Expression patterns of gonadotropin hormones and their receptors during early sexual differentiation in nile tilapia Oreochromis niloticus

Biology of Reproduction

Volumn 87, Issue 5, 2012, Pages

  Yan, Hongwei ^a   Ijiri, Shigeho ^a   Wu, Quan ^a   Kobayashi, Tohru ^b   Li, Shuang ^a   Nakaseko, Taro ^a   Adachi, Shinji ^a   Nagahama, Yoshitaka ^c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF SHIZUOKA   (Japan)

^c EHIME UNIVERSITY   (Japan)

Author keywords

GTHRs; GTHs; Nile tilapia; Sex differentiation

Indexed keywords

FOLLITROPIN; FOLLITROPIN RECEPTOR; LUTEINIZING HORMONE; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; OREOCHROMIS NILOTICUS; OVARY; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENTIATION; TESTIS;

ANIMALS; BRAIN; CICHLIDS; FEMALE; FOLLICLE STIMULATING HORMONE; GONADOTROPINS; GONADS; LUTEINIZING HORMONE; MALE; MORPHOGENESIS; PITUITARY GLAND; RECEPTORS, FSH; RECEPTORS, GONADOTROPIN; RECEPTORS, LH; RNA, MESSENGER; SEX DIFFERENTIATION;

OREOCHROMIS NILOTICUS; TILAPIA;

EID: 84869468608     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.101220     Document Type: Article

References (57)

1. Norris DO. Vertebrate Endocrinology, 4th ed. San Diego, CA: Academic Press; 2007.
2. Que'rat B. Molecular evolution of the glycoprotein hormones in vertebrates In: KG, Davey, RE, Peter, Tobe SS (eds.), Perspectives in Comparative Endocrinology. Ottawa: National Research Council of Canada; 1994; 27-35.
3. Swanson P, Dickey JT, Campbell B. Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 2003; 28:53-59.
4. Fan HG, Wang DS, Kobayashi T, Senthilkumaran B, Sudhakumari CC, Yoshikuni M, Nagahama Y. Molecular cloning of the three gonadotropin subunits and early expression of FSH-b during sex differentiation in the Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 2003; 28:143-144.
5. Wu FR, Zhang XY, Zhang WL, Huang BF, Liu ZH, Hu CJ, Wang DS.Expression of three gonadotropin subunits in Southern catfish gonad and their possible roles during early gonadal development. Comp Biochem Physiol A Mol Integr Physiol 2009; 153:44-48.
6. Urbatzka R, Lorenz C, Lutz I, Kloas W. Expression profiles of LHb, FSHb and their gonadal receptor mRNAs during sexual differentiation of Xenopus laevis tadpoles. Gen Comp Endocrinol 2010; 168:239-244.
7. Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology.Endocr Rev 1997; 18:739-773.
8. Kumar RS, Trant JM. Piscine glycoprotein hormone gonadotropin and thyrotropin receptors: a review of recent developments. Comp Biochem Physiol B 2001; 129:347-355.
9. Segaloff DL, Ascoli M. The lutropin/choriogonadotropin receptor.. .4 years later. Endocr Rev 1993; 14:324-347.
10. Biason-Lauber A. Molecular medicine of steroid hormone biosynthesis.Mol Aspects Med 1998; 19:155-220.
11. Oba Y, Hirai T, Yoshiura Y, Yoshikuni M, Kawauchi H, Nagahama Y.Cloning, functional characterization, and expression of a gonadotropin receptor cDNA in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem Biophys Res Commun 1999; 263:584-590.
12. Oba Y, Hirai T, Yoshiura Y, Yoshikuni M, Kawauchi H, Nagahama Y.The duality of fish gonadotropin receptors: cloning and functional characterization of a second gonadotropin receptor cDNA expressed in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem Biophys Res Commun 1999; 265:366-371.
13. Kumar RS, Ijiri S, Trant JM. Molecular biology of channel catfish gonadotropin receptors. 1. Cloning of a functional luteinizing hormone receptor and preovulatory induction of gene expression. Biol Reprod 2001; 64:1010-1018.
14. Kumar RS, Ijiri S, Trant JM. Molecular biology of the channel catfish gonadotropin receptors. 2. Complementary DNA cloning, functional expression, and seasonal gene expression of the follicle-stimulating hormone receptor. Biol Reprod 2001; 65:710-717.
15. Hirai T, Oba Y, Yao ZX, Chang XT, Yoshiura Y, Kobayashi T, Nagahama Y. Putative gonadotropin receptors in tilapia (Oreochromis niloticus) gonads: cDNA cloning and expression during oogenesis. In:Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds.), Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. Bergen, Norway: John Grieg A/S; 2000:201.
16. Oba Y, Hirai T, Yoshiura Y, Nagahama Y. Fish pituitary glycoprotein receptors: cloning and characterization of two different gonadotropin receptors from gonads and two thyrotropin-like receptors from thyroid of amago salmon (Oncorhynchus rhodurus). In: Norberg B, Kjesbu OS, Taranger GL, Andersson E and Stefansson SO (eds.), Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish.Bergen, Norway: John Grieg A/S; 2000:164-166.
17. Suda M, Kodama M, Oshima Y, Yamamoto K, Nakamura Y, Tanaka S, Kikuyama S, Nakamura M. Up-regulation of FSHR expression during gonadal sex determination in the frog Rana rugosa. Gen Comp Endocrinol 2011; 172:475-486.
18. Kobayashi T, Kajiura-Kobayashi H, Nagahama H. Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 2000; 99:139-142.
19. Nakamura M, Kobayashi T, Chang XT, Nagahama Y. Gonadal sex differentiation in teleost fish. J Exp Zool 1998; 281:362-372.
20. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 2008; 78:333-341.
21. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi KI, Nagahama Y. 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 2007; 21:712-725.
22. Steinkampf MP, Mendelson CR, Simpson ER. Regulation by folliclestimulating hormone of the synthesis of aromatase cytochrome P-450 in human granulosa cells. Mol Endocrinol 1987; 1:465-471.
23. Fitzpatrick SL, Richards JS. Regulation of cytochrome P450 aromatase messenger ribonucleic acid and activity by steroids and gonadotropins in rat granulosa cells. Endocrinology 1991; 129:1452-1462.
24. Parhar IS, Soga T, Ogawa S, Sakuma YFSH. and LH-b subunits in the preoptic nucleus: ontogenic expression in teleost. Gen Comp Endocrinol 2003; 132:369-378.
25. Suzuki K, Kawauchi H, Nagahama Y. Isolation and characterization of two distinct gonadotropins from chum salmon pituitary glands. Gen Comp Endocrinol 1988; 71:292-301.
26. Ikeuchi T, Mochida K, Ura K, Adachi S, Yamauchi K. Specific antibodies against synthetic peptides of salmonid GTH I and II b subunits. Zool Sci 1995; 12:317-323.
27. Saga T, Yamaki K, Doi Y, Yoshizuka M. Chronological study of the appearance of adenohypophysial cells in the ayu (Plecoglossus altivelis).Anat Embryol (Berl) 1999; 200:469-475.
28. García-Ayala A, Villaplana M, García-Hernández MP, Chaves-Pozo E, Agulleiro BFSH-, LH-, and TSH-expressing cells during development of Sparus aurata L. (Teleostei): an immunocytochemical study.Gen Comp Endocrinol 2003; 134:72-79.
29. Pandolfi M, Lo Nostro FL, Shimizu A, Pozzi AG, Meijide FG, Vazquez GR, Maggese MC. Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation. Anat Embryol (Berl) 2006; 211:355-365.
30. Shimizu A, Hamaguchi M, Ito H. OhkuboM, Udagawa M, Fujii K, Kobayashi T, Nakamura M. Appearances and chronological changes of mummichog Fundulus heteroclitus FSH cells and LH cells during ontogeny, sexual differentiation, and gonadal development. Gen Comp Endocrinol 2008; 156:312-322.
31. Miranda LA, Strüssmann CA, Somoza GM. Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen Comp Endocrinol 2001; 124:45-52.
32. Guzmán JM, Bayarri MI, Ramos J, Zohar Y, Sarasquete C, Mañanós EL.Follicle stimulating hormone (FSH) and luteinizing hormone (LH) gene expression during larval development in Senegalese sole (Solea senegalensis).Comp Biochem Physiol A Mol Integr Physiol 2009; 154:37-43.
33. Wong TT, Gothilf Y, Zmora N, Kight KE, Meiri I, Elizur A, Zohar Y.Developmental expression of three forms of gonadotropin-releasing hormone and ontogeny of the hypothalamic-pituitary-gonadal axis in gilthead seabream (Sparus aurata). Biol Reprod 2004; 71:1026-1035.
34. Suzuki K, Nagahama Y, Kawauchi H. Steroidogenic activities of 2 distinct salmon gonadotropins. Gen Comp Endocrinol 1988; 71:452-458.
35. Shimizu A, Yamashita M. Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides. Gen Comp Endocrinol 2002; 125:79-91.
36. Kendall SK, Saunders TL, Jin L, Lloyd RV, Glode LM, Nett TM, Keri RA, Nilson JH, Camper SA. Targeted ablation of pituitary gonadotropes in transgenic mice. Mol Endocrinol 1991; 5:2025-2036.
37. Ohta T, Miyake H, Miura C, Kamei H, Aida K, Miura T. Folliclestimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica. Biol Reprod 2007; 77:970-977.
38. Wong TT, Zohar Y. Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 2004;145:5210-5220.
39. So WK, Kwok H, Ge W. Zebrafish gonadotropins and their receptors. II.Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits-their spatial-temporal expression patterns and receptor specificity. Biol Reprod 2005; 72:1382-1396.
40. Sakai F, Swapna I, Sudhakumari CC, Ganesh MVNL, Kagawa H, Kobayashi T, Fan H, Nagahama Y, Senthilkumaran B. Immunocytochemical localization of gonadotropins during the development of XX and XY Nile tilapia. Fish Physiol Biochem 2005; 31:177-181.
41. Aizen J, Kasuto H, Golan M, Zakay H, Levavi-Sivan B. Tilapia folliclestimulating hormone (FSH): immunochemistry, stimulation by gonadotropin-releasing hormone, and effect of biologically active recombinant FSH on steroid secretion. Biol Reprod 2007; 76:692-700.
42. Melamed P, Rosenfeld H, Elizur A, Yaron Z. Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comp Biochem Physiol C 1998; 119:325-338.
43. Kasper RS, Shved N, Takahashi A, Reinecke M, Eppler EA. Systematic immunohistochemical survey of the distribution patterns of GH, prolactin,somatolactin, bTSH, b-FSH, b-LH, ACTH, and a-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 2006; 325:303-313.
44. Akazome Y, Abe T, Mori T. Differentiation of chicken gonad as an endocrine organ: expression of LH receptor, FSH receptor, cytochrome P450c17 and aromatase genes. Reproduction 2002; 123:721-728.
45. Baron D, Houlgatte R, Fostier A, Guiguen Y. Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 2005; 73:959-966.
46. Braun T, Schofield PR, Sprengel R. Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO J 1991;10:1885-1890.
47. Tilly JL, Aihara T, Nishimori K, Jia XC, Billig H, Kowalski KI, Perlas EA, Hsueh AJ. Expression of recombinant human follicle-stimulating hormone receptor: species-specific ligand binding, signal transduction, and identification of multiple ovarian messenger ribonucleic acid transcripts.Endocrinology 1992; 131:799-806.
48. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T. 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 2007; 359:935-940.
49. Fitzpatrick SL, Richards JS. Identification of a cyclic adenosine 30, 50-monophosphate-response element in the rat aromatase promoter that is required for transcriptional activation in rat granulosa cells and R2C Leydig cells. Mol Endocrinol 1994; 8:1309-1319.
50. Chang XT, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y. Two types of aromatase with diVerent encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 2005; 141:101-115.
51. Wong TT, Ijiri S, Zohar Y. 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 2006; 74:857-864.
52. Kagawa H, Gen K, Okuzawa K, Tanaka H. Effects of luteinizing hormone and follicle-stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicles of red seabream, Pagrus major. Biol Reprod 2003; 68:1562-1568.
53. Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D.a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000; 14:2587-2595.
54. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T. Sex-specific expression of an evolutionarily conserved male regulatory gene, Dmrt1, in birds. Cytogenet Cell Genet 2000; 89:252-257.
55. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 2004; 231:518-526.
56. Kobayashi T, Kajiura-Kobayashi H, Guan G, Nagahama Y. Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish Nile tilapia (Oreochromis niloticus). Dev Dyn 2008; 237:297-306.
57. Chen JK, Hechert LL. Dmrt1 expression is regulated by folliclestimulating hormone and phorbol esters in postnatal Sertoli cells.Endocrinology 2001; 142(3):1167-1168.