Differential expression of three estrogen receptors mRNAs in tissues, growth development, embryogenesis and gametogenesis from large yellow croaker, Larimichthys crocea

General and Comparative Endocrinology

Volumn 216, Issue , 2015, Pages 134-151

  Chen, Shihai ^a   Pu, Lulu ^a   Xie, Fangjing ^a   Zou, Zhihua ^a   Jiang, Yonghua ^a   Han, Kunhuang ^a,b   Wang, Yilei ^a   Zhang, Ziping ^c  

^a JIMEI UNIVERSITY   (China)

^b Ningde Fufa Fisheries Co Ltd   (China)

^c Center for Agriculture and Natural Resources   (United States)

Author keywords

Embryogenesis; Estrogen receptor; Gametogenesis; Growth development; In situ hybridization; Larimichthys crocea

Indexed keywords

ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA1; ESTROGEN RECEPTOR BETA2; MESSENGER RNA; UNCLASSIFIED DRUG; ESTROGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; GAMETOGENESIS; GENE EXPRESSION; GROWTH CURVE; IN SITU HYBRIDIZATION; LARIMICHTHYS CROCEA; LIVER LEVEL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SCIAENIDAE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; OOCYTE; OVARY FOLLICLE; OVULATION; PERCIFORMES; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TESTIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; EMBRYONIC DEVELOPMENT; ESTROGENS; FEMALE; GAMETOGENESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MALE; MOLECULAR SEQUENCE DATA; OOCYTES; OVARIAN FOLLICLE; OVULATION; PERCIFORMES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TESTIS;

EID: 84946233196     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2015.04.005     Document Type: Article

References (60)

1. Amer M.A., Miura T., Miura C., Yamauchi K. Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol. Reprod. 2001, 65:1057-1066.
2. Amores A., Force A., Yan Y.-L., Joly L., Amemiya C., Fritz A., Ho R.K., Langeland J., Prince V., Wang Y.-L. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
3. Bondesson M., Hao R., Lin C.-Y., Williams C., Gustafsson J.-Å. Estrogen receptor signaling during vertebrate development. BBA Gene Regul. Mech. 2014.
4. Bouma J., Nagler J.J. Estrogen receptor-alpha protein localization in the testis of the rainbow trout (Oncorhynchus mykiss) during different stages of the reproductive cycle. Biol. Reprod. 2001, 65:60-65.
5. Carreau S., Bouraima-Lelong H., Delalande C. Role of estrogens in spermatogenesis. Front. Biosci. (Elite edition) 2011, 4:1-11.
6. Celeghin A., Benato F., Pikulkaew S., Rabbane M.G., Colombo L., Dalla Valle L. The knockdown of the maternal estrogen receptor 2a (esr2a) mRNA affects embryo transcript contents and larval development in zebrafish. Gen. Comp. Endocrinol. 2011, 172:120-129.
7. Chakraborty T., Shibata Y., Zhou L.-Y., Katsu Y., Iguchi T., Nagahama Y. Differential expression of three estrogen receptor subtype mRNAs in gonads and liver from embryos to adults of the medaka, Oryzias latipes. Mol. Cell. Endocrinol. 2011, 333:47-54.
8. Chen H., Zhang Y., Li S., Lin M., Shi Y., Sang Q., Liu M., Zhang H., Lu D., Meng Z., Liu X., Lin H. Molecular cloning, characterization and expression profiles of three estrogen receptors in protogynous hermaphroditic orange-spotted grouper (Epinephelus coioides). Gen. Comp. Endocrinol. 2011, 172:371-381.
9. Cheskis B.J., Greger J.G., Nagpal S., Freedman L.P. Signaling by estrogens. J. Cell. Physiol. 2007, 213:610-617.
10. Choi C., Habibi H. Molecular cloning of estrogen receptor α and expression pattern of estrogen receptor subtypes in male and female goldfish. Mol. Cell. Endocrinol. 2003, 204:169-177.
11. Clark S., Rainville J., Zhao X., Katzenellenbogen B.S., PfaffD., Vasudevan N. Estrogen receptor-mediated transcription involves the activation of multiple kinase pathways in neuroblastoma cells. J. Steroid Biochem. Mol. Biol. 2014, 139:45-53.
12. Cotter K.A., Yershov A., Novillo A., Callard G.V. Multiple structurally distinct ERalpha mRNA variants in zebrafish are differentially expressed by tissue type, stage of development and estrogen exposure. Gen. Comp. Endocrinol. 2013, 194:217-229.
13. Coumailleau P., Pellegrini E., Adrio F., Diotel N., Cano-Nicolau J., Nasri A., Vaillant C., Kah O. Aromatase, estrogen receptors and brain development in fish and amphibians. BBA Gene Regul. Mech. 2014.
14. Diotel N., Vaillant C., Gabbero C., Mironov S., Fostier A., Gueguen M.-M., Anglade I., Kah O., Pellegrini E. Effects of estradiol in adult neurogenesis and brain repair in zebrafish. Horm. Behav. 2013, 63:193-207.
15. Fairall L., Schwabe J.W., Chapman L., Finch J.T., Rhodes D. The crystal structure of a two zinc-finger peptide reveals an extension to the rules for zinc-finger/DNA recognition. Nature 1993, 366:483-487.
16. Finn R.N., Kristoffersen B.A. Vertebrate vitellogenin gene duplication in relation to the "3R hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2007, 2:e169.
17. Griffin L.B., January K.E., Ho K.W., Cotter K.A., Callard G.V. Morpholino-mediated knockdown of ERalpha, ERbetaa, and ERbetab mRNAs in zebrafish (Danio rerio) embryos reveals differential regulation of estrogen-inducible genes. Endocrinology 2013, 154:4158-4169.
18. Gustafsson J.-Å. What pharmacologists can learn from recent advances in estrogen signalling. Trends Pharmcol. Sci. 2003, 24:479-485.
19. Hawkins M.B., Thomas P. The unusual binding properties of the third distinct teleost estrogen receptor subtype ERbetaa are accompanied by highly conserved amino acid changes in the ligand binding domain. Endocrinology 2004, 145:2968-2977.
20. Hawkins M.B., Thornton J.W., Crews D., Skipper J.K., Dotte A., Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl. Acad. Sci. USA 2000, 97:10751-10756.
21. Hu J., Sun S., Guo M., Song H. Use of antagonists and morpholinos in loss-of-function analyses: estrogen receptor ESR2a mediates the effects of 17alpha-ethinylestradiol on primordial germ cell distribution in zebrafish. Reprod. Biol. Endocrinol. 2014, 12:40.
22. Huang W., Zhang Y., Zheng S., Han K. The embryonic development of hybrids between chinese drum Miichthys miiuy ♀ and large yellow croaker Larimichthys crocea♂. Chin. J. Fish. 2014, 27:47-51.
23. Jalabert B. Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reprod. Nutr. Dev. 2005, 45:261-280.
24. Janz D.M., Van Der Kraak G. Suppression of apoptosis by gonadotropin, 17beta-estradiol, and epidermal growth factor in rainbow trout preovulatory ovarian follicles. Gen. Comp. Endocrinol. 1997, 105:186-193.
25. Kah O., Anglade I., Leprêtre E., Dubourg P., de Monbrison D. The reproductive brain in fish. Fish Physiol. Biochem. 1993, 11:85-98.
26. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S., Sasaki H., Masushige S., Gotoh Y., Nishida E., Kawashima H. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995, 270:1491-1494.
27. Kim B.-H., Takemura A., Kim S.J., Lee Y.-D. Vitellogenin synthesis via androgens in primary cultures of tilapia hepatocytes. Gen. Comp. Endocrinol. 2003, 132:248-255.
28. Kumar V., Green S., Stack G., Berry M., Jin J.-R., Chambon P. Functional domains of the human estrogen receptor. Cell 1987, 51:941-951.
29. Kwon H.C., Choi S.H., Kim Y.U., Son S.O., Kwon J.Y. Androgen action on hepatic vitellogenin synthesis in the eel, Anguilla japonica is suppressed by an androgen receptor antagonist. J. Steroid Biochem. Mol. Biol. 2005, 96:175-178.
30. Liu J. Study on the development of pseudosciaena crocea (Richardson) embryo and its morphological characteristics and the ecology of its larval, juvenile fish. Mar. Sci. 1999, 61-65.
31. Liu X., Su H., Zhu P., Zhang Y., Huang J., Lin H. Molecular cloning, characterization and expression pattern of androgen receptor in Spinibarbus denticulatus. Gen. Comp. Endocrinol. 2009, 160:93-101.
32. Lubzens E., Young G., Bobe J., Cerdà J. Oogenesis in teleosts: how fish eggs are formed. Gen. Comp. Endocrinol. 2010, 165:367-389.
33. MacKay M., Raelson J., Lazier C. Up-regulation of estrogen receptor mRNA and estrogen receptor activity by estradiol in liver of rainbow trout and other teleostean fish. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 1996, 115:201-209.
34. Meng X., Bartholomew C., Craft J.A. Differential expression of vitellogenin and oestrogen receptor genes in the liver of zebrafish, Danio rerio. Anal. Bioanal. Chem. 2010, 396:625-630.
35. Menuet A., Anglade I., Le Guevel R., Pellegrini E., Pakdel F., Kah O. Distribution of aromatase mRNA and protein in the brain and pituitary of female rainbow trout: comparison with estrogen receptor α. J. Comp. Neurol. 2003, 462:180-193.
36. Miura T., Miura C., Ohta T., Nader M.R., Todo T., Yamauchi K. Estradiol-17β stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Commun. 1999, 264:230-234.
37. Miura T., Miura C.I. Molecular control mechanisms of fish spermatogenesis. Fish Physiol. Biochem. 2003, 28:181-186.
38. Moens C. Whole mount RNA in situ hybridization on zebrafish embryos: probe synthesis. CSH Protoc. 2008, 2008. (pdb prot5036).
39. Mouriec K., Lareyre J.J., Tong S.K., Le Page Y., Vaillant C., Pellegrini E., Pakdel F., Chung B.C., Kah O., Anglade I. Early regulation of brain aromatase (cyp19a1b) by estrogen receptors during zebrafish development. Dev. Dyn. 2009, 238:2641-2651.
40. Nagler J.J., Cavileer T., Sullivan J., Cyr D.G., Rexroad C. The complete nuclear estrogen receptor family in the rainbow trout: discovery of the novel ERalpha2 and both ERbeta isoforms. Gene 2007, 392:164-173.
41. Nagler J.J., Krisfalusi M., Cyr D.G. Quantification of rainbow trout (Oncorhynchus mykiss) estrogen receptor-alpha messenger RNA and its expression in the ovary during the reproductive cycle. J. Mol. Endocrinol. 2000, 25:243-251.
42. Nelson E.R., Habibi H.R. Functional significance of nuclear estrogen receptor subtypes in the liver of goldfish. Endocrinology 2010, 151:1668-1676.
43. Nelson E.R., Habibi H.R. Estrogen receptor function and regulation in fish and other vertebrates. Gen. Comp. Endocrinol. 2013, 192:15-24.
44. Nilsson S., Mäkelä S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J.-Å. Mechanisms of estrogen action. Physiol. Rev. 2001, 81:1535-1565.
45. O'donnell L., Robertson K.M., Jones M.E., Simpson E.R. Estrogen and spermatogenesis 1. Endocr. Rev. 2001, 22:289-318.
46. Palstra A.P., Schnabel D., Nieveen M.C., Spaink H.P., van den Thillart G.E. Temporal expression of hepatic estrogen receptor 1, vitellogenin1 and vitellogenin2 in European silver eels. Gen. Comp. Endocrinol. 2010, 166:1-11.
47. Pang Y., Thomas P. Involvement of estradiol-17β and its membrane receptor, G protein coupled receptor 30 (GPR30) in regulation of oocyte maturation in zebrafish, Danio rerio. Gen. Comp. Endocrinol. 2009, 161:58-61.
48. Pellegrini E., Menuet A., Lethimonier C., Adrio F., Gueguen M.-M., Tascon C., Anglade I., Pakdel F., Kah O. Relationships between aromatase and estrogen receptors in the brain of teleost fish. Gen. Comp. Endocrinol. 2005, 142:60-66.
49. Peyon P., Baloche S., Burzawa-Gerard E. Investigation into the possible role of androgens in the induction of hepatic vitellogenesis in the European eel: in vivo and in vitro studies. Fish Physiol. Biochem. 1997, 16:107-118.
50. Pu L., Han K., Xie F., Zou Z., Close D., Zhang Z., Wang Y. Molecular cloning, characterization, and gene expression of the androgen receptor in the large yellow croaker, Larimichthys crocea. Fish Physiol. Biochem. 2013, 39:309-324.
51. Richards J.S. Hormonal control of gene expression in the ovary. Endocr. Rev. 1994, 15:725-751.
52. Schwabe J.W., Chapman L., Finch J.T., Rhodes D. The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: how receptors discriminate between their response elements. Cell 1993, 75:567-578.
53. Shi Y., Liu X., Zhu P., Li J., Sham K.W., Cheng S.H., Li S., Zhang Y., Cheng C.H., Lin H. G-protein-coupled estrogen receptor 1 is involved in brain development during zebrafish (Danio rerio) embryogenesis. Biochem. Biophys. Res. Commun. 2013, 435:21-27.
54. Thomas P. Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen. Comp. Endocrinol. 2012, 175:367-383.
55. Thomas P., Alyea R., Pang Y., Peyton C., Dong J., Berg A. Conserved estrogen binding and signaling functions of the G protein-coupled estrogen receptor 1 (GPER) in mammals and fish. Steroids 2010, 75:595-602.
56. Weigel N. Steroid hormone receptors and their regulation by phosphorylation. Biochem. J. 1996, 319:657-667.
57. Wood A.W., van der Kraak G. Inhibition of apoptosis in vitellogenic ovarian follicles of rainbow trout (Oncorhynchus mykiss) by salmon gonadotropin, epidermal growth factor, and 17beta-estradiol. Mol. Reprod. Dev. 2002, 61:511-518.
58. Wu C., Patiño R., Davis K.B., Chang X. Localization of estrogen receptor α and β RNA in germinal and nongerminal epithelia of the channel catfish testis. Gen. Comp. Endocrinol. 2001, 124:12-20.
59. You X., Cai M., Jiang Y., Wang Z. Histological observation on gonadal sex differentiation in large yellow croaker (Larimichthys crocea). J. Fish. China 2012, 1057-1064.
60. Zhu P., Zhang Y., Zhuo Q., Lu D., Huang J., Liu X., Lin H. Discovery of four estrogen receptors and their expression profiles during testis recrudescence in male Spinibarbus denticulatus. Gen. Comp. Endocrinol. 2008, 156:265-276.