Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 789–803 | Cite as

Diethylstilbestrol arrested spermatogenesis and somatic growth in the juveniles of yellow catfish (Pelteobagrus fulvidraco), a fish with sexual dimorphic growth

  • Zhi–Hao Liu
  • Qi–Liang Chen
  • Qiang Chen
  • Fang Li
  • Ying–Wen Li


In fish, spermatogenesis and somatic growth are mainly regulated by hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-somatic (HPS) axes, respectively. Xenoestrogens have been reported to impair spermatogenesis in some fishes, and arrest somatic growth in some others, whereas, whether xenoestrogens are capable of disrupting spermatogenesis and somatic growth simultaneously in fish that exhibits sexual dimorphic growth is little known, and the underlying mechanisms remain poorly understood. In this study, male juveniles of yellow catfish (Pelteobagrus fulvidraco), which exhibits a sexual dimorphic growth that favors males, were exposed to diethylstilbestrol (DES) for 28 days. After exposure, DES significantly disrupted the spermatogenesis (decreased gonadal-somatic index (GSI) and germ cell number) and arrested the somatic growth (declined body weight) of the catfish juveniles. Gene expression and plasma steroid analyses demonstrated the suppressed mRNA levels of genes in HPG axis (gnrh-II, fshβ, and lhβ in the brain and dmrt1, sf1, fshr, cyp17a1, cyp19a1a, and cyp11b2 in the testis) and decreased 17β-estrodial (E2) and 11-ketotestosterone (11-KT) levels in plasma. Further analysis revealed the arrested germ cell proliferation (cyclin d1), meiosis (dmc1, sycp3), and enhanced apoptosis (decreased bcl-2 and elevated bax/bcl-2 ratio) in the testis. Besides, DES also suppressed the mRNA levels of genes in HPS axis (ghrh, gh, and prl in the brain and ghr, igf1, igf2a, and igf2b in the liver). The suppressed HPG and HPS axes were thus supposed to disturb spermatogenesis and arrest somatic growth in yellow catfish. The present study greatly extended our understanding on the mechanisms underlying the toxicity of DES on spermatogenesis and somatic growth of fish.


Diethylstilbestrol Pelteobagrus fulvidraco Spermatogenesis Somatic growth HPG/HPS axis 


Funding information

This work was supported by the Chongqing Research Program of Basic Research and Frontier Technology (cstc2016jcyjA0133), the Scientific and Technological Research Program of Chongqing Municipal Education Commission (KJ130622, KJ1600308), the key project of Chongqing Normal University (13XLZ08), and the Open project fund of ‘Key laboratory of Freshwater Fish Reproduction and development (Ministry of Education, China) (FFRD-2015-02)’, China.


  1. Adedeji OB, Durhan EJ, Garcia-Reyero N, Kahl MD, Jensen KM, Lalone CA, Makynen EA, Perkins EJ, Thomas L, Villeneuve DL, Ankley GT (2009) Short-term study investigating the estrogenic potency of diethylstilbesterol in the fathead minnow (Pimephales promelas). Environ Sci Technol 46(14):7826–7835. CrossRefGoogle Scholar
  2. Ahmed SA (2000) The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 150(1-3):191–206. CrossRefPubMedGoogle Scholar
  3. Aitken RJ (2011) The capacitation-apoptosis highway: oxysterols and mammalian sperm function. Biol Reprod 85(1):9–12. CrossRefPubMedGoogle Scholar
  4. Arcand-Hoy LD, Benson WH (1998) Fish reproduction: and ecologically relevant indicator of endocrine disruption. Environ Toxicol Chem 17(1):49–57. CrossRefGoogle Scholar
  5. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7(5):812–821. CrossRefPubMedGoogle Scholar
  6. Baroiller JF, D'Cotta H, Shved N, Berishvili G, Toguyeni A, Fostier A, Eppler E, Reinecke M (2014) Oestrogen and insulin-like growth factors during the reproduction and growth of the tilapia Oreochromis niloticus and their interactions. Gen Comp Endocrinol 205:142–150. CrossRefPubMedGoogle Scholar
  7. Bondanelli M, Ambrosio MR, Margutti A, Franceschetti P, Zatelli MC, degli Uberti EC (2003) Activation of the somatotropic axis by testosterone in adult men: evidence for a role of hypothalamic growth hormone-releasing hormone. Neuroendocrinology 77:380–387, 6, DOI:
  8. Brander SM (2013) Thinking outside the box: assessing endocrine disruption in aquatic life. In: Ajuha S (ed) Monitoring water quality: pollution assessment, analysis, and remediation. Elsevier, Amsterdam, Netherlands, pp 103–145. CrossRefGoogle Scholar
  9. Chen W, Fan Z, Yang J (2006) Investigation of gonad histological structure of Pelteobagrus fluvidraco (Richardson). J Northeast Agric Univ (Chinese) 37:194–198Google Scholar
  10. Chen HC, Kuo HW, Ding WH (2009) Determination of estrogenic compounds in wastewater using liquid chromatography-tandem mass spectrometry with electrospray and atmospheric pressure photoionization following desalting extraction. Chemosphere 74(4):508–514. CrossRefPubMedGoogle Scholar
  11. 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(16):3223–3230. CrossRefPubMedGoogle Scholar
  12. Chimento A, Sirianni R, Casaburi I, Pezzi V (2014) Role of estrogen receptors and g protein-coupled estrogen receptor in regulation of hypothalamus-pituitary-testis axis and spermatogenesis. Front Endocrinol (Lausanne) 5:1. CrossRefGoogle Scholar
  13. Chu L, Li J, Liu Y, Cheng CH (2015) Gonadotropin signaling in zebrafish ovary and testis development: insights from gene knockout study. Mol Endocrinol 29(12):1743–1758. CrossRefPubMedCentralPubMedGoogle Scholar
  14. Davis LK, Pierce AL, Hiramatsu N, Sullivan CV, Hirano T, Grau EG (2008) Gender-specific expression of multiple estrogen receptors, growth hormone receptors, insulin-like growth factors and vitellogenins, and effects of 17 beta-estradiol in the male tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 156(3):544–551. CrossRefPubMedGoogle Scholar
  15. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30(4):293–342. CrossRefPubMedCentralPubMedGoogle Scholar
  16. Duan C (1997) The insulin-like growth factor system and its biological actions in fish. Am Zool 37(6):491–503. CrossRefGoogle Scholar
  17. Dunkel L, Hirvonen V, Erkkilä K (1997) Clinical aspects of male germ cell apoptosis during testis development and spermatogenesis. Cell Death Differ 4(3):171–179. CrossRefPubMedGoogle Scholar
  18. 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. CrossRefPubMedGoogle Scholar
  19. Gillio Meina E, Lister A, Bosker T, Servos M, Munkittrick K, MacLatchy D (2013) Effects of 17α-ethinylestradiol (EE2) on reproductive endocrine status in mummichog (Fundulus heteroclitus) under differing salinity and temperature conditions. Aquat Toxicol 134–135:92–103. CrossRefPubMedGoogle Scholar
  20. Giusti RM, Iwamoto K, Hatch EE (1995) Diethylstilbestrol revisited: a review of the long-term health effects. Ann Intern Med 122(10):778–788. CrossRefPubMedGoogle Scholar
  21. Grey CL, Chang JP (2013) Growth hormone-releasing hormone stimulates GH release while inhibiting ghrelin- and sGnRH-induced LH release from goldfish pituitary cells. Gen Comp Endocrino 186:150–156. CrossRefGoogle Scholar
  22. Gui JF, Zhu ZY (2012) Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull 57(15):1751–1760. CrossRefGoogle Scholar
  23. Guyón NF, Roggio MA, Amé MV, Hued AC, Valdés ME, Giojalas LC, Wunderlin DA, Bistoni MA (2012) Impairments in aromatase expression, reproductive behavior, and sperm quality of male fish exposed to 17β-estradiol. Environ Toxicol Chem 31(5):935–940. CrossRefPubMedGoogle Scholar
  24. Hatef A, Alavi SM, Abdulfatah A, Fontaine P, Rodina M, Linhart O (2012) Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicol Environ Saf 76(2):56–62. CrossRefPubMedGoogle Scholar
  25. He YJ, Chen W, Zheng XY, Wang XN, Huang X (2013) Fate and removal of typical pharmaceuticals and personal care products by three different treatment processes. Sci Total Environ 447:248–254. CrossRefPubMedGoogle Scholar
  26. Herbst AL, Ulfelder H, Poskanzer DC (1971) Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 284(16):878–881. CrossRefPubMedGoogle Scholar
  27. Holloway AC, Leatherland JF (1997) Effect of gonadal steroid hormones on plasma growth hormone concentrations in sexually immature rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 105(2):246–254. CrossRefPubMedGoogle Scholar
  28. Huang Y, Wang XL, Zhang JW, KS W (2015) Impact of endocrine-disrupting chemicals on reproductive function in zebrafish (Danio rerio). Reprod Domest Anim 50(1):1–6. CrossRefPubMedGoogle Scholar
  29. Jiao B, Huang X, Chan CB, Zhang L, Wang D, Cheng CH (2006) The co-existence of two growth hormone receptors in teleost fish and their differential signal transduction, tissue distribution and hormonal regulation of expression in seabream. J Mol Endocrinol 36(1):23–40. CrossRefPubMedGoogle Scholar
  30. Kajiura-Kobayashi H, Kobayashi T, Nagahama Y (2005) Cloning of cDNAs and the differential expression of A-type cyclins and Dmc1 during spermatogenesis in the Japanese eel, a teleost fish. Dev Dyn 232(4):1115–1123. CrossRefPubMedGoogle Scholar
  31. Kebir O, Krebs MO (2012) Diethylstilbestrol and risk of psychiatric disorders: a critical review and new insights. World J Biol Psychiatry 13(2):84–95. CrossRefPubMedGoogle Scholar
  32. Kinnberg K, Toft G (2003) Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicol Environ Saf 54(1):16–24. CrossRefPubMedGoogle Scholar
  33. Lee LT, Siu FK, Tam JK, Lau IT, Wong AO, Lin MC, Vaudry H, Chow BK (2007) Discovery of growth hormone-releasing hormones and receptors in nonmammalian vertebrates. Proc Natl Acad Sci U S A 104(7):2133–2138. CrossRefPubMedCentralPubMedGoogle Scholar
  34. Leet JK, Gall HE, Sepúlveda MS (2011) A review of studies on androgen and estrogen exposure in fish early life stages: effects on gene and hormonal control of sexual differentiation. J Appl Toxicol 31(5):379–398. CrossRefPubMedGoogle Scholar
  35. Lei B, Huang S, Zhou Y, Wang D, Wang Z (2009) Levels of six estrogens in water and sediment from three rivers in Tianjin area, China. Chemosphere 76(1):36–42. CrossRefPubMedGoogle Scholar
  36. Lei B, Peng W, Li W, Yu Y, Xu J, Wang Y (2016) Diethylstilbestrol at environmental levels affects the development of early life stage and target gene expression in Japanese Medaka (Oryzias latipes). Ecotoxicology 25(3):563–573. CrossRefPubMedGoogle Scholar
  37. Li MH, Yang HH, Li MR, Sun YL, Jiang XL, Xie QP, Wang TR, Shi HJ, Sun LN, Zhou LY, Wang DS (2013) Antagonistic roles of Dmrt1 and Foxl2 in sex differentiation via estrogen production in tilapia as demonstrated by TALENs. Endocrinology 154(12):4814–4825. CrossRefPubMedGoogle Scholar
  38. Liu H, Guan B, Xu J, Hou C, Tian H, Chen H (2013) Genetic manipulation of sex ratio for the large-scale breeding of YY super-male and XY all-male yellow catfish (Pelteobagrus fulvidraco (Richardson)). Mar Biotechnol (NY) 15(3):321–328. CrossRefGoogle Scholar
  39. Lubick N (2009) India’s drug problem. Nature 457(7230):640–641. CrossRefPubMedGoogle Scholar
  40. Luzio A, Matos M, Santos D, Fontaínhas-Fernandes AA, Monteiro SM, Coimbra AM (2016) Disruption of apoptosis pathways involved in zebrafish gonad differentiation by 17α-ethinylestradiol and fadrozole exposures. Aquat Toxicol 177:269–284. CrossRefPubMedGoogle Scholar
  41. Lynn SG, Wallat GK, Malison JA, Shepherd BS (2011) Developmental expression and estrogen responses of endocrine genes in juvenile yellow perch (Perca flavescens). Gen Comp Endocrinol 171(2):151–159. CrossRefPubMedGoogle Scholar
  42. Ma X, Liu X, Zhang Y, Zhu P, Ye W, Lin H (2007a) Two growth hormone receptors in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and expression profiles in the gonad during the reproductive cycle. Comp Biochem Physiol B Biochem Mol Biol 147(2):325–339. CrossRefPubMedGoogle Scholar
  43. Ma M, Rao K, Wang Z (2007b) Occurrence of estrogenic effects in sewage and industrial wastewaters in Beijing, China. Environ Pollut 147(2):331–336. CrossRefPubMedGoogle Scholar
  44. Ma Q, Liu SF, Zhuang ZM, Sun ZZ, Liu CL, Tang QS (2012) The co-existence of two growth hormone receptors and their differential expression profiles between female and male tongue sole (Cynoglossus semilaevis). Gene 511(2):341–352. CrossRefPubMedGoogle Scholar
  45. Ma W, Wu J, Zhang J, He Y, Gui J, Mei J (2016) Sex differences in the expression of GH/IGF axis genes underlie sexual size dimorphism in the yellow catfish (Pelteobagrus fulvidraco). Sci China Life Sci 59(4):431–433. CrossRefPubMedGoogle Scholar
  46. Mailand N, Gibbs-Seymour I, Bekker-Jensen S (2013) Regulation of PCNA-protein interactions for genome stability. Nat Rev Mol Cell Biol 14(5):269–282. CrossRefPubMedGoogle Scholar
  47. McLachlan JA (2016) Environmental signaling: from environmental estrogens to endocrine-disrupting chemicals and beyond. Andrology 4(4):684–694. CrossRefPubMedGoogle Scholar
  48. Mei J, Gui JF (2015) Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sci China Life Sci 58(2):124–136. CrossRefPubMedGoogle Scholar
  49. Meinhardt UJ, Ho KK (2006) Modulation of growth hormone action by sex steroids. Clin Endocrinol 65(4):413–422. CrossRefGoogle Scholar
  50. Miller HD, Clark BW, Hinton DE, Whitehead A, Martin S, Kwok KW, Kullman SW (2012) Anchoring ethinylestradiol induced gene expression changes with testicular morphology and reproductive function in the medaka. PLoS One 7(12):e52479. CrossRefPubMedCentralPubMedGoogle Scholar
  51. Moldovan GL, Pfander B, Jentsch S (2007) PCNA, the maestro of the replication fork. Cell 129(4):665–679. CrossRefPubMedGoogle Scholar
  52. Morais RD, Thomé RG, Santos HB, Bazzoli N, Rizzo E (2016) Relationship between bcl-2, bax, beclin-1, and cathepsin-D proteins during postovulatory follicular regression in fish ovary. Theriogenology 85(6):1118–1131. CrossRefPubMedGoogle Scholar
  53. Nader MR, Miura T, Ando N, Miura C, Yamauchi K (1999) Recombinant human insulin-like growth factor I stimulates all stages of 11-ketotestosterone-induced spermatogenesis in the Japanese eel, Anguilla japonica, in vitro. Biol Reprod 61(4):944–947. CrossRefPubMedGoogle Scholar
  54. Naderi M, Safahieh A, Madiseh SD, Zolgharnein H, Ghatrami ER (2015) Induction of vitellogenin synthesis in immature male yellowfin seabream (Acanthopagrus latus) exposed to 4-nonylphenol and 17β-estradiol. Toxicol Ind Health 31(3):209–220. CrossRefPubMedGoogle Scholar
  55. Newbold RR (2011) Developmental exposure to endocrine-disrupting chemicals programs for reproductive tract alterations and obesity later in life. Am J Clin Nut 94(6_Suppl):1939S–1942S. CrossRefGoogle Scholar
  56. Norbeck LA, Sheridan MA (2011) An in vitro model for evaluating peripheral regulation of growth in fish: effects of 17β-estradiol and testosterone on the expression of growth hormone receptors, insulin-like growth factors, and insulin-like growth factor type 1 receptors in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 173(2):270–280. CrossRefPubMedGoogle Scholar
  57. Ozaki Y, Saito K, Shinya M, Kawasaki T, Sakai N (2011) Evaluation of Sycp3, Plzf and cyclin B3 expression and suitability as spermatogonia and spermatocyte markers in zebrafish. Gene Expr Patterns 11(5-6):309–315. CrossRefPubMedGoogle Scholar
  58. Panter GH, Hutchinson TH, Länge R, Lye CM, Sumpter JP, Zerulla M, Tyler CR (2002) Utility of a juvenile fathead minnow screening assay for detecting (anti-)estrogenic substances. Environ Toxicol Chem 21(2):319–326. CrossRefPubMedGoogle Scholar
  59. Paul-Prasanth B, Shibata Y, Horiguchi R, Nagahama (2011) Y exposure to diethylstilbestrol during embryonic and larval stages of medaka fish (Oryzias latipes) leads to sex reversal in genetic males and reduced gonad weight in genetic females. Endocrinology 152: 707–717. doi:, 2.
  60. Phumyu N, Boonanuntanasarn S, Jangprai A, Yoshizaki G, Na-Nakorn U (2012) Pubertal effects of 17α-methyltestosterone on GH-IGF-related genes of the hypothalamic-pituitary-liver-gonadal axis and other biological parameters in male, female and sex-reversed Nile tilapia. Gen Comp Endocrinol 177(2):278–292. CrossRefPubMedGoogle Scholar
  61. Pojana G, Gomiero A, Jonkers N, Marcomini A (2007) Natural and synthetic endocrine disrupting compounds (EDCs) in water, sediment and biota of a coastal lagoon. Environ In 33:929–936Google Scholar
  62. Qian Y, Yan A, Lin H, Li W (2012) Molecular characterization of the GHRH/GHRH-R and its effect on GH synthesis and release in orange-spotted grouper (Epinephelus coioides). Comp Biochem Physiol B Biochem Mol Biol 163(2):229–237. CrossRefPubMedGoogle Scholar
  63. Qin F, Wang X, Liu S, Zheng Y, Li M, Zhang Y, Wang Z (2014) Gene expression profiling of key genes in hypothalamus-pituitary-gonad axis of rare minnow Gobiocypris rarus in response to EE2. Gene 552(1):8–17. CrossRefPubMedGoogle Scholar
  64. Rajakumar A, Singh R, Chakrabarty S, Murugananthkumar R, Laldinsangi C, Prathibha Y, Sudhakumari CC, Dutta-Gupta A, Senthilkumaran B (2012) Endosulfan and flutamide impair testicular development in the juvenile Asian catfish, Clarias batrachus. Aquat Toxicol 110-111:123–132. CrossRefPubMedGoogle Scholar
  65. Raun AP, Preston RL (2001) History of diethystilbestrol use in cattle. Am Soc Anim Sci 80: 1–7.Google Scholar
  66. Reinecke M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone-insulin-like growth factor-I system. J Fish Biol 76(6):1233–1254. CrossRefPubMedGoogle Scholar
  67. Reinecke M, Björnsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutiérrez J (2005) Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142(1-2):20–24. CrossRefPubMedGoogle Scholar
  68. Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J (2005) Duplication of growth hormone receptor (GHR) in fish genome: gene organization and transcriptional regulation of GHR type I and II in gilthead sea bream (Sparus aurata). Gen Comp Endocrinol 142(1-2):193–203. CrossRefPubMedGoogle Scholar
  69. Sakamoto T, McCormick SD (2006) Prolactin and growth hormone in fish osmoregulation. Gen Comp Endocrinol 147(1):24–30. CrossRefPubMedGoogle Scholar
  70. Sambroni E, Lareyre JJ, Le Gac F (2013) Fsh controls gene expression in fish both independently of and through steroid mediation. PLoS One 8(10):e76684. CrossRefPubMedCentralPubMedGoogle Scholar
  71. Sansam CL, Pezza RJ (2015) Connecting by breaking and repairing: mechanisms of DNA strand exchange in meiotic recombination. FEBS J 282(13):2444–2457. CrossRefPubMedCentralPubMedGoogle Scholar
  72. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108. CrossRefGoogle Scholar
  73. Schulz RW, Miura T (2002) Spermatogenesis and its endocrine regulation. Fish Physiol Biochem 26(1):43–56. CrossRefGoogle Scholar
  74. Schulz RW, de França LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165(3):390–411. CrossRefGoogle Scholar
  75. Sena GC, Freitas-Lima LC, Merlo E, Podratz PL, de Araújo JF, Brandão PA, Carneiro MT, Zicker MC, Ferreira AV, Takiya CM, de Lemos Barbosa CM, Morales MM, Santos-Silva AP, Miranda-Alves L, Silva IV, Graceli JB (2017) Environmental obesogen tributyltin chloride leads to abnormal hypothalamic-pituitary-gonadal axis function by disruption in kisspeptin/leptin signaling in female rats. Toxicol Appl Pharmacol 319:22–38. CrossRefPubMedGoogle Scholar
  76. Shved N, Berishvili G, D'Cotta H, Baroiller JF, Segner H, Eppler E, Reinecke M (2007) Ethinylestradiol differentially interferes with IGF-I in liver and extrahepatic sites during development of male and female bony fish. J Endocrinol 195(3):513–523. CrossRefPubMedGoogle Scholar
  77. Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161(1):20–29. CrossRefPubMedGoogle Scholar
  78. Sridevi P, Chaitanya RK, Prathibha Y, Balakrishna SL, Dutta-Gupta A, Senthilkumaran B (2015) Early exposure of 17α-ethynylestradiol and diethylstilbestrol induces morphological changes and alters ovarian steroidogenic pathway enzyme gene expression in catfish, Clarias gariepinus. Environ Toxico 30(4):439–451. CrossRefGoogle Scholar
  79. Swapna I, Senthilkumaran B (2009) Influence of ethynylestradiol and methyltestosterone on the hypothalamo-hypophyseal-gonadal axis of adult air-breathing catfish, Clarias gariepinus. Aquat Toxicol 95(3):222–229. CrossRefPubMedGoogle Scholar
  80. Syrjänen JL, Pellegrini L, Davies OR (2014) A molecular model for the role of SYCP3 in meiotic chromosome organisation. elife 3.
  81. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61(3):283–357. CrossRefPubMedGoogle Scholar
  82. de Waal PP, Leal MC, García-López A, Liarte S, de Jonge H, Hinfray N, Brion F, Schulz RW, Bogerd J (2009) Oestrogen-induced androgen insufficiency results in a reduction of proliferation and differentiation of spermatogonia in the zebrafish testis. J Endocrinol 202(2):287–297. CrossRefPubMedGoogle Scholar
  83. 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(3):712–725. CrossRefPubMedGoogle Scholar
  84. Wang DS, Jiao B, Hu C, Huang X, Liu Z, Cheng CH (2008) Discovery of a gonad-specific IGF subtype in teleost. Biochem Biophys Res Commun 367(2):336–341. CrossRefPubMedGoogle Scholar
  85. Wang L, Ying GG, Zhao JL, Liu S, Yang B, Zhou LJ, Tao R, HC S (2011) Assessing estrogenic activity in surface water and sediment of the Liao River system in northeast China using combined chemical and biological tools. Environ Pollut 159(1):148–156. CrossRefPubMedGoogle Scholar
  86. Wang Y, Li Y, Chen Q, Liu Z (2017) Diethylstilbestrol impaired oogenesis of yellow catfish juveniles through disrupting hypothalamic-pituitary-gonadal axis and germ cell development. J Appl Toxicol.
  87. Wang Y, Xu L, Li D, Teng M, Zhang R, Zhou Z, Zhu W (2015) Enantioselective bioaccumulation of hexaconazole and its toxic effects in adult zebrafish (Danio rerio). Chemosphere 138:798–805. CrossRefPubMedGoogle Scholar
  88. Whittington CM, Wilson AB (2013) The role of prolactin in fish reproduction. Gen Comp Endocrinol 191:123–136. CrossRefPubMedGoogle Scholar
  89. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285. CrossRefPubMedGoogle Scholar
  90. Wu L, Yang P, Luo F, Wang D, Zhou L (2016) R-spondin1 signaling pathway is required for both the ovarian and testicular development in a teleosts, Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 230–231:177–185. CrossRefPubMedGoogle Scholar
  91. Yang L, Lin L, Weng S, Feng Z, Luan T (2008) Sexually disrupting effects of nonylphenol and diethylstilbestrol on male silver carp (Carassius auratus) in aquatic microcosms. Ecotoxicol Environ Saf 71(2):400–411. CrossRefPubMedGoogle Scholar
  92. Ye X, Guo X, Cui X, Zhang X, Zhang H, Wang MK, Qiu L, Chen S (2012) Occurrence and removal of endocrine-disrupting chemicals in wastewater treatment plants in the Three Gorges Reservoir area, Chongqing, China. J Environ Monit 14(8):2204–2211. CrossRefPubMedGoogle Scholar
  93. Yin P, Li YW, Chen QL, Liu ZH (2017) Diethylstilbestrol, flutamide and their combination impaired the spermatogenesis of male adult zebrafish through disrupting HPG axis, meiosis and apoptosis. Aquat Toxicol 185:129–137. CrossRefPubMedGoogle Scholar
  94. Zhang X, Gao Y, Li Q, Li G, Guo Q, Yan C (2011) Estrogenic compounds and estrogenicity in surface water, sediments, and organisms from Yundang Lagoon in Xiamen, China. Arch Environ Contam Toxicol 61(1):93–100. CrossRefPubMedGoogle Scholar
  95. Zhang X, Wang H, Li M, Cheng Y, Jiang D, Sun L, Tao W, Zhou L, Wang Z, Wang D (2014) Isolation of doublesex- and mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia. Biol Reprod 91:136. CrossRefPubMedGoogle Scholar
  96. Zhang J, Ma W, He Y, Wu J, Dawar FU, Ren F, Zhao X, Mei J (2016) Sex biased expression of ghrelin and GHSR associated with sexual size dimorphism in yellow catfish. Gene 578(2):169–176. CrossRefPubMedGoogle Scholar
  97. Zhang J, Ma W, He Y, Dawar FU,2, Xiong S, Mei J (2017) Potential contributions of miR-200a/-200b and their target gene-leptin to the sexual size dimorphism in yellow catfish. Front Physiol 8:970. doi:
  98. Zhong X, Xu Y, Liang Y, Liao T, Wang J (2005) The Chinese rare minnow (Gobiocypris rarus) as an in vivo model for endocrine disruption in freshwater teleosts: a full life-cycle test with diethylstilbestrol. Aquat Toxicol 71(1):85–95. CrossRefPubMedGoogle Scholar
  99. Zhou LY, Wang DS, Shibata Y, Paul-Prasanth B, Suzuki A, Nagahama Y (2007) Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka, Oryzias latipes. Biochem Biophys Res Commun 362(3):619–625. CrossRefPubMedGoogle Scholar
  100. Zou JJ, Trudeau VL, Cui Z, Brechin J, Mackenzie K, Zhu Z, Houlihan DF, Peter RE (1997) Estradiol stimulates growth hormone production in female goldfish. Gen Comp Endocrinol 106(1):102–112. CrossRefPubMedGoogle Scholar
  101. Zou S, Kamei H, Modi Z, Duan C (2009) Zebrafish IGF genes: gene duplication, conservation and divergence, and novel roles in midline and notochord development. PLoS One 4(9):e7026. CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Zhi–Hao Liu
    • 1
  • Qi–Liang Chen
    • 1
  • Qiang Chen
    • 1
  • Fang Li
    • 1
  • Ying–Wen Li
    • 1
  1. 1.Chongqing Key Laboratory of Animal Biology, College of Life SciencesChongqing Normal UniversityChongqingChina

Personalised recommendations