrol.2010.08.028.
41. Gall HE, Sassman SA, Lee LS, Jafvert CT. 2011. Hormone hydro-chemograph behavior in a tile drained agroecosystem receiving animal manure and waste effluent. Environ. Sci. Technol. (submitted).
42. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, Behringer RR, Lecureuil C, Guillou F, Huff V. 2006. The Wilms tumor gene, WT1, is required for SOX9 expression and maintenance of tubular architecture in the developing testis. Proc. Natl Acad. Sci. USA 103: 11987-11992; doi: 10.1073/pnas.0600994103.
43. Godwin J. 2009. Social determination of sex in reef fishes. Semin. Cell Dev. Biol. 20(3): 264-270; doi: 10.1016/j.semcdb.2008.12.003.
44. Griffiths R, Orr KL, Adam A, Barber I. 2000. DNA sex identification in the three-spined stickleback. J. Fish Biol. 57(5): 1331-1334; doi: 10.1111/j.1095-8649.2000.tb00490.x.
45. Guan G, Kobayashi T, Nagahama Y. 2000. Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the tilapia (Oreochromis niloticus). Biochem. Biophys. Res. Commun. 272(3): 662-666; doi: 10.1006/bbrc.2000.2840.
46. Guiguen Y, Baroiller J-F, Ricordel M-J, Iseki K, McMeel OM, Martin SAM, Fostier A. 1999. Involvement of estrogens in the process of sex differentiation in two fish species: The rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol. Reprod. Dev. 54(2): 154-162. doi: 10.1002/(sici)1098-2795(199910)54:2<154::aid-mrd7>3.0.co;2-5.
47. Guo YQ, Cheng HH, Gao S, Zhou RJ. 2004. Phylogenetic tree and synteny of DMRT genes family of vertebrates. Acta Genet. Sin. 31: 1103-1108.
48. Guo YQ, Cheng HH, Huang X, Gao S, Yu HS, Zhou RJ. 2005. Gene structure, multiple alternative splicing and expression in gonads of zebrafish DMRT1. Biochem. Biophys. Res. Commun. 330(3): 950-957; doi: 10.1016/j.bbrc.2005.0366.
49. Hagino S, Kagoshima M, Asida S. 2001. Effects of ethinylestradiol, diethylstilbestrol, 4-t-pentylphenol, 17β-estradiol, methyltestosterone and flutamide on sex reversal in S-rR strain medaka (Oryzias latipes). Environ. Sci. 8(1): 075-087.
50. Hahlbeck E, Griffiths R, Bengtsson B-E. 2004a. The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption: I. Sexual differentiation. Aquat. Toxicol. 70(4): 287-310; doi: 10.1016/j.aquatox.2004.10.003.
51. Hahlbeck E, Katsiadaki I, Mayer I, Adolfsson-Erici M, James J, Bengtsson B-E. 2004b. The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption II - kidney hypertrophy, vitellogenin and spiggin induction. Aquat. Toxicol. 70(4): 311-326; doi: 10.1016/j.aquatox.2004.10.004.
52. He CL, Du JL, Wu GC, Lee YH, Sun LT, Chang CF. 2003. Differential DMRT1 transcripts in gonads of the protandrous black porgy, Acanthopagrus schlegeli. Cytogenet. Genome Res. 101: 309-313; doi: 10.1159/000074354.
53. Hill RL, Janz DM. 2003. Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat. Toxicol. 63(4): 417-429; doi: 10.1016/S0166-445X(02)00207-2.
54. Hirai N, Nanba A, Koshio M, Kondo T, Morita M, Tatarazako N. 2006. Feminization of Japanese medaka (Oryzias latipes) exposed to 17β-estradiol: effect of exposure period on spawning performance in sex-transformed females. Aquat. Toxicol. 79(3): 288-295; doi: 10.1016/j.aquatox.2006.06.018.
55. Holbech H, Kinnberg K, Petersen GI, Jackson P, Hylland K, Norrgren L, Bjerregaard P. 2006. Detection of endocrine disrupters: evaluation of a fish sexual development test (FSDT). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 144(1): 57-66; doi: 10.1016/j.cbpc.2006.05.006.
56. Hossain A, Saunders GF. 2001. The human sex-determining gene SRY is a direct target of WT1. J. Biol. Chem. 276: 16817-16823; doi: 10.1074/jbc.M009056200.
57. Huang X, Cheng H, Guo Y, Liu L, Gui J, Zhou R. 2002. A conserved family of doublesex-related genes from fishes. J. Exp. Zool. 294(1): 63-67; doi: 10.1002/jez.10044.
58. Ijiri S, Kaneko H, Kobayashi T, Wang D-S, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. 2008. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 78(2): 333-341; doi: 10.1095/biolreprod.107.064246.
59. Irwin LK, Gray S, Oberdörster E. 2001. Vitellogenin induction in painted turtle, Chrysemys picta, as a biomarker of exposure to environmental levels of estradiol. Aquat. Toxicol. 55: 49-60.
60. Jensen KM, Makynen EA, Kahl MD, Ankley GT. 2006. Effects of the feedlot contaminant 17α-trenbolone on reproductive endocrinology of the fathead minnow. Environ. Sci. Technol. 40(9): 3112-3117; doi: 10.1021/es052174s.
61. Jobling S, Tyler CR. 2003. Endocrine disruption in wild freshwater fish. Pure Appl. Chem. 75(11-12): 2219-2234.
62. Jobling S, Coey S, Whitmore JG, Kime DE, Van Look KJW, McAllister BG, Beresford N, Henshaw AC, Brighty G, Tyler CR, Sumpter JP. 2002. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 67(2): 515-524; doi: 10.1095/biolreprod67.2.515.
63. Johns SM, Denslow ND, Kane MD, Watanabe KH, Orlando EF, Sepúlveda MS. 2009a. Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages. Environ. Toxicol.: n/a-n/a; doi: 10.1002/tox.20545.
64. Johns SM, Kane MD, Denslow ND, Watanabe KH, Orlando EF, Villeneuve DL, Ankley GT, Sepúlveda MS. 2009b. Characterization of ontogenetic changes in gene expression in the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 28(4): 873-880; doi: 10.1897/08-213r.1.
65. Karube M, Fernandino JI, Strobl-Mazzulla P, Strüssmann CA, Yoshizaki G, Somoza GM, Patiño R. 2007. Characterization and expression profile of the ovarian cytochrome P-450 aromatase (cyp19A1) gene during thermolabile sex determination in pejerrey, Odontesthes bonariensis. J. Exp. Zool. A Ecol. Genet. Physiol. 307A(11): 625-636; doi: 10.1002/jez.416.
66. Kawauchi H, Suzuki K, Itoh H, Swanson P, Naito N, Nagahama Y, Nozaki M, Nakai Y, Itoh S. 1989. The duality of teleost gonadotropins. Fish Physiol. Biochem. 7(1): 29-38; doi: 10.1007/bf00004687.
67. Kazeto Y, Ijiri S, Place AR, Zohar Y, Trant JM. 2001. The 5'-flanking regions of CYP19A1 and CYP19A2 in zebrafish. Biochem. Biophys. Res. Commun. 288(3): 503-508; doi: 10.1006/bbrc.2001.5796.
68. Khoo G, Lim MH, Suresh H, Gan DY, Lim KF, Chen F, Chan W-K, Lim TM, Phang VE. 2003. Genetic linkage maps of the guppy (Poecilia reticulata): assignment of RAPD markers to multipoint linkage groups. Marine Biotech. 5(3): 279-293; doi: 10.1007/s10126-002-0072-3.
69. Kitano T, Takamune K, Kobayashi T, Nagahama Y, Abe SI. 1999. Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J. Mol. Endocrinol. 23(2): 167-176; doi: 10.1677/jme.0.0230167.
70. Kitano T, Takamune K, Nagahama Y, Abe S-I. 2000. Aromatase inhibitor and 17α-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol. Reprod. Develop. 56(1): 1-5; doi: 10.1002/(sici)1098-2795(200005)56:1<1::aid-mrd1>3.0.co;2-3.
71. Kjær J, Olsen P, Bach K, Barlebo HC, Ingerslev F, Hansen M, Sørensen BH. 2007. Leaching of estrogenic hormones from manure-treated structured soils. Environ. Sci. Technol. 41(11): 3911-3917.
72. Klamt B, Koziell A, Poulat F, Wieacker P, Scambler P, Berta P, Gessler M. 1998. Frasier syndrome is caused by defective alternative splicing of WT1 leading to an altered ratio of WT1 +/-KTS splice isoforms. Hum. Mol. Genet. 7: 709-714; doi: 10.1093/hmg/7.4.709.
73. Kluver N, Herpin A, Braasch I, Driessle J, Schartl M. 2009. Regulatory back-up circuit of medaka WT1 co-orthologs ensures PGC maintenance. Dev. Biol. 325(1): 179-188; doi: 10.1016/j.ydbio.2008.10.009.
74. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2003. Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet. Genome Res. 101(3-4): 289-294; doi: 10.1159/000074351.
75. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. 2004. Two DM domain genes, DMY and DMRT1 involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dyn. 231(3): 518-526; doi: 10.1002/dvdy.20158.
76. Koger CS, Teh SJ, Hinton DE. 2000. Determining the sensitive developmental stages of intersex induction in medaka (Oryzias latipes) exposed to 17β-estradiol or testosterone. Mar. Environ. Res. 50(1-5): 201-206.
77. Kolok AS, Sellin MK. 2008. The Environmental Impact of Growth-promoting Compounds Employed by the United States Beef Cattle Industry: History, Current Knowledge, and Future Directions, Whitacre DM (ed.). Springer: New York.
78. Kolok AS, Snow DD, Kohno S, Sellin MK, Guillette LJ, Jr. 2007. Occurrence and biological effect of exogenous steroids in the Elkhorn River, Nebraska, USA. Sci. Total Environ. 388: 104-115.
79. Kondo M, Nanda I, Hornung U, Asakawa S, Shimizu N, Mitani H, Schmid M, Shima A, Schartl M. 2003. Absence of the candidate male sex-determining gene DMRT1b(Y) of medaka from other fish species. Curr. Biol. 13(5): 416-420; doi: 10.1016/S0960-9822(03)00125-8.
80. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351(6322): 117-121; doi: 10.1038/351117a0.
81. Kwon JY, Haghpanah V, Kogson-Hurtado LM, McAndrew BJ, Penman DJ. 2000. Masculinization of genetic female nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287(1): 46-53; doi: 10.1002/1097-010X(20000615)287:1<46::AID-JEZ6>3.3.CO;2-O.
82. Kwon JY, McAndrew BJ, Penman DJ. 2001. Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus. Mol. Reprod. Develop. 59(4): 359-370; doi: 10.1002/mrd.1042.
83. Langdon KA, Warne M, Kookana RS. 2010. Aquatic hazard assessment for pharmaceuticals, personal care products, and endocrine-disrupting compounds from biosolids-amended land. Integr. Environ. Assess. Manag. 6(4): 663-676.
84. Lange IG, Daxenberger A, Schiffer B, Witters H, Ibarreta D, Meyer HD. 2002. Sex hormones originating from different livestock production systems: fate and potential endocrine disrupting activity in the environment. Anal. Chimica Acta 473: 27-37.
85. Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panter GH, Sumpter JP. 2001. Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 20(6): 1216-1227; doi: 10.1002/etc.5620200610.
86. Lee LS, Carmosini N, Sassman SA, Dion HM, Sepúlveda MS. 2007. Agricultural contributions of antimicrobials and hormones on soil and water quality. Adv. Agron. 93: 1-68; doi: 10.1016/S0065-2113(06)93001-6.
87. León A, Teh SJ, Hall LC, Teh FC. 2007. Androgen disruption of early development in Qurt strain medaka (Oryzias latipes). Aquat. Toxicol. 82(3): 195-203; doi: 10.1016/j.aquatox.2007.02.012.
88. Li JZ, Zhou YP, Zhen Y, Xu Y, Cheng PX, Wang HN, Deng FJ. 2009. Cloning and characterization of the SSB-1 and SSB-4 genes expressed in zebrafish gonads. Biochem. Genet. 47: 179-190; doi: 10.1007/s10528-008-9215-1.
89. Liao T, Guo Q, Jin S, Cheng W, Xu Y. 2009. Comparative responses in rare minnow exposed to 17β-estradiol during different life stages. Fish Physiol. Biochem. 35(3): 341-349.
90. Liu Z, Wu F, Jiao B, Zhang X, Hu C, Huang B, Zhou L, Huang X, Wang Z, Zhang Y, Nagahama Y, Cheng CHK, Wang D. 2007. Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. J. Endocrinol. 194(1): 223-241; doi: 10.1677/joe-07-0135.
91. Liu Z, Kanjo Y, Mizutani S. 2009. Urinary excretion rates of natural estrogens and androgens from humans, and their occurrence and fate in the environment: a review. Sci. Total Environ. 407: 4975-4985.
92. Loffler KA, Zarkower D, Koopman P. 2003. Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 144: 3237-3243; doi: 10.1210/en.2002-0095.
93. Lucas SD, Jones DL. 2006. Biodegradation of estrone and 17β-estradiol in grassland soils amended with animal wastes. Soil Biol. Biochem. 38(9): 2803-2815; doi: 10.1016/j.soilbio.2006.04.033.
94. Maack G, Segner H. 2004. Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 139(1-3): 47-55.
95. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre J-J, Bernot A, Laudet V, Guiguen Y. 2000. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. B.B.A. - Gene Struct. Expr. 1493(1-2): 180-187; doi: 10.1016/S0167-4781(00)00186-X.
96. Matsuda M. 2005. Sex determination in the teleost medaka, Oryzias latipes. Annu. Rev. Genet. 39: 293-307; doi: 10.1146/annurev.genet.39.110304.095800.
97. Matsuda M, Kusama T, Oshiro T, Kurihara Y, Hamaguchi S, Sakaizumi M. 1997. Isolation of a sex chromosome-specific DNA sequence in the medaka, Oryzias latipes. Genes Genet. Syst. 72(5): 263-268.
98. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417(6888): 559-563; doi: 10.1038/nature751.
99. Matsuda M, Shinomiya A, Kinoshita M, Suzuki A, Kobayashi T, Paul-Prasanth B, Lau EL, Hamaguchi S, Sakaizumi M, Nagahama Y. 2007. Dmy gene induces male development in genetically female (Xx) medaka fish. Proc. Natl Acad. Sci. USA 104(10): 3865-3870; doi: 10.1073/pnas.0611707104.
100. Matthews J, Gustafsson J-Ã. 2003. Estrogen signaling: a subtle balance between ERα and ERβ. Mol. Interven. 3(5): 281-292; doi: 10.1124/mi.3.5.281.
101. Matthiessen P, Arnold D, Johnson AC, Pepper TJ, Pottinger TG, Pulman KGT. 2006. Contamination of headwater streams in the United Kingdom by oestrogenic hormones from livestock farms. Sci. Total Environ. 367: 616-630.
102. McGee MR, Julius ML, Vajda AM, Norris DO, Barber LB, Schoenfuss HL. 2009. Predator avoidance performance of larval fathead minnows (Pimephales promelas) following short-term exposure to estrogen mixtures. Aquat. Toxicol. 91(4): 355-361.
103. Morais Da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R. 1996. SOX9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 14: 62-68.
104. Munday PL, Buston PM, Warner RR. 2006. Diversity and flexibility of sex-change strategies in animals. Trends Ecol. Evol. 21(2): 89-95; doi: 10.1016/j.tree.2005.10.020.
105. Nagahama Y. 1994. Endocrine regulation of gametogenesis in fish. Int. J. Dev. Biol. 38: 217-229.
106. Nagarnaik PM, Mills MA, Boulanger B. 2010. Concentrations and mass loadings of hormones, alkylphenols, and alkylphenol ethoxylates in healthcare facility wastewaters. Chemosphere 78: 1056-1062; doi: 10.1016/j.chemosphere.2009.11.019.
107. Nakamoto M, Suzuki A, Matsuda M, Nagahama Y, Shibata N. 2005. Testicular type SOX9 is not involved in sex determination but might be in the development of testicular structures in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 333: 729-736; doi: 10.1016/j.bbrc.2005.05.158.
108. Nakamoto M, Matsuda M, Wang DS, Nagahama Y, Shibata N. 2006. Molecular cloning and analysis of gonadal expression of FOXL2 in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 344: 353-361; doi: 10.1016/j.bbrc.2006.03.137.
109. Nakamoto M, Wang D-S, Suzuki A, Matsuda M, Nagahama Y, Shibata N. 2007. Dax1 suppresses P450arom expression in medaka ovarian follicles. Mol. Reprod. Dev. 74(10): 1239-1246; doi: 10.1002/mrd.20689.
110. Nakamura S, Aoki Y, Saito D, Kuroki Y, Fujiyama A, Naruse K, Tanaka M. 2008. SOX9b/SOX9a2-EGFP transgenic medaka reveals the morphological reorganization of the gonads and a common precursor of both the female and male supporting cells. Mol. Reprod. 75(3): 472-6; doi: 10.1002/mrd.20746.
111. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan ZH, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. 2002. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc. Natl Acad. Sci. USA 99(18): 11778-11783; doi: 10.1073/pnas.182314699.
112. Örn S, Holbech H, Madsen TH, Norrgren L, Petersen GI. 2003. Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat. Toxicol. 65(4): 397-411; doi: 10.1016/S0166-445X(03)00177-2.
113. Pailler J, Guignard C, Meyer B, Iffly J, Pfister L, Hoffmann L, Krein A. 2009. Behavior and fluxes of dissolved antibiotics, analgesics and hormones during flood events in a small heterogeneous catchment in the Grand Duchy of Luxembourg. Water Air Soil Pollut. 203: 79-98.
114. Pandian TJ, Sheela SG. 1995. Hormonal induction of sex reversal in fish. Aquaculture 138(1-4): 1-22; doi: 10.1016/0044-8486(95)01075-0.
115. Panter GH, Thompson RS, Sumpter JP. 1998. Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone. Aquat. Toxicol. 42(4): 243-253.
116. Park SY, Jameson JL. 2005. Minireview: transcriptional regulation of gonadal development and differentiation. Endocrinology 146(3): 1035-1042; doi: 10.1210/en.2004-1454.
117. Parrott JL, Beverley RB. 2005. Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1ng/L reduces egg fertilization success and demasculinizes males. Environ. Toxicol. 20(2): 131-141; doi: 10.1002/tox.20087.
118. Perner B, Englert C, Bollig F. 2007. The Wilms tumor genes WT1a and WT1b control different steps during formation of the zebrafish pronephros. Dev. Biol. 309: 87-96; doi: 10.1016/j.ydbio.2007.06.022.
119. Peters REM, Courtenay SC, Hewitt LM, MacLatchy DL. 2010. Effects of 17α-ethynylestradiol on early-life development, sex differentiation and vitellogenin induction in mummichog (Fundulus heteroclitus). Mar. Environ. Res. 69(3): 178-186; doi: 10.1016/j.marenvres.2009.10.002.
120. Piferrer F, Zanuy S, Carrillo M, Solar II, Devlin RH, Donaldson EM. 1994. Brief treatment with an aromatase inhibitor during sex differentiation causes chromosomally female salmon to develop as normal, functional males. J. Exp. Zool. 270(3): 255-262; doi: 10.1002/jez.1402700304.
121. Qi-Yan D, Feng-Yu W, Hui-Ying H, Zhong-Jie C. 2007. Cloning and study of adult-tissue-specific expression of Sox9 in Cyprinus carpio. J. Genet. 86: 85-91.
122. Quérat B, Sellouk A, Salmon C. 2000. Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) β subunits of the two gonadotropins and the thyroid-stimulating hormone. Biol. Reprod. 63(1): 222-228; doi: 10.1095/biolreprod63.1.222.
123. Raymond CS, Murphy MW, O'sullivan MG, Bardwell VJ, Zarkower D. 2000. DMRT1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Gene Dev. 14: 2587-2595; doi: 10.1101/gad.834100.
124. Rodríguez-Marí A, Yan Y-L, BreMiller RA, Wilson C, Cañestro C, Postlethwait JH. 2005. Characterization and expression pattern of zebrafish anti-Müllerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr. Patterns 5(5): 655-667; doi: 10.1016/j.modgep.2005.02.008.
125. Sandra G-E, Norma M-M. 2010. Sexual determination and differentiation in teleost fish. Rev. Fish Biol. 20(1): 101-121; doi: 10.1007/s11160-009-9123-4.
126. Sawyer SJ, Gerstner KA, Callard GV. 2006. Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: Gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen. Comp. Endocrinol. 147(2): 108-117.
127. Schlueter PJ, Sang X, Duan C, Wood AW. 2007. Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev. Biol. 305: 377-387; doi: 10.1016/j.ydbio.2007.02.015.
128. Seki M, Yokota H, Matsubara H, Maeda M, Tadokoro H, Kobayashi K. 2004. Fish full life-cycle testing for androgen methyltestosterone on medaka (Oryzias latipes). Environ. Toxicol. Chem. 23(3): 774-781; doi: 10.1897/03-26.
129. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf A-M, Lovell-Badge R, Goodfellow PN. 1990. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346(6281): 240-244; doi: 10.1038/346240a0.
130. Soto AM, Calabro JM, Prechtl NV, Yau AY, Orlando EF, Daxenberger A, Kolok AS, Guillette LJ, Jr, le Bizec B, Lange IG, Sonnenschein C. 2004. Androgenic and estrogenic activity in water bodies receiving cattle feedlot effluent in eastern Nebraska, USA. Environ. Health Perspect. 112(3): 346-352; doi: 10.1289/ehp.6590.
131. Swanson P, Suzuki K, Kawauchi H, Dickhoff WW. 1991. Isolation and characterization of two coho salmon gonadotropins, GTH I and GTH II. Biol. Reprod. 44(1): 29-38; doi: 10.1095/biolreprod44.1.29.
132. Takamatsu N, Kanda H, Ito M, Yamashita A, Yamashita S, Shiba T. 1997. Rainbow trout SOX9: cDNA cloning, gene structure and expression. Gene 202(1-2): 167-170; doi: 10.1016/S0378-1119(97)00483-6.
133. Tchoudakova A, Callard GV. 1998. Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology 139(4): 2179-2189; doi: 10.1210/en.139.4.2179.
134. Tchoudakova A, Kishida M, Wood E, Callard GV. 2001. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. 78(5): 427-439; doi: 10.1016/S0960-0760(01)00120-0.
135. Thomas KV, Hurst MR, Matthiessen P, McHugh M, Smith A, Waldock MJ. 2002. An assessment of in vitro androgenic activity identification of environmental androgens in United Kingdom estuaries. Environ. Toxicol. Chem. 21(7): 1456-1461.
136. Tong S-K, Chung B-c. 2003. Analysis of zebrafish cyp19 promoters. J. Steroid Biochem. 86(3-5): 381-386; doi: 10.1016/S0960-0760(03)00347-9.
137. Tong S-K, Chiang EF-l, Hsiao P-H, Chung B-c. 2001. Phylogeny, expression and enzyme activity of zebrafish cyp19 (P450 aromatase) genes. J. Steroid Biochem. 79(1-5): 299-303; doi: 10.1016/S0960-0760(01)00146-7.
138. Trant JM, Gavasso S, Ackers J, Chung B-C, Place AR. 2001. Developmental expression of cytochrome P450 aromatase genes (CYP19a and CYP19b) in zebrafish fry (Danio rerio). J. Exp. Zool. 290(5): 475-483; doi: 10.1002/jez.1090.
139. Tyler CR, van Aerle R, Hutchinson TH, Maddix S, Trip H. 1999. An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ. Toxicol. Chem. 18(2): 337-347; doi: 10.1002/etc.5620180234.
140. USEPA. 1999. Biosolids Generation, Use and Disposal in the United States. EPA530-R-99-009. Office of Solid Waste: Washington, DC.
141. USEPA. 2000. Proposed Regulations to Address Water Pollution from Concentrated Animal Feeding Operations. EPA 833-F-00-016. Office of Water: Washington, DC.
142. van Aerle R, Pounds N, Hutchinson TH, Maddix S, Tyler CR. 2002. Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow, Pimephales promelas. Ecotoxicology 11(6): 423-434.
143. Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y. 2007. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev. Dyn. 236(8): 2198-206; doi: 10.1002/dvdy.21212.
144. Von Hofsten J, Jones I, Karlsson J, Olsson PE. 2001. Developmental expression patterns of FTZ-f1 homologues in zebrafish (Danio rerio). Gen. Comp. Endocrinol. 121(2): 146-55; doi: 10.1006/gcen.2000.7582.
145. Wada H, Shimada A, Fukamachi S, Naruse K, Shima A. 1998. Sex-linked inheritance of the if locus in the medaka fish (Oryzias latipes). Zool. Sci. 15(1): 123-126; doi: 10.2108/zsj.15.123.
146. Wang DS, Kobayashi T, Zhou LY, Nagahama Y. 2004. Molecular cloning and gene expression of FOXL2 in the Nile tilapia, Oreochromis niloticus. Biochem. Biophys. Res. Commun. 320(1): 83-9; doi: 10.1016/j.bbrc.2004.05.133.
147. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi KI, Nagahama Y. 2007. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with Ad4 binding protein/steroidogenic factor 1. Mol. Endocrinol. 21(3): 712-725; doi: 10.1210/me.2006-0248.
148. Wang DS, Zhou LY, Kobayashi T, Matsuda M, Shibata Y, Sakai F, Nagahama Y. 2010. Doublesex- and mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology 151(3): 1331-1340; doi: 10.1210/en.2009-0999.
149. Warner RR. 1975. Adaptive significance of sequential hermaphroditism in animals. Am. Nat. 109: 61-82; doi: 10.1086/282974.
150. Watanabe T, Fujita H, Yamasaki K, Seki S, Taniguchi N. 2004. Preliminary study on linkage mapping based on microsatellite DNA and AFLP markers using homozygous clonal fish in ayu (Plecoglossus altivelis). Mar. Biotechnol. 6(4): 327-334; doi: 10.1007/s10126-003-0026-4.
151. Weber LP, Hill RL, Janz DM. 2003. Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. Aquat. Toxicol. 63(4): 431-446.
152. Xuan R, Blassengale AA, Wang Q. 2008. Degradation of estrogenic hormones in a silt loam soil. J. Agric. Food Chem. 56(19): 9152-9158; doi: 10.1021/jf8016942.
153. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T. 2007. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem. Biophys. Res. Commun. 359(4): 935-940; doi: 10.1016/j.bbrc.2007.05.208.
154. Ying G-G, Kookana RS. 2005. Sorption and degradation of estrogen-like-endocrine disrupting chemicals in soil. Environ. Toxicol. Chem. 24(10): 2640-2645; doi: 10.1897/05-074r.1.
155. Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Abe S, Kitano T. 2004. Sexually dimorphic expression of a teleost homologue of mullerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem. Biophys. Res. Commun. 322(2): 508-513; doi: 10.1016/j.bbrc.2004.07.162.
156. Žlábek V, Randák T, Kolářová J, Svobodová Z, Kroupová H. 2009. Sex differentiation and vitellogenin and 11-ketotestosterone levels in chub, Leuciscus cephalus L., exposed to 17 β-estradiol and testosterone during early development. Bulletin Environ. Contam. Toxicol. 82(3): 280-284.