Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Expression of follicle-stimulating hormone and luteinising hormone binding sites in the bitch ovary during the follicular phase

Marie Saint-Dizier A B E F , Nina Jaffré A E , Karine Reynaud A , Benoît Remy D , Sandra Thoumire A C and Sylvie Chastant-Maillard A C
+ Author Affiliations
- Author Affiliations

A UMR 1198 INRA/ENVA/CNRS Biologie du Développement et Reproduction, 7 Avenue du Général de Gaulle, 94 700 Maisons-Alfort, France.

B AgroParisTech (Paris Institute of Technology for Life, Food and Environmental Sciences), 16 rue Claude Bernard, 75 231 Paris Cedex 05, France.

C Department of Reproduction, Ecole Nationale Vétérinaire d’Alfort, 7 Avenue du Général de Gaulle, 94 700 Maisons-Alfort, France.

D Physiologie de la reproduction animale, Faculté de Médecine Vétérinaire, Université de Liège, Boulevard de Colonster 20, B-4000 Liège (Sart Tilman), Belgique.

E These authors contributed equally to this work.

F Corresponding author. Email: stdizier@agroparistech.fr

Reproduction, Fertility and Development 20(8) 925-934 https://doi.org/10.1071/RD08119
Submitted: 26 May 2008  Accepted: 21 July 2008   Published: 10 October 2008

Abstract

In the female dog, in contrast with most mammals, the growing follicle starts to luteinise several days before ovulation. Little is known about the physiological control of the final follicular growth in this species. In order to better understand the pituitary regulation of follicular growth, specific binding sites for FSH and LH were localised and quantified by autoradiography using [125I]-porcine (p) gonadotrophins on ovarian sections (7 μm) from adult Beagle bitches during the follicular phase. Follicles were analysed either before the LH surge (n = 4 bitches; n = 117 follicles) or after the LH surge and before ovulation (n = 5 bitches; n = 110 follicles). FSH binding sites were specifically and homogeneously expressed at high levels on granulosa cells of all healthy follicles from the preantral stage onwards. In contrast, LH binding sites were detected homogeneously and at high levels only on granulosa cells of follicles larger than 1 mm in diameter, including luteinised follicles. Theca binding of LH (but not FSH) was also observed, but only when using high concentrations of [125I]-pLH. The overall incidence of atresia was 45.8% and was dependent upon follicular diameter. Quantitative analysis of labelling showed that atretic follicles had reduced levels of both FSH and LH binding sites compared with healthy follicles. In healthy follicles, levels of both FSH and LH binding sites changed with follicle diameter. Compared with other mammals, the acquisition of LH binding on canine granulosa cells occurs in smaller sized follicles relative to the size of ovulation.


Acknowledgements

The authors thank Marc Chodkiewicz for critical reading of the manuscript. This work was funded by the National Institute for Agronomic Research (INRA) and the French Department of Agriculture and Fishing (Ministère de l’Agriculture et de la Pêche). The authors declare that there is no conflict of interest that would prejudice the impartiality of this study.


References

Abdennebi, L. , Monget, P. , Pisselet, C. , Remy, J. J. , Salesse, R. , and Monniaux, D. (1999). Comparative expression of luteinizing hormone and follicle-stimulating hormone receptors in ovarian follicles from high and low prolific sheep breeds. Biol. Reprod. 60, 845–854.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Anderson A. C., and Simpson M. E. (1973). ‘The Ovary and Reproduction Cycle of the Dog (BEAGLE).’ (Geron-X Inc.: Los Altos.)

Ascoli, M. , Fanelli, F. , and Segaloff, D. L. (2002). The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141–174.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Marseloo N., Fontbonne A., Bassu G., Rivière S., Leblanc B., Rault D., Biourge V., and Chastant-Maillard S. (2004). Comparison of ovarian ultrasonography with hormonal parameters for the determination of the time of ovulation in bitches. In ‘Proceedings of the 5th International Symposium on Canine and Feline Reproduction: Basic and Applied Research on Domestic, Exotic and Endangered Carnivores, 4–5 August 2004, Embu das Artes, São Paulo, Brazil’. pp. 132–134.

McBride, M. W. , Aughey, E. , O’Shaughnessy, P. J. , and Jeffcoate, I. A. (2001). Ovarian function and FSH receptor characteristics during canine anoestrus. J. Reprod. Fertil. Suppl. 57, 3–10.
PubMed |  CAS |

McDougall, K. , Hay, M. A. , Goodrowe, K. L. , Garley, C. J. , and King, W. A. (1997). Changes in the number of follicles and of oocytes in ovaries of prepubertal, peripubertal and mature bitches. J. Reprod. Fertil. Suppl. 51, 25–31.
PubMed |  CAS |

Meduri, G. , Vuhai-Luuthi, M. T. , Jolivet, A. , and Milgrom, E. (1992). New functional zonation in the ovary as shown by immunohistochemistry of luteinizing hormone receptor. Endocrinology 131, 366–373.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Millar, W. T. , and Smith, J. F. (1983). Protein iodination using iodogen. Int. J. Appl. Radiat. Isot. 34, 639–641.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Monniaux, D. , and de Reviers, M. M. (1989). Quantitative autoradiographic study of FSH binding sites in prepubertal ovaries of three strains of rats. J. Reprod. Fertil. 85, 151–162.
PubMed |  CAS |

Monniaux, D. , Huet, C. , Besnard, N. , Clement, F. , Bosc, M. , Pisselet, C. , and Monget, P. (1997). Follicular growth and ovarian dynamics in mammals. J. Reprod. Fertil. Suppl. 51, 3–23.
PubMed |  CAS |

Murphy, B. D. (2000). Models of luteinization. Biol. Reprod. 63, 2–11.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Nakano, R. , Sasaki, K. , Shima, K. , and Kitayama, S. (1983). follicle-stimulating hormone and luteinizing hormone receptors on porcine granulosa cells during follicular maturation: an autoradiographic study. Exp. Clin. Endocrinol. 81, 17–23.
PubMed |  CAS |

Oktay, K. , Briggs, D. , and Gosden, R. G. (1997). Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J. Clin. Endocrinol. Metab. 82, 3748–3751.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Oxberry, B. A. , and Greenwald, G. S. (1982). An autoradiographic study of the binding of 125I-labeled follicle-stimulating hormone, human chorionic gonadotropin and prolactin to the hamster ovary throughout the estrous cycle. Biol. Reprod. 27, 505–516.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Paisley, L. G. , and Fahning, M. L. (1977). Effects of exogenous follicle-stimulating hormone and luteinizing hormone in bitches. J. Am. Vet. Med. Assoc. 171, 181–185.
PubMed |  CAS |

Reynaud, K. , Fontbonne, A. , Marseloo, N. , Thoumire, S. , Chebrout, M. , Viaris de Lesegno, C. V. , and Chastant-Maillard, S. (2005). In vivo meiotic resumption, fertilization and early embryonic development in the bitch. Reproduction 130, 193–201.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Reynaud, K. , Fontbonne, A. , Marseloo, N. , Viaris de Lesegno, C. V. , Saint-Dizier, M. , and Chastant-Maillard, S. (2006). In vivo canine oocyte maturation, fertilization and early embryogenesis: a review. Theriogenology 66, 1685–1693.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Roy, S. K. , Wang, S. C. , and Greenwald, G. S. (1987). Radioreceptor and autoradiographic analysis of FSH, hCG and prolactin binding sites in primary to antral hamster follicles during the periovulatory period. J. Reprod. Fertil. 79, 307–313.
PubMed |  CAS |

Saint-Dizier, M. , Malandain, E. , Thoumire, S. , Remy, B. , and Chastant-Maillard, S. (2007). Expression of follicle stimulating hormone and luteinizing hormone receptors during follicular growth in the domestic cat ovary. Mol. Reprod. Dev. 74, 989–996.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Shille, V. M. , Thatcher, M. J. , and Simmons, K. J. (1984). Efforts to induce estrus in the bitch, using pituitary gonadotropins. J. Am. Vet. Med. Assoc. 184, 1469–1473.
PubMed |  CAS |

Shima, K. , Kitayama, S. , and Nakano, R. (1987). Gonadotropin binding sites in human ovarian follicles and corpora lutea during the menstrual cycle. Obstet. Gynecol. 69, 800–806.
PubMed |  CAS |

Simoni, M. , Gromoll, J. , and Nieschlag, E. (1997). The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18, 739–773.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Spanel-Borowski, K. (1981). Morphological investigations on follicular atresia in canine ovaries. Cell Tissue Res. 214, 155–168.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Spanel-Borowski, K. , Thor-Wiedemann, S. , and Pilgrim, C. (1984). Cell proliferation in the dog (beagle) ovary during prooestrus and early oestrus. Acta Anat. 118, 153–158.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Stocco, C. , Telleria, C. , and Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117–149.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Takao, Y. , Honda, T. , Ueda, M. , Hattori, N. , Yamada, S. , Maeda, M. , Fujiwara, H. , Mori, T. , and Wimalasena, J. (1997). Immunohistochemical localization of the LH/hCG receptor in human ovary: hCG enhances cell surface expression of LH/hCG receptor on luteinizing granulosa cells in vitro. Mol. Hum. Reprod. 3, 569–578.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Teerds, K. J. , and Dorrington, J. H. (1995). Immunolocalization of transforming growth factor alpha and luteinizing hormone receptor in healthy and atretic follicles of the adult rat ovary. Biol. Reprod. 52, 500–508.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Telfer, E. , and Gosden, R. G. (1987). A quantitative cytological study of polyovular follicles in mammalian ovaries with particular reference to the domestic bitch (Canis familiaris). J. Reprod. Fertil. 8, 137–147.


Tisdall, D. J. , Watanabe, K. , Hudson, N. L. , Smith, P. , and McNatty, K. P. (1995). FSH receptor gene expression during ovarian follicle development in sheep. J. Mol. Endocrinol. 15, 273–281.
PubMed |  CAS |

Uilenbroek, J. T. , Woutersen, P. J. , and van der Schoot, P. (1980). Atresia of preovulatory follicles: gonadotropin binding and steroidogenic activity. Biol. Reprod. 23, 219–229.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Verstegen, J. , Onclin, K. , Silva, L. , and Concannon, P. W. (1997). Termination of obligate anoestrus and induction of fertile ovarian cycles in dogs by administration of purified pig LH. J. Reprod. Fertil. 111, 35–40.
PubMed |  CAS |

Wandji, S. A. , Pelletier, G. , and Sirard, M. A. (1992). Ontogeny and cellular localization of 125I-labeled insulin-like growth factor-I, 125I-labeled follicle-stimulating hormone, and 125I-labeled human chorionic gonadotropin binding sites in ovaries from bovine fetuses and neonatal calves. Biol. Reprod. 47, 814–822.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Wildt, D. E. , Panko, W. B. , Chakraborty, P. K. , and Seager, S. W. (1979). Relationship of serum estrone, estradiol-17beta and progesterone to LH, sexual behavior and time of ovulation in the bitch. Biol. Reprod. 20, 648–658.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Xu, Z. , Garverick, H. A. , Smith, G. W. , Smith, M. F. , Hamilton, S. A. , and Youngquist, R. S. (1995). Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Biol. Reprod. 53, 951–957.
Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |