Molecular cloning of Foxl2 gene and the effects of endocrine-disrupting chemicals on its mRNA level in rare minnow, Gobiocypris rarus

Fish Physiology and Biochemistry

Volumn 38, Issue 3, 2012, Pages 653-664

  Wang, Houpeng ^a   Wu, Tingting ^a   Qin, Fang ^a   Wang, Lihong ^a   Wang, Zaizhao ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Endocrine disrupting chemicals; Foxl2; Gobiocypris rarus; Real time PCR

Indexed keywords

4 NONYLPHENOL; 4,4' ISOPROPYLIDENEDIPHENOL; 4-NONYLPHENOL; AROMATASE; COMPLEMENTARY DNA; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; FISH PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; MESSENGER RNA; PHENOL DERIVATIVE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CYPRINIFORMES; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OVARY; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SEX DIFFERENTIATION; TISSUE DISTRIBUTION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; AROMATASE; BASE SEQUENCE; CLONING, MOLECULAR; CYPRINIDAE; DNA, COMPLEMENTARY; ENDOCRINE DISRUPTORS; ETHINYL ESTRADIOL; FEMALE; FISH PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOLECULAR SEQUENCE DATA; OVARY; PHENOLS; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SEX DIFFERENTIATION; TISSUE DISTRIBUTION; UP-REGULATION;

CYPRINIDAE; GOBIOCYPRIS RARUS; MAMMALIA; VERTEBRATA;

EID: 84860884418     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-011-9548-2     Document Type: Article

References (68)

1. Alam MA, Horiguchi R, Kobayashi Y, Hirai T, Nakamura M (2008) Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra. Gen Comp Endocrinol 157: 75-85.
2. Atkinson S, Atkinson MJ, Tarrant AM (2003) Estrogens from sewage in coastal marine environments. Environ Health Perspect 111: 531-535.
3. Baron D, Cocquet J, Xia X, Fellous M, Guiguen Y, Veitia RA (2004) An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J Mol Endocrinol 33: 705-715.
4. Baron D, Batista F, Chaffaux S, Cocquet J, Cotinot C, Cribiu E, De Baere E, Guiguen Y, Jaubert F, Pailhoux E, Pannetier M, Vaiman D, Vigier B, Veitia R, Fellous M (2005) Foxl2 gene and the development of the ovary: a story about goat, mouse, fish and woman. Reprod Nutr Dev 45: 377-382.
5. Belaid B, Richard-Mercier N, Pieau C, Dorizzi M (2001) Sex reversal and aromatase in the European pond turtle: treatment with letrozole after the thermosensitive period for sex determination. J Exp Zool 290: 490-497.
6. Biles JE, McNeal TP, Begley TH, Hollifield HC (1997) Determination of bisphenol-A in reusable polycarbonate food-contact plastics and migration to food-stimulating liquids. J Agric Food Chem 45: 3541-3544.
7. Bjerselius R, Lundstedt-Enkel K, Olsén H, Mayer I, Dimberg K (2001) Male goldfish reproductive behavior and physiology are severely affected by exogenous exposure to 17β-estradiol. Aquat Toxicol 53: 139-152.
8. Blázquez M, Gonzalez A, Papadaki M, Mylonas C, Piferrer F (2008) Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 158: 95-101.
9. Brotons JA, Olea-Serrano MF, Villalobos M, Pedraza V, Olea N (1995) Xenoestrogens released from lacquer coating in food cans. Environ Health Perspect 103: 608-612.
10. Chardard D, Dournon C (1999) Sex reversal by aromatase inhibitor treatment in the newt Pleurodeles waltl. J Exp Zool 283: 43-50.
11. Cheshenko K, Pakdel F, Segner H, Kah O, Eggen RI (2008) Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish. Gen Comp Endocrinol 155: 31-62.
12. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Baere E, Messiaen L, Cotinot C, Fellous M, Veitia RA (2002) Evolution and expression of FOXL2. J Med Genet 39: 916-922.
13. Conley A, Hinshelwood M (2001) Mammalian aromatases. Reproduction 121: 685-695.
14. Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L, Nagaraja R, Porcu S, Ristaldi MS, Marzella R, Rocchi M, Nicolino M, Lienhardt-Roussie A, Nivelon A, Verloes A, Schlessinger D, Gasparini P, Bonneau D, Cao A, Pilia G (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet 27: 159-166.
15. Elbrecht A, Smith RG (1992) Aromatase enzyme activity and sex determination in chickens. Science 255: 467-470.
16. Ellsworth BS, Burns AT, Escudero KW, Duval DL, Nelson SE, Clay CM (2003) The gonadotropin releasing hormone (GnRH) receptor activating sequence (GRAS) is a composite regulatory element that interacts with multiple classes of transcription factors including Smads, AP-1 and a forkhead DNA binding protein. Mol Cell Endocrinol 206: 93-111.
17. Esterhuyse MM, Helbing CC, van Wyk JH (2008) Temporal expression of two Cytochrome P450 Aromatase isoforms during development in Oreochromis mossambicus, in association with histological development. Comp Biochem Physiol D 3: 297-306.
18. Fenske M, Segner H (2004) Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat Toxicol 67: 105-126.
19. Galay-Burgos M, Gealy C, Navarro-Martin L, Piferrer F, Zanuy S, Sweeney GE (2006) Cloning of the promoter from the gonadal aromatase gene of the European sea bass and identification of single nucleotide polymorphisms. Comp Biochem Physiol A 145: 47-53.
20. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, Couty I, Batellier F, Cotinot C (2004) Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn 231: 859-870.
21. Guiguen Y, Baroiller JF, Ricordel MJ, Iseki K, McMeel OM, Martin SA, 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: 154-162.
22. Hill RL Jr, Janz DM (2003) Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat Toxicol 63: 417-429.
23. Hudson QJ, Smith CA, Sinclair AH (2005) Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 233: 1052-1055.
24. Ijiri S, Kaneko H, Kobayashi T, Wang DS, 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: 333-341.
25. Kanda H, Okubo T, Omori N, Niihara H, Matsumoto N, Yamada K, Yoshimoto S, Ito M, Yamashita S, Shiba T, Takamatsu N (2006) Transcriptional regulation of the rainbow trout CYP19a gene by FTZ-F1 homologue. J. Steroid Biochem. Mol Biol 99: 85-92.
26. Kaufmann E, Knochel W (1996) Five years on the wings of fork head. Mech Dev 57: 3-20.
27. Kazeto Y, Place AR, Trant JM (2004) Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat Toxicol 69: 25-34.
28. Khim JS, Lee KT, Kannan K, Villeneuve DL, Giesy JP, Koh CH (2001) Trace organic contaminants in sediment and water from Ulsan Bay and its vicnity, Kerea. Arch Environ Contam Toxicol 40: 141-150.
29. 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: 289-294.
30. Lange R, Hutchinson TH, Croudace CP, Siegmund F, Scheweinfurth 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: 1216-1227.
31. Lee YM, Seo JS, Kim IC, Yoon YD, Lee JS (2006) Endocrine disrupting chemicals (bisphenol A, 4-nonylphenol, 4-tert-octylphenol) modulate expression of two distinct cytochrome P450 aromatase genes differently in gender types of the hermaphroditic fish Rivulus marmoratus. Biochem Biophys Res Commun 345: 894-903.
32. Liao T, Guo QL, Jin SW, Cheng W, Xu Y (2009) Comparative responses in rare minnow exposed to 17β-estradiol during different life stages. Fish Physiol Biochem 35: 341-349.
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
34. 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.
35. Miyata S, Kubo T (2000) In vitro effects of estradiol and aromatase inhibitor treatment on sex differentiation in Xenopus laevis gonads. Gen Comp Endocrinol 119: 105-110.
36. Monteiro PR, Reis-Henriques MA, Coimbra J (2000) Plasma steroid levels in female flounder (Platichthys flesus) after chronic dietary exposure to single polycyclic aromatic hydrocarbons. Mar Environ Res 49: 453-467.
37. Nagahama Y, Nakamura M, Kitano T, Tokumoto T (2004) Sexual plasticity in fish: a possible target of endocrine disruptor action. Environ Sci 11: 73-82.
38. Naimi A, Martinez AS, Specq ML, Diss B, Mathieu M, Sourdaine P (2009) Molecular cloning and gene expression of Cg-Foxl2 during the development and the adult gametogenetic cycle in the oyster Crassostrea gigas. Comp Biochem Physiol B 154: 134-142.
39. 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.
40. Noaksson E, Linderoth M, Bosveld ATC, Balka L (2003) Altered steroid metabolism in several teleost species exposed to endocrine disrupting substances in refuse dump leachate. Gen Comp Endocrinol 134: 273-284.
41. Olea N, Pulger R, Perez P, Olea-Serrano MF, Rivas A, NovilloFertrell A, Pedraza V, Soto AM, Sonnenschein C (1996) Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104: 298-305.
42. Orn 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: 397-411.
43. Oshima Y, Uno Y, Matsuda Y, Kobayashi T, Nakamura M (2008) Molecular cloning and gene expression of Foxl2 in the frog Rana rugosa. Gen Comp Endocrinol 159: 170-177.
44. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pepin B, Cotinot C, Veitia R, Pailhoux E (2006) FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 36: 399-413.
45. Patil JG, Gunasekera RM (2008) Tissue and sexually dimorphic expression of ovarian and brain aromatase mRNA in the Japanese medaka (Oryzias latipes): implications for their preferential roles in ovarian and neural differentiation and development. Gen Comp Endocrinol 158: 131-137.
46. Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197: 229-281.
47. Piferrer F, Blázquez M (2005) Aromatase distribution and regulation in fish. Fish Physiol Biochem 31: 215-226.
48. Rempel MA, Schlenk D (2008) Effects of environmental estrogens and antiandrogens on endocrine function, gene regulation, and health in fish. In: Jeon KW (ed) International review of cell and molecular biology, vol 267. Elsevier, Amsterdam, pp 251-296.
49. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C (1995) Endocrine sex reversal of gonads by the aromatase inhibitor Letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature dependent sex determination. Gen Comp Endocrinol 100: 314-326.
50. Sudhakumari CC, Senthilkumaran B, Kobayashi T, Kajiura-Kobayashi H, Wang DS, Yoshikuni M, Nagahama Y (2005) Ontogenic expression patterns of several nuclear receptors and cytochrome P450 aromatases in brain and gonads of the Nile tilapia Oreochromis niloticus suggests their involvement in sex differentiation. Fish Physiol Biochem 31: 129-135.
51. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
52. Tashiro Y, Takemura A, Fujii H, Takahira K, Nakanishi Y (2003) Livestock wastes as a source of estrogens and their effects on wildlife of Manko tidal flat, Okinawa. Mar Pollut Bull 47: 143-147.
53. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
54. Vaillant S, Guemene D, Dorizzi M, Pieau C, Richard-Mercier N, Brillard JP (2003) Degree of sex reversal as related to plasma steroid levels in genetic female chickens (Gallus domesticus) treated with Fadrozole. Mol Reprod Dev 65: 420-428.
55. Vizziano D, Baron D, Randuineau G, Mahe S, Cauty C, Guiguen Y (2008) Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation. Biol Reprod 78: 939-946.
56. Vizziano-Cantonnet D, Baron D, Mahe S, Cauty C, Fostier A, Guiguen Y (2008) Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal transdifferentiation. J Mol Endocrinol 41: 277-288.
57. Wang JW (1999) Spawning performance and development of oocytes in Gobiocypris rarus. Acta Hydrobiol Sin 23: 161-166.
58. Wang D, Kobayashi T, Zhou L, Nagahama Y (2004) Molecular cloning and gene expression of Foxl2 in the Nile tilapia, Oreochromis niloticus. Biochem Biophys Res Commun 320: 83-89.
59. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, 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: 712-725.
60. Wang J, Liu X, Wang H, Wu T, Hu X, Qin F, Wang Z (2010) Expression of two cytochrome P450 aromatase genes is regulated by endocrine disrupting chemicals in rare minnow Gobiocypris rarus juveniles. Comp Biochem Physiol C 152: 313-320.
61. Wang H, Wang J, Wu T, Qin F, Hu X, Wang L, Wang Z (2011) Molecular characterization of estrogen receptor genes in Gobiocypris rarus and their expression upon endocrine disrupting chemicals exposure in juveniles. Aquat Toxicol 101: 276-287.
62. Wartenberg H, Lenz E, Schweikert HU (1992) Sexual differentiation and the germ cell in sex reversed gonads after aromatase inhibition in the chicken embryo. Andrologia 24: 1-6.
63. Wibbels T, Crews D (1994) Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J Endocrinol 141: 295-299.
64. Wong TT, Shigeho I, Zohar Y (2006) Molecular biology of ovarian aromatase in sex reversal: complementary DNA and 50-flanking region isolation and differential expression of ovarian aromatase in the gilthead seabream (Sparus aurata). Biol Reprod 74: 857-864.
65. 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: 935-940.
66. Zha J, Wang Z, Wang N, Ingersoll C (2007) Histological alternation and vitellogenin induction in adult rare minnow (Gobiocypris rarus) after exposure to ethynylestradiol and nonylphenol. Chemosphere 66: 488-495.
67. Zha J, Sun L, Spear PA, Wang Z (2008a) Comparison of ethinylestradiol and nonylphenol effects on reproduction of Chinese rare minnows (Gobiocypris rarus). Ecotoxicol Environ Saf 71: 390-399.
68. Zha J, Sun L, Zhou Y, Spear PA, Ma M, Wang Z (2008b) Assessment of 17α-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow. Toxicol Appl Pharmacol 226: 298-308.