Cloning of FSH-β, LH-β and glycoprotein hormone α subunits in pejerrey Odontesthes bonariensis (Valenciennes): Expression profile and relationship with GnRH expression and plasma sex steroid levels in male fish

Journal of Fish Biology

Volumn 71, Issue 6, 2007, Pages 1571-1589

  Miranda, L A ^a   Strussmann C A ^b   Guilgur, L G ^a   Strobl Mazzulla, P H ^a   Somoza, G M ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Gonadotropin releasing hormones; Gonadotropins; Pejerrey; Sex steroids

Indexed keywords

ANIMALIA; ODONTESTHES BONARIENSIS; ONCORHYNCHUS;

EID: 36849052990     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2007.01621.x     Document Type: Article

References (69)

1. Aguirre, U. A., Timossi, C., Matsumura, D. P. Dias, J. A. (1999). Role of glycosylation in function of follicle-stimulating hormone. Endocrine 11, 205 215.
2. Ando, H., Swanson, P., Kitani, T., Koide, N., Okada, H., Ueda, H. Urano, A 2004). Synergistic effects of salmon gonadotropin-releasing hormone and estradiol-17β on gonadotropin subunit gene expression and release in masu salmon pituitary cells in vitro. General and Comparative Endocrinology 137, 109 121.
3. Antonopoulou, E., Swanson, P., Mayer, I. Borg, B 1999). Feedback control of gonadotropins in Atlantic salmon, Salmo salar, male parr II. Aromatase inhibitor and androgen effects. General and Comparative Endocrinology 114, 142 150.
4. Applied Biosystems (1997). ABI Prism Sequence Detection System. Relative Quantitation of Gene Expression, 1997, User Bulletin number 2. Foster city, CA : Applied Biosystems.
5. Barnett, D. K., Bunnell, T. M., Millar, R. P. Abbott, D. H. (2006). Gonadotropin-releasing hormone II stimulates female sexual behavior in marmoset monkeys. Endocrinology 147, 615 623.
6. 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. Biology of Reproduction 58, 814 820.
7. Breton, B., Govoroun, M. Mikolajczyk, T 1998). GTH I and GTH II secretion profiles during the reproductive cycle in female rainbow trout: relationship with pituitary responsiveness to GnRH-A stimulation. General and Comparative Endocrinology 111, 38 50.
8. Degani, G., Mañanos, E. L. Zohar, Y 1997). Changes in plasma and pituitary in female blue gourami during the end of vitellogenesis and final oocyte maturation. Journal of Experimental Zoology 279, 377 385.
9. Degani, G., Goldberg, D., Tzchori, I., Hurvitz, A., Yom Din, S. Jackson, K 2003a). Cloning of European eel (Anguilla anguilla) FSH-β subunit, and expression of FSH-β and LH-β in males and females after sex determination. Comparative Biochemistry and Physiology 13B, 283 293.
10. Degani, G., Jackson, K., Goldberg, D., Sarfati, R. Avtalion, R 2003b). Gene expression in blue gourami (Trichogaster trichopterus, Pallas, 1770) during spermatogenesis and male sexual behavior. Zoological Science 20, 737 743.
11. Dickey, J. T. Swanson, P 1998). Effects of sex steroids on gonadotropin (FSH and LH) regulation in coho salmon (Oncorhynchus kisutch). Journal of Molecular Endocrinology 21, 291 306.
12. Dickey, J. T. Swanson, P 2000). Effects of salmon gonadotropin-releasing hormone on follicle stimulating hormone secretion and subunit gene expression in coho salmon (Oncorhynchus kisutch). General and Comparative Endocrinology 118, 436 449.
13. Fink, G 1988). Gonadotropin secretion and its control. In The Physiology of Reproduction (Knobil, E. Neill, J. D., eds pp. 1349 1377. New York : Raven Press.
14. Gen, K., Okuzawa, K., Senthilkumaran, B., Tanaka, H., Moriyama, S. Kagawa, H 2000). Unique expression of gonadotropin-I and -II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biology of Reproduction 63, 308 319.
15. Gómez, J. M., Weil, C., Ollitrault, M., Bail, P. Y., Breton, B. 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). General and Comparative Endocrinology 113, 413 428.
16. Govoroun, M., Chyb, J. Breton, B 1998). Immunological cross-reactivity between rainbow trout GTH I and GTH II and their α and β subunits: application to the development of specific radioimmunoassays. General and Comparative Endocrinology 111, 28 37.
17. Guilgur, L. G., Ortí, G., Strobl-Mazzulla, P. H., Fernandino, J. I., Miranda, L. A. Somoza, G. M. (2007). Characterization of the cDNAs encoding three GnRH forms in the pejerrey fish Odontesthes bonariensis (Atheriniformes) and the evolution of GnRH precursors. Journal of Molecular Evolution 64, 614 627.
18. Hassin, S., Gothilf, Y., Blaise, O. Zohar, Y 1998). Gonadotropin-I and gonadotropin-II subunit gene expression of male striped bass (Morone saxatilis) after gonadotropin-releasing hormone analogue injection: quantitation using an optimized ribonuclease protection assay. Biology of Reproduction 58, 1233 1240.
19. Hassin, S., Claire, M., Holland, H. Zohar, Y 2000). Early maturity in the male striped bass, Morone saxatilis: follicle-stimulating hormone and luteinizing hormone gene expression and their regulation by gonadotropin- releasing hormone analogue and testosterone. Biology of Reproduction 63, 1691 1697.
20. Huggard, D. L., Khakoo, Z., Kassam, G., Mahmoud, S. S. Habibi, H. R. (1996). Effect of testosterone on maturational gonadotropin subunit mRNA levels in the goldfish pituitary. Biology of Reproduction 54, 1184 1191.
21. Huggard-Nelson, D. L., Nathwani, P. S., Kermouni, A. Habibi, H. R. (2002). Molecular characterization of LH-β and FSH-β subunits and their regulation by estrogen in the goldfish pituitary. Molecular and Cellular Endocrinology 188, 171 193.
22. Jackson, K., Goldberg, D., Ofir, M., Abraham, M. Degani, G 1999). Blue gourami (Trichogaster trichopterus) gonadotropic beta-subunits (I and II) cDNA sequences and expression during oogenesis. Journal of Molecular Endocrinology 23, 177 187.
23. Kajimura, S., Yoshiura, Y., Suzuki, M. Aida, K 2001). cDNA cloning of two gonadotropin β subunits (GTH-Iβ and -IIβ) and their expression profiles during gametogenesis in the japanese flounder (Paralichthys olivaceus). General and Comparative Endocrinology 122, 117 129.
24. Kandel-Kfir, M., Gur, G., Melamed, P., Zilberstein, Y., Cohen, Y., Zmora, N., Kobayashi, M., Elizur, A. Yaron, Z 2002). Gonadotropin response to GnRH during sexual ontogeny in the common carp, Cyprinus carpio. Comparative and Biochemistry Physiology 132C, 17 26.
25. Kauffman, A. Rissman, E. F. (2004). A critical role for the evolutionarily conserved gonadotropin-releasing hormone II: mediation of energy status and female sexual behavior. Endocrinology 145, 3639 3646.
26. Kawauchi, H., Suzuki, K., Itoh, H., Swanson, P., Naito, N., Nagahama, Y., Nakai, Y. Itoh, S 1989). The duality of teleost gonadotropins. Fish Physiology and Biochemistry 7, 29 38.
27. Kim, D. J., Cho, Y. Ch. Sohn, Y. Ch. (2005). Molecular characterization of rockfish (Sebastes schlegeli) gonodotropin subunits and their mRNA expression profiles during oogenesis. General and Comparative Endocrinology 141, 282 290.
28. Kim, M. H., Amano, M., Suetake, H., Kobayashi, M. Aida, K 1997). GnRH neurons and gonadal maturation in masu salmon and goldfish. In Gene to Behavior (Parhar, I. S. Sakuma, Y., eds pp. 313 324. Tokyo : Brain Shuppan.
29. Kobayashi, M., Amano, M., Hasegawa, Y., Okuzawa, K. Aida, K 1992). Effects of olfactory tract section on brain GnRH distribution, plasma gonadotropin levels, and gonadal stage in goldfish. Zoological Science 9, 765 773.
30. Kobayashi, M., Amano, M., Kim, M. H., Furukawa, K., Hasegawa, Y. Aida, K 1994). Gonaotropin-releasing hormones of terminal nerve origin are not essential to ovarian development and ovulation in goldfish. General and Comparative Endocrinology 95, 192 200.
31. Kobayashi, M., Sohn, Y. C., Yoshiura, Y. Aida, K 2000). Effects of sex steroids on the mRNA levels of gonadotropin subunits in juvenile and ovariectomized goldfish Carassius auratus. Fisheries Science 66, 223 231.
32. Lapthorn, A. J., Harris, D. C., Littlejohn, A., Lustbader, J. W., Canfield, R. E., Machin, K. J., Morgan, F. J. Isaacs, N. W. (1994). Crystal structure of human chorionic gonadotropin. Nature 369, 455 461.
33. Li, Ch. J., Li, Z., Wang, Y., Hong, Y. H. Gui, J. F. (2005). Molecular and expression characterization of three gonadotropin subunits common α, FSHβ and LHβ in groupers. Molecular and Cellular Endocrinology 233, 33 46.
34. Liu, Z., Kim, S. Karsi, A 2001). Channel catfish follicle-stimulating hormone and luteinizing hormone: complementary DNA cloning and expression during ovulation. Marine Biotechnology 3, 590 599.
35. López, H. L., Baigún, C. R., Iwaskiw, J. M., Delfino, R. L. Padín, O. H. (2001). La cuenca del Salado: Uso y posibilidades de sus recursos pesqueros. La Plata : Universidad de La Plata.
36. Mateos, J., Mañanós, E., Martínez-Rodríguez, G., Carrillo, M., Querat, B. Zanuy, S 2003). Molecular characterization of sea bass gonadotropin subunits (α, FSHβ, and LHβ) and their expression during the reproductive cycle. General and Comparative Endocrinology 133, 216 232.
37. Miranda, L. A., Guilgur, L. G. Somoza, G. M. (2003). Molecular cloning of cDNAs encoding FSH-β and LH-β subunits in the pejerrey fish, Odontesthes bonariensis. Fish Physiology and Biochemistry 28, 101 102.
38. Montaner, A. D., Park, M., Fischer, W. H., Craig, A. G., Chang, J. P., Somoza, G. M., Rivier, J. E. Sherwood, N. M. (2001). Primary structure of a novel gonadotropin-releasing hormone (GnRH) variant in the brain of pejerrey (Odontesthes bonariensis). Endocrinology 142, 1453 1460.
39. Nelson, J. S. (1994). Fishes of the World. New York : John Wiley & Sons, Inc.
40. Okuzawa, K., Gen, K., Bruysters, M., Bogerd, J., Gothilf, Y., Zohar, Y. Kagawa, H 2003). Seasonal variation of the three native gonadotropin-releasing hormone messenger ribonucleic acids levels in the brain of female red sea brean. General and Comparative Endocrinology 131, 324 332.
41. Peter, R. E. Yu, K. L. (1997). Neuroendocrine regulation of ovulation in fishes: basic and applied aspects. Reviews in Fish Biology and Fisheries 7, 173 197.
42. Pierce, J. G. Parsons, T. F. (1981). Glycoprotein hormones: structure and function. Annual Review of Biochemistry 50, 465 495.
43. Prat, F., Zanuy, S., Carrillo, M., de Mones, A. Fostier, A 1990). Seasonal changes in plasma levels of gonadal steroids of sea bass, Dicentrarchus labrax L. General and Comparative Endocrinology 78, 361 373.
44. Prat, F., Sumpter, J. P. Tyler, C. R. (1996). Validation of radioimmunoassay 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). Biology of Reproduction 54, 1375 1382.
45. Quérat, B., Sellouk, A. Salmon, C 2000). Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) b-subunits of the two gonadotropins and the thyroid-stimulating hormone. Biology of Reproduction 63, 222 228.
46. Quérat, B., Tonnerre-Doncarli, C., Genies, F. Salmon, C 2001). Duality of gonadotropins in gnathostomes. General and Comparative Endocrinology 124, 308 314.
47. Rebers, F. E. M., Tensen, C. P., Schulz, R. W., Goos, H. J. Th. Bogerd, J 1997). Modulation of glycoprotein hormone α- and gonadotropin IIβ-subunit mRNA levels in the pituitary of mature male African catfish, Clarias gariepinus. Fish Physiology and Biochemistry 17, 99 108.
48. Senthilkumaran, B., Okuzawa, K., Gen, K., Ookura, T. Kagawa, H 1999). Distributional and seasonal variations in levels of three native GnRHs in the brain and pituitary of perciform fish. Journal of Neuroendocrinology 11, 181 186.
49. Schulz, R. W., Vischer, H. F., Cavacco, J. E., Santos, E. M., Tyler, C. R., Goos, H. J. Bogerd, J 2001). Gonadotropins, their receptors, and the regulation of testicular functions in fish. Comparative Biochemistry and Physiology 129, 407 417.
50. Sohn, Y. C., Yoshiura, Y., Kobayashi, M. Aida, K 1998). Effect of sex steroids on the mRNA levels of gonadotropin I and II subunits in the goldfish, Carassius auratus. Fisheries Science 64, 715 721.
51. Sohn, Y. C., Yoshiura, Y., Kobayashi, M. Aida, K 1999). Seasonal changes in the mRNA levels of gonadotropin and thyrotropin in the goldfish, Carassius auratus. General Comparative and Endocrinology 113, 436 444.
52. Sohn, Y. C., Kobayashi, M. Aida, K 2001). Regulation of gonadotropin β subunit gene expression by testosterone and gonadotropin-releasing hormones in the goldfish, Carassius auratus. Comparative Biochemistry and Physiology 129, 419 426.
53. Suzuki, K., Kawauchi, H. Nagahama, Y 1988). Development of salmon GTH I and GTH II radioimmunoassays. General and Comparative Endocrinoogy 71, 459 467.
54. Swanson, P 1991). Salmon gonadotropins: reconciling old and new ideas. In Reproductive Physiology of Fish (Scott, A. P., Sumpter, J. P., Kime, D. E. Rolfe, W. S., eds pp. 2 7. Sheffield : Fish Symposium 91.
55. Swanson, P., Suzuki, K., Kawauchi, H. Dickhoff, W. W. (1991). Isolation and characterisation of two coho salmon gonadotropins. GTH I and GTH II. Biology of Reproduction 44, 29 38.
56. Swanson, P., Dickey, J. T. Campbell, B 2003). Biochemistry and physiology of fish gonadotropins. Fish Physiology and Biochemistry 28, 1 7.
57. Vischer, H. F., Teves, A. C. C., Ackermans, J. C. M., van Dijk, W., Schulz, R. W. Bogerd, J 2003). Cloning and spatiotemporal expression of the follicle-stimulating hormone β subunit complementary DNA in the African catfish (Clarias gariepinus). Biology of Reproduction 68, 1324 1332.
58. Volkoff, H. Peter, R. E. (1999). Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. General and Comparative Endocrinology 116, 347 355.
59. Weil, C., Bongoussa-Houuaadec, M., Gallais, C., Itoh, S., Sekine, S. Valotaire, Y 1995). Preliminary evidence suggesting variations of GTH-I and GTH-II mRNA levels at different stages of gonadal development in rainbow trout Oncorhynchus mykiss. General and Comparative Endocrinology 100, 237 233.
60. Weil, C., Carre, F., Blaise, O., Breton, B. Le Bail, P. Y. (1999). Differential effect of insulin-like growth factor I on in vitro gonadotropin (I and II) and growth hormone secretions in rainbow trout (Oncorhynchus mykiss) at different stages of the reproductive cycle. Endocrinology 140, 2054 2062.
61. Weltzein, F. A., Kobayashi, T., Andersson, E., Norberg, B. Andersen, Ø 2003). Molecular characterization and expression of FSHβ, LHβ, and common α-subunit in males Atlantic halibut (Hippoglossus hippoglossus). General and Comparative Endocrinology 131, 87 96.
62. Xiong, F., Liu, D., Le Drean, Y., Elsholtz, H. C. Hew, C. L. (1994). Differential recruitment of steroid hormone response elements may dictate the expression of the pituitary gonadotropin II β subunit gene during salmon maturation. Molecular Endocrinology 8, 782 793.
63. Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Levavi-Sivan, B. Elizur, A 2001). Regulation of gonadotropin subunit genes in tilapia. Comparative and Biochemistry Physiology 129C, 489 502.
64. Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Elizur, A. Levavi-Sivan, B 2003). Regulation of fish gonadotropins. International Review of Cytology: A Survey of Cell Biology 225, 131 185.
65. Yoshiura, M., Kobayashi, M., Kato, Y. Aida, K 1997). Molecular cloning of cDNAs encoding two gonadotropin beta-subunits (GTH-Iβ and GTH-IIβ) from the goldfish, Carassius auratus. General and Comparative Endocrinology 105, 379 389.
66. Yu, K. L., Nahorniak, C. S., Peter, R. E., Corrigan, A., Rivier, J. E. Vale, W. W. (1987). Brain distribution of radioimmunoassayable gonadotropin-releasing hormone in female goldfish: seasonal variation and periovulatory changes. General and Comparative Endocrinology 67, 234 246.
67. Yu, K. L., Peng, C. Peter, R. E. (1991). Changes in brain levels of gonadotropin-releasing hormone and serum levels of gonadotropin and growth hormone in goldfish during spawning. Canadian Journal of Zoology 69, 182 188.
68. Degani, G., Jackson, K. Goldberg, D 2004). Transcription of FSH-β, LH-β and growth hormone in female Trichogaster trichopterus (Pallas 1770) treated with GnRH analog. In Symposiom Proceedings of the VI International Congress on the Biology of Fish. The Molecular Basis of Environmental Adaptation (Renshaw, E. Mackiley, D., eds pp. 45 57. Manaus : American Fisheries Society. Available at http://www-heb.pac.dfo-mpo.gc.ca/congress/2004/mole/molec.htm
69. Nicholas, K. B. Nicholas, H. B. (1997). GeneDoc: A Tool for Editing and Annotating Multiple Sequence Aligmments. Available at http://www.psc.edu/biomed/ genedoc