Expression of gonadotropin and gonadotropin receptor genes during early sexual maturation in male Atlantic salmon parr

Molecular Reproduction and Development

Volumn 75, Issue 2, 2008, Pages 403-413

  Maugars, Gersende ^a   Schmitz, Monika ^a,b  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b KARLSTAD UNIVERSITY   (Sweden)

Author keywords

11 ketotestosterone; FSH; FSHR; LH; LHR; Puberty; Spermatogenesis

Indexed keywords

11 OXOTESTOSTERONE; FOLLITROPIN; FOLLITROPIN BETA SUBUNIT; GONADOTROPIN; GONADOTROPIN RECEPTOR; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FRESHWATER ENVIRONMENT; GENE EXPRESSION REGULATION; GONADOTROPIN RELEASE; HYPOPHYSIS GONAD SYSTEM; MALE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; SALMON; SEMEN ANALYSIS; SEXUAL MATURATION; SPERMATOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; GENE EXPRESSION REGULATION; GONADOTROPINS; MALE; RECEPTORS, FSH; RECEPTORS, GONADOTROPIN; RECEPTORS, LH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMO SALAR; SEXUAL MATURATION; TESTIS;

SALMO SALAR; TELEOSTEI; VERTEBRATA;

EID: 37849030397     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20767     Document Type: Article

References (59)

1. Antonopoulou E, Jakobsson S, Mayer I, Swanson P, Borg B. 1997. In vivo and in vitro effects of 17 alpha, 20 beta-dihydroxy-4-pregnene-S-one on testicular androgens in Atlantic salmon, Salmo salar, mature parr. J Exp Zool 277:66-71.
2. Ascoli M, Fanelli F, Segaloff DL. 2002. The Lutropin/Choriogonadotropin receptor, a 2002 perspective. Endocr Rev 23:141-174.
3. 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 73:959-966.
4. Berglund I. 1992. Growth and early sexual maturation in Baltic salmon (Salmo salar) parr. Can J Zool 70:205-211.
5. Bogerd J, Blomenrohr M, Andersson E, van der Putten HHAGM, Tensen CP, Vischer HF, Granneman JCM, Janssen-Dommerholt C, Goos HJT, Schulz RW. 2001. Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Biol Reprod 64:1633-1643.
6. Bogerd J, Granneman JCM, Schulz RW, Vischer HF. 2005. Fish FSH receptors bind LH: How to make the human FSH receptor to be more fishy? Gen Comp Endocrinol 142:34-43.
7. Borg B. 1994. Androgens in teleost fishes. Comp Biochem Physiol C 109:219-245.
8. Borg B, Antonopoulou E, Mayer I, Andersson E, Berglund I, Swanson P. 1998. Effects of gonadectomy and androgen treatments on pituitary and plasma levels of gonadotropins in mature male Atlantic salmon, Salmo salar, parr-positive feedback control of both gonadotropins. Biol Reprod 58:814-820.
9. Campbell B, Dickey JT, Swanson P. 2003. Endocrine changes during onset of puberty in male spring Chinook salmon, Oncorhynchus tshawytscha. Biol Reprod 69:2109-2117.
10. Cavaco JEB, Vilrokx C, Trudeau VL, Schulz RW, Goos HJT. 1998. Sex steroids and the initiation of puberty in male African catfish (Clarias gariepinus). Am J Physiol 44:R1793-R1802.
11. Chaves-Pozo E, Mulero V, Meseguer J, Ayala AG. 2005. An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L.). Biol Reprod 72:593-601.
12. Dahia CL, Rao AJ. 2006. Regulation of FSH receptor, PKI β, IL-6 and calcium mobilization: Possible mediators of differential action of FSH. Mol Cell Endocrinol 247:73-81.
13. Gomez JM, Weil C, Ollitrault M, Le Bail P-Y, Breton B, Le Gac F. 1999. Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 113:413-428.
14. Ko H, Park W, Kim D-J, Kobayashi M, Sohn YC. 2007. Biological activities of recombinant Manchurian trout FSH and LH: Their receptor specificity, steroidogenic and vitellogenic potencies. J Mol Endocrinol 38:99-111.
15. Kumar RS, Ijiri S, Trant JM. 2001a. Molecular biology of channel catfish gonadotropin receptors: 1. Cloning of a functional luteinizing hormone receptor and preovulatory induction of gene expression. Biol Reprod 64:1010-1018.
16. Kumar RS, Ijiri S, Trant JM. 2001b. 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 65:710-717.
17. Kusakabe M, Nakamura I, Evans J, Swanson P, Young G. 2006. Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes. J Endocrinol 189:541-554.
18. Kwok HF, So WK, Wang YJ, Ge W. 2005. Zebrafish gonadotropins and their receptors: 1. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone receptors-evidence for their distinct functions in follicle development. Biol Reprod 72:1370-1381.
19. Larsson S, Berglund I. 2006. Thermal performance of juvenile Atlantic salmon (Salmo salar L.) of Baltic Sea origin. J Therm Biol 31:243-246.
20. Lejeune H, Chuzel F, Thomas T, Avallet O, Habert R, Durand P, Saez J. 1996. Paracrine regulation of Leydig cells. Ann Endocrinol 57:55-63.
21. Lejeune H, Sanchez P, Chuzel F, Langlois D, Saez JM. 1998. Time-course effects of human recombinant luteinizing hormone on porcine Leydig cell specific differentiated functions. Mol Cell Endocrinol 144:59-69.
22. Loir M. 1990. Interstitial cells from the testis of the trout (Oncorhynchus mykiss) In vivo and in primary culture. Cell Tissue Res 261:133-144.
23. Loir M. 1999. Spermatogonia of rainbow trout: II. In vitro study of the influence of pituitary hormones, growth factors and steroids on mitotic activity. Mol Reprod Dev 53:434-442.
24. Maguire S, Tribley W, Griswold M. 1997. Follicle-stimulating hormone (FSH) regulates the expression of FSH receptor messenger ribonucleic acid in cultured Sertoli cells and in hypophysectomized rat testis. Biol Reprod 56:1106-1111.
25. Maugars G, Schmitz M. 2006. Molecular cloning and characterization of FSH and LH receptors in Atlantic salmon (Salmo salar L.). Gen Comp Endocrinol 149:108-117.
26. Mayer I, Berglund I, Rydevik M, Borg B, Schulz R. 1990a. Plasma levels of five androgens and 17-hydroxy-20-dihydroprogesterone in immature and mature male Baltic salmon (Salmo salar) parr and the effects of castration and androgen replacement in mature parr. Can J Zool 68:263-267.
27. Mayer I, Lundqvist H, Berglund I, Schmitz M, Schulz R, Borg B. 1990b. Seasonal endocrine changes in Baltic salmon, Salmo salar, immature parr and mature male parr. I. Plasma levels of five androgens, 17-hydroxy-20β- dihydroprogesterone, and 17β-estradiol. Can J Zool 68:1360-1365.
28. Menon KMJ, Nair AK, Wang L. 2006. A novel post-transcriptional mechanism of regulation of luteinizing hormone receptor expression by an RNA binding protein from the ovary. Mol Cell Endocrinol 246:135-141.
29. Miura T, Yamauchi K, Takahashi H, Nagahama Y. 1991. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). J Natl Acad Sci USA 88:5774-5778.
30. Miwa S, Yan L, Swanson P. 1994. Localization of two gonadotropin receptors in the salmon gonad by in vitro ligand autoradiography. Biol Reprod 50:629-642.
31. Nijenhuis WAJ, Male R, Swanson P, Andersson E, Bogerd J, Schulz RW. 2004. The gonadotropin receptors of Atlantic salmon (Salmo salar) 2004 5-9 September; Castellón, Spain
32. Oba Y, Hirai T, Yoshiura Y, Yoshikuni M, Kawauchi H, Nagahama Y. 1999a. Cloning, functional characterization, and expression of a gonadotropin receptor cDNA in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem Biophys Res Commun 263:584-590.
33. Oba Y, Hirai T, Yoshiura Y, Yoshikuni M, Kawauchi H, Nagahama Y. 1999b. 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 265:366-371.
34. Oba Y, Hirai T, Yoshiura Y, Kobayashi T, Nagahama Y. 2001. Fish gonadotropin and thyrotropin receptors: The evolution of glycoprotein hormone receptors in vertebrates. Comp Biochem Physiol B 129:441-448.
35. Patino R, Sullivan CV. 2002. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57-70.
36. Pierce J, Parsons TF. 1981. Glycoprotein hormones: Structure and function. Ann Rev Biochem 50:465-495.
37. Planas JV, Swanson P. 1995. Maturation associated changes in the response of the salmon testis to the steroidogenic actions of gonadotropins (GTH I and GTH II) in vitro. Biol Reprod 52:697-704.
38. Prat F, Sumpter J, Tyler C. 1996. Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss). Biol Reprod 54:1375-1382.
39. Querat 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 63:222-228.
40. Rahman MA, Ohta K, Yamaguchi A, Chuda H, Hirai T, Matsuyama M. 2003. Gonadotropins, gonadotropin receptors and their expressions during sexual maturation in yellowtail, a carangid fish. Fish Physiol Biochem 28:81-83.
41. Rowe DK, Thorpe JE. 1990. Suppression of maturation in male Atlantic salmon (Salmo salar L.) parr by reduction in feeding and growth during spring months. Aquaculture 86:291-313.
42. Rozen S, Skaletsky HJ. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, New Jersey: Humana Press. pp 365-386.
43. Schulz R. 1984. Serum levels of 11-oxotestosterone in male and 17β-estradiol in female rainbow trout (Salmo gairdneri) during the first reproductive cycle. Gen Comp Endocrinol 56:111-120.
44. Schulz RW, Miura T. 2002. Spermatogenesis and its endocrine regulation. Fish Physiol Biochem 26:43-56.
45. Schulz RW, van Dijk W, Bogerd J. 2003. Sertoli cell proliferation and FSH signalling in African catfish, Clarias gariepinus. Fish Physiol Biochem 28:223-224.
46. Schulz RW, Menting S, Bogerd J, Franca LR, Vilela DAR, Godinho HP. 2005. Sertoli cell proliferation in the adult testis - Evidence from two fish species belonging to different orders. Biol Reprod 73:891-898.
47. Scott AP, Sumpter JP. 1989. Seasonal variations in testicular germ cell stages and in plasma concentrations of sex steroids in male rainbow trout (Salmo gairdneri) maturing at 2 years old. Gen Comp Endocrinol 73:46-58.
48. Shan L, Hardy D, Catterall J, Hardy M. 1995. Effects of luteinizing hormone (LH) and androgen on steady state levels of messenger ribonucleic acid for LH receptors, androgen receptors, and steroidogenic enzymes in rat Leydig cell progenitors in vivo. Endocrinology 136:1686-1693.
49. So WK, Kwok HF, Ge W. 2005. 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 72:1382-1396.
50. Swanson P, Bernard M, Nozaki M, Suzuki H, Kawauchi H, Dickhoff WW. 1989. Gonadotropins I and II in juvenile coho salmon. Fish Physiol Biochem 7:169-176.
51. Swanson P, Dickey J, Campbell T. 2003. Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53-59.
52. Thorpe JE, Talbot C, Miles MS, Keay DS. 1990. Control of maturation in cultured Atlantic salmon, Salmo salar, in pumped seawater tanks, by restricting food intake. Aquaculture 86:315-326.
53. Vischer HF, Bogerd J. 2003. Cloning and functional characterization of a gonadal luteinizing hormone receptor complementary DNA from the African catfish (Clarias gariepinus). Biol Reprod 68:262-271.
54. Vischer H, Granneman J, Linskens M, Schulz R, Bogerd J. 2003. Both recombinant African catfish LH and FSH are able to activate the African catfish FSH receptor. J Mol Endocrinol 31:133-140.
55. Walker WH, Cheng J. 2005. FSH and testosterone signaling in Sertoli cells. Reproduction 130:15-28.
56. Weil C, Bougoussa-Houadec M, Gallais C, Itoh S, Sekine S, Valotaire Y. 1995. Preliminary evidence suggesting variations of GtH 1 and GtH 2 mRNA levels at different stages of gonadal development in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 100:327-333.
57. Wong T-T, Gothilf Y, Zmora N, Kight KE, Meiri I, Elizur A, Zohar Y. 2004. Developmental expression of three forms of gonadotropin-releasing hormone and ontogeny of the hypothalamic-pituitary-gonadal axis in gilthead seabream (Sparus aurata). Biol Reprod 71:1026-1035.
58. Yan L, Swanson P, Dickhoff W. 1992. A two-receptor model for salmon gonadotropins (GTH I and GTH II). Biol Reprod 47:418-427.
59. Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B. 2003. Regulation of fish gonadotropins. Int Rev Cytol 225:131-185.