Molecular cloning and expression analysis of Fshr and Lhr in relation to Fshb and Lhb subunits during the period of temperature-dependent sex determination in pejerrey Odontesthes bonariensis

Molecular Reproduction and Development

Volumn 77, Issue 6, 2010, Pages 521-532

  Shinoda, Takahiro ^a   Miranda, Leandro A ^b   Okuma, Kozue ^a   Hattori, Ricardo S ^a   Fernandino, Juan I ^b   Yoshizaki, Goro ^a   Somoza, Gustavo M ^b   Strüssmann, Carlos A ^a  

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

^b INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FOLLITROPIN; FOLLITROPIN BETA SUBUNIT; LUTEINIZING HORMONE BETA SUBUNIT; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; FISH; GENE EXPRESSION; GONAD; HISTOLOGY; HYPOPHYSIS; LARVA; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; ODONTESTHES BONARIENSIS; ORGANOGENESIS; PRIORITY JOURNAL; SEX DETERMINATION; SEX DIFFERENTIATION; SEX RATIO; STEROIDOGENESIS; TEMPERATURE; TEMPERATURE DEPENDENCE; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; FEMALE; FISHES; MALE; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS; RECEPTORS, FSH; RECEPTORS, LH; SEX DIFFERENTIATION; SMEGMAMORPHA; TEMPERATURE; TISSUE DISTRIBUTION;

ANIMALIA; ODONTESTHES BONARIENSIS;

EID: 77954498594     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21179     Document Type: Article

References (60)

1. Andersson E, Nijenhuis W, Male R, Swanson P, Bogerd J, Taranger GL, Schulz RW. 2009. Pharmacological characterization, localization and quantification of expression of gonadotropin receptors in Atlantic salmon (Salmo salar L.) ovaries. Gen Comp Endocrinol 163:329-339.
2. Bogerd J, Blomenrohr M, Andersson E, van der Putten HHAG, 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. (Pubitemid 32493478)
3. Conover DO, Kynard BE. 1981. Environmental sex determination: Interaction of temperature and genotype in a fish. Science 213:577-579.
4. Devlin RH, Nagahama Y. 2002. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture 208:191-364.
5. Dufau ML. 1998. The luteinizing hormone receptor. Ann Rev Physiol 60:461-496.
6. Fernandino JI, Hattori RS, Kimura H, Strüssmann CA, Somoza GM. 2008. Expression profile and estrogenic regulation of Anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature-dependent sex determination. Dev Dyn 237:3192-3199.
7. Fitzpatrick MS, Pereira CB, Schreck CB. 1993. In vitro steroid secretion during early development of mono-sex rainbow trout: Sex differences, onset of pituitary control, and effects of dietary steroid treatment. Gen Comp Endocrinol 91:199-215.
8. Guilgur LG, Ortí G, Strobl-Mazzulla HP, Fernandino JI, Miranda LA, Somoza G. 2007. Characterization of the cDNAs encoding three GnRH forms in the pejerrey fish Odontesthes bonariensis (Atheriniformes) and the evolution of GnRH precursors. J Mol Evol 64:614-627.
9. Hannon GJ. 2002. RNA interference. Nature 418:244-251.
10. He L, Hannon GJ. 2004. MicroRNAs: Small RNAs with a big role in gene regulation. Nat Rev Genet 5:522-531.
11. Hattori RS, Fernandino JI, Kishii A, Kimura H, Kinno T, Oura M, Somoza GM, Yokota M, Strüssmann CA, Watanabe S. 2009. Cortisol-induced masculinization: Does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination? PLoS ONE 4:e6548.
12. Hirai T, Oba Y, Yao ZX, Chang XT, Yoshiura Y, Kobayashi T, Nagahama Y. 2000. 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, editors. Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. Bergen, Norway. p 201.
13. Huang WT, Hsieh JC, Chiou MJ, Chen JY, Wu JL, Kuo CM. 2008. Application of RNAi technology to the inhibition of zebrafish GtHα, FSHβ, and LHβ expression and to functional analyses. Zool Sci 25:614-621.
14. Ito LS, Yamashita M, Takashima F, Strüssmann CA. 2005. Dynamics and histological characteristics of gonadal sex differentiation in pejerrey (Odontesthes bonariensis) at feminizing and masculinizing temperatures. J Exp Zool 303A:504-514.
15. Jeng SR, Yueh WS, Chen GR, Lee YH, Dufour S, Chang CF. 2007. Differential expression and regulation of gonadotropins and their receptors in the Japanese eel, Anguilla japonica. Gen Comp Endocrinol 154:161-173.
16. Kagawa H, Gen K, Okuzawa K, Tanaka H. 2003. 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 68:1562-1568.
17. Karube M, Fernandino JI, Strobl-Mazzulla PH, Strüssmann CA, Yoshizaki G, Somoza GM, Patiño R. 2007. Characterization and expression profile of the ovarian cytochrome p-450 aromatase (cyp19a1) gene during the thermolabile sex determination period in pejerrey, Odontesthes bonariensis. J Exp Zool 307A:625-636.
18. Kobayashi T, Andersen O. 2008. The gonadotropin receptors FSH-R and LH-R of Atlantic halibut (Hippoglossus hippoglossus). 1: Isolation of multiple transcripts encoding full-length and truncated variants of FSH-R. Gen Comp Endocrinol 156:584-594.
19. Kobayashi T, Pakarinen P, Torgersen J, Huhtaniemi I, Andersen O. 2008. The gonadotropin receptors FSH-R and LH-R of Atlantic halibut (Hippoglossus hippoglossus). 2: Differential follicle expression and asynchronous oogenesis. Gen Comp Endocrinol 156:595-602.
20. Kobayashi Y, Nakamura M, Sunobe T, Usami T, Kobayashi T, Manabe H, Paul-Prasanth B, Suzuki N, Nagahama Y. 2009. Sex change in the gobiid fish is mediated through rapid switching of gonadotropin receptors from ovarian to testicular portion or vice versa. Endocrinology 150:1503-1511.
21. 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.
22. 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.
23. Kumar RS, Trant JM. 2001. Piscine glycoprotein hormone gonadotropin and thyrotropin receptors: A review of recent developments. Comp Biochem Physiol 129B:347-355.
24. Kumar RS, Trant JM. 2004. Hypophyseal gene expression profiles of FSH-β, LH-β, and glycoprotein hormone-a subunits in Ictalurus punctatus throughout a reproductive cycle. Gen Comp Endocrinol 136:82-89.
25. Kumar TJ. 2007. Mouse models for gonadotropins: A 15-year saga. Mol Cell Endocrinol 260-262:249-254.
26. Kumar TJ. 2009. FSHβ knockout mouse model: A decade ago and into the future. Endocrinology 36:1-5.
27. Kwok HF, So WK, Wang Y, Ge W. 2005. Zebrafish gonadotropins and their receptors: I. 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.
28. Laan M, Richmond H, He C, Campbell RK. 2002. Zebrafish as a model for vertebrate reproduction: Characterization of the first functional zebrafish (Danio rerio) gonadotropin receptor. Gen Comp Endocrinol 125:349-364.
29. LaPolt PS, Jia XC, Sincich C, Hsueh AJ. 1991. Ligand-induced downregulation of testicular and ovarian luteinizing hormone (LH) receptors is preceded by tissue-specific inhibition of alternatively processed LH receptor transcripts. Mol Endocrinol 5:397-403. (Pubitemid 21923704)
30. 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.
31. Menon KMJ, Munshi U, Clouser CL, Nair AK. 2004. Regulation of luteinizing hormone/human chorionic gonadotropin receptor expression: A perspective. Biol Reprod 70:861-866.
32. Mittelholzer C, Andersson E, Taranger GL, Consten D, Hirai T, Senthilkumaran B, Nagahama Y, Norberg B. 2009. Molecular characterization and quantification of the gonadotropin receptors FSH-R and LH-R from Atlantic cod (Gadus morhua). Gen Comp Endocrinol 160:47-58.
33. Miranda LA, Strüssmann CA, Somoza GM. 2001. Immunocytochemical identification of GTH1 and GTH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen Comp Endocrinol 124:45-52.
34. Miranda LA, Strobl-Mazzulla PH, Strüssmann CA, Parhar I, Somoza GM. 2003. Gonadotropin-releasing hormone neuronal development during the sensitive period of temperature sex determination in the pejerrey fish, Odontesthes bonariensis. Gen Comp Endocrinol 132:444-453.
35. Miranda LA, Cassará MC, Somoza GM. 2005. Increase of milt production by hormonal treatment in the pejerrey fish Odontesthes bonariensis. Aquac Res 36:1473-1479.
36. Miranda LA, Berasain GE, Velasco CM, Shirojo Y, Somoza GM. 2006. Natural spawning and intensive culture of pejerrey Odontesthes bonariensis juveniles. Biocell 30:89-95.
37. Miranda LA, Strüssmann CA, Guilgur LG, Strobl-Mazzulla HP, Somoza GM. 2007. Cloning of FSH-β, LH-β and glycoprotein hormone α subunits in pejerrey Odontesthes bonariensis (Valenciennes): Expression profile and relationship with GnRHs expression and plasma sex steroid levels in male fish. J Fish Biol 71:1571-1589.
38. Miranda LA, Strüssmann CA, Somoza GM. 2008. Effects of light and temperature on GnRHs, GtHs expression and plasma steroids levels in pejerrey (Odontesthes bonariensis) females. Fish Physiol Biochem 35:101-108.
39. 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. (Pubitemid 24058524)
40. Moles G, Carrillo M, Mañanós E, Mylonas CC, Zanuy S. 2007. Temporal profile of brain and pituitary GnRHs, GnRH-R and gonadotropin mRNA expression and content during early development in European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 150:75-86.
41. 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.
42. 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.
43. 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 129B:441-448.
44. Robert C, Gagné D, Lussier JG, Bousquet D, Barnes FL, Sirard MA. 2003. Presence of LH receptor mRNA in granulosa cells as a potential marker of oocyte developmental competence and characterization of the bovine splicing isoforms. Reproduction 125:437-446.
45. Rocha A,Gómez A, Zanuy S, Cerdá-Reverter JM, Carrillo M. 2007. Molecular characterization of two sea bass gonadotropin receptors: cDNA cloning, expression analysis, and functional activity. Mol Cell Endocrinol 272:63-76.
46. Silva J, Chang K, Hannon GJ, Rivas FV. 2004. RNA-interference-based functional genomics in mammalian cells: Reverse genetics coming of age. Oncogene 23:8401-8409.
47. Simoni M, Gromoll J, Nieschlag E. 1997. The follicle-stimulating hormone receptor: Biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 18:739-773.
48. 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.
49. Somoza GM, Miranda LA, Berasain GE, Colautti DC, Remes-Lenicov M, Strüssmann CA. 2008. Historical aspects, current status, and prospects of pejerrey aquaculture in South America. Aquac Res 9:784-793.
50. Strüssmann CA, Moriyama S, Hanke EF, Calsina Cota JC, Takashima F. 1996a. Evidence of thermolabile sex determination in pejerrey. J Fish Biol 48:643-651. (Pubitemid 27048094)
51. Strüssmann CA, Takashima F, Toda K. 1996b. Sex differentiation and hormonal feminization in pejerrey Odontesthes bonariensis. Aquaculture 139:31-45. (Pubitemid 126685182)
52. Strüssmann CA, Saito T, Usui M, Yamada H, Takashima F. 1997. Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J Exp Zool 278:167-177.
53. Swanson P, Dickey JT, Campbell B. 2003. Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:1-7.
54. Vischer HF, Bogerd J. 2003. Cloning and functional characterization of a gonadal luteinizing hormone receptor complementary DNA from the African catfish (Clarias gariepinus). Biol Rep 68:62-271.
55. White RB, Thomas P. 1992. Stimulation of in vitro steroidogenesis by pituitary hormones in a turtle (Trachemys scripta) within the temperature-sensitive period for sex determination. Biol Reprod 47:952-959.
56. Wong TT, Zohar Y. 2003. The involvement of gonadotropin receptors in sex reversal: Expression, distribution and regulation of gonadal FSH and LH receptors in the gilthead seabream. Fish Physiol Biochem 28:179-180.
57. Wong TT, Shigeho I, Zohar Y. 2006. 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 74:857-864.
58. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T. 2007. 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 359:935-940.
59. Yan L, Swanson P, Dickhoff WW. 1992. A two-receptor model for salmon gonadotropins GTH I and GTH II. Biol Rep 47:418-427.
60. Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O. 2010. Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438-455.