Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Intrafollicular oestradiol production, expression of the LH receptor (LHR) gene and its isoforms, and early follicular deviation in Bos indicus

S. Wohlres-Viana A , E. K. N. Arashiro B , M. A. Machado A C , L. S. A. Camargo A C , L. G. B. Siqueira C , M. P. Palhao B and J. H. M. Viana B D E
+ Author Affiliations
- Author Affiliations

A Federal University of Juiz de Fora, Rua Jose Lourenço Kelmer S/N, Juiz de Fora, MG, 36036-900 Brazil.

B University of Alfenas, Rod. MG 179 Km 0, Campus Universitario, Alfenas, MG, 37130-000 Brazil.

C Embrapa Gado de Leite, Rua Eugenio do Nascimento 610, Juiz de Fora, MG, 36038-330 Brazil.

D Embrapa Recursos Genéticos e Biotecnologia, PqEB, Av. W5 Norte, Brasília, DF, 70770-917 Brazil.

E Corresponding author. Email: henrique.viana@embrapa.br

Reproduction, Fertility and Development 29(10) 1958-1970 https://doi.org/10.1071/RD16284
Submitted: 20 July 2016  Accepted: 19 November 2016   Published: 21 December 2016

Abstract

The aim of the present study was to characterise the roles of intrafollicular oestradiol production and granulosa cell (GC) expression of the LH receptor (LHR) gene and its isoforms during follicular deviation in Bos indicus. Follicular wave emergence was synchronised in heifers from a Bos taurus dairy (Holstein; n = 10) and a B. indicus dairy breed (Gir; n = 10). Follicles were aspirated individually at sizes corresponding to the periods of predeviation, deviation and postdeviation. Intrafollicular oestradiol (IF-E2) and progesterone (IF-P4) concentrations were determined in the follicular fluid (FF) by radioimmunoassay, and relative expression of P450 aromatase (CYP19A1) and LHR forms was evaluated in GC using real-time quantitative–polymerase chain reaction. Despite differences in the size of the dominant follicle at deviation, changes in CYP19A1 expression and IF-E2 concentrations were similar in follicles of the same diameter in both breeds. A peak in total LHR expression occurred after follicular deviation in association with low expression of LHR isoforms. The results suggest that regulation of LHR function by sequential changes in the expression pattern of LHR isoforms may play a role in the early deviation of the dominant follicle, as observed in B. indicus breeds.

Additional keywords: alternative splicing, bovine, Bos indicus, follicular dynamics, steroidogenesis.


References

Aatsinki, J. T., Pietilg, E. M., Lakkakorpi, J. T., and Rajaniemi, H. J. (1992). Expression of the LH/CG receptor gene in rat ovarian tissue is regulated by an extensive alternative splicing of the primary transcript. Mol. Cell. Endocrinol. 84, 127–135.
Expression of the LH/CG receptor gene in rat ovarian tissue is regulated by an extensive alternative splicing of the primary transcript.CrossRef | 1:CAS:528:DyaK3sXhvVersrg%3D&md5=66a4df0f34af959a8e6a05db604a5ed4CAS |

Abdennebi, L., Lesport, A. S., Remy, J. J., Grebert, D., Pisselet, C., Monniaux, D., and Salesse, R. (2002). Differences in splicing of mRNA encoding LH receptor in theca cells according to breeding season in ewes. Reproduction 123, 819–826.
Differences in splicing of mRNA encoding LH receptor in theca cells according to breeding season in ewes.CrossRef | 1:CAS:528:DC%2BD38XkvVCiu7w%3D&md5=93fc799027bb2d532c97533b04ce5968CAS |

Alvarez, P., Spicer, L. J., Chase, C. C., Payton, M. E., Hamilton, T. D., Stewart, R. E., Hammond, A. C., Olson, T. A., and Wettemann, R. P. (2000). Ovarian and endocrine characteristics during an estrous cycle in Angus, Brahman, and Senepol cows in a subtropical environment. J. Anim. Sci. 78, 1291–1302.
Ovarian and endocrine characteristics during an estrous cycle in Angus, Brahman, and Senepol cows in a subtropical environment.CrossRef | 1:CAS:528:DC%2BD3cXjsFemurs%3D&md5=8778cbae6112159c275a36e396db89feCAS |

Amsterdam, A., Rotmensch, S., and Ben-Ze’ev, A. (1989). Coordinated regulation of morphological and biochemical differentiation in a steroidogenic cell: the granulosa cell model. Trends Biochem. Sci. 14, 377–382.
Coordinated regulation of morphological and biochemical differentiation in a steroidogenic cell: the granulosa cell model.CrossRef | 1:CAS:528:DyaK3cXmvFQ%3D&md5=1b778ec6f09bfc4b6a58890e713cf8e6CAS |

Arashiro, E. K. N., Palhao, M. P., Wohlres-Viana, S., Siqueira, L. G. B., Camargo, L. S. A., Henry, M., and Viana, J. H. M. (2013). In vivo collection of follicular fluid and granulosa cells from individual follicles of different diameters in cattle by adapted ovum pick-up system. Reprod. Biol. Endocrinol. 11, 73–80.
In vivo collection of follicular fluid and granulosa cells from individual follicles of different diameters in cattle by adapted ovum pick-up system.CrossRef |

Bacich, D. J., Rohan, R. M., Norman, R. J., and Rodgers, R. J. (1994). Characterization and relative abundance of alternatively spliced luteinizing hormone receptor messenger ribonucleic acid in the ovine ovary. Endocrinology 135, 735–744.
| 1:CAS:528:DyaK2cXlvFOnu74%3D&md5=cb5513e0ec9636f1d02f7e0d048d38b9CAS |

Bao, B., and Garverick, H. A. (1998). Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J. Anim. Sci. 76, 1903–1921.
Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review.CrossRef | 1:CAS:528:DyaK1cXkvV2hsLk%3D&md5=2db582294995c4a2fd6bdba3d79e5ca7CAS |

Bao, B., Garverick, A., Smith, G. W., Smith, M. F., Salfen, B. E., and Youngquist, R. S. (1997). Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles. Biol. Reprod. 56, 1158–1168.
Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles.CrossRef | 1:CAS:528:DyaK2sXisl2qs7w%3D&md5=74bbc8c6c805e052b909e53501d59d9eCAS |

Beg, M. A., Bergfelt, D. R., Kot, K., Wiltbank, M. C., and Ginther, O. J. (2001). Follicular-fluid factors and granulosa-cell gene expression associated with follicle deviation in cattle. Biol. Reprod. 64, 432–441.
Follicular-fluid factors and granulosa-cell gene expression associated with follicle deviation in cattle.CrossRef | 1:CAS:528:DC%2BD3MXnsVKrsg%3D%3D&md5=16e5ef7bcb1bdbd9aa571a3e9da543b7CAS |

Bó, G. A., Baruselli, P. S., and Martínez, M. F. (2003). Pattern and manipulation of follicular development in Bos indicus cattle. Anim. Reprod. Sci. 78, 307–326.
Pattern and manipulation of follicular development in Bos indicus cattle.CrossRef |

Bodensteiner, K. J., Wiltbank, M. C., Bergfelt, D. R., and Ginther, O. J. (1996). Alterations in follicular estradiol and gonadotropin receptors during development of bovine antral follicles. Theriogenology 45, 499–512.
Alterations in follicular estradiol and gonadotropin receptors during development of bovine antral follicles.CrossRef | 1:CAS:528:DyaK28Xit1GhtLw%3D&md5=4ea2fefab9a13986c4bc0eb1033ed0a4CAS |

Buratini, J., Teixeira, A. B., Costa, I. B., Glapinski, V. F., Pinto, M. G., Giometti, I. C., Barros, C. M., Cao, M., Nicola, E. S., and Price, C. A. (2005). Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles. Reproduction 130, 343–350.
Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles.CrossRef | 1:CAS:528:DC%2BD2MXhtFWisr3I&md5=2ec30abb46fc76635917c01503181387CAS |

Camargo, L. S. A., Boite, M. C., Wohlres-Viana, S., Mota, G. B., Serapiao, R. V., Sa, W. F., Viana, J. H. M., and Nogueira, L. A. G. (2011). Osmotic challenge and expression of aquaporin 3 and Na/K ATPase genes in bovine embryos produced in vitro. Cryobiology 63, 256–262.
Osmotic challenge and expression of aquaporin 3 and Na/K ATPase genes in bovine embryos produced in vitro.CrossRef | 1:CAS:528:DC%2BC3MXhsFCqsLfP&md5=e6557b4804b1664a3ef0873419035839CAS |

Carvalho, J. B., Carvalho, N. A., Reis, E. L., Nichi, M., Souza, A. H., and Baruselli, P. S. (2008). Effect of early luteolysis in progesterone-based timed AI protocols in Bos indicus, Bos indicus × Bos taurus, and Bos taurus heifers. Theriogenology 69, 167–175.
Effect of early luteolysis in progesterone-based timed AI protocols in Bos indicus, Bos indicus × Bos taurus, and Bos taurus heifers.CrossRef | 1:CAS:528:DC%2BD1cXhsVykug%3D%3D&md5=7fc45a36f869c253f319fabbc7155222CAS |

Castilho, C., Garcia, J. M., Renesto, A., Nogueira, G. P., and Brito, L. F. (2007). Follicular dynamics and plasma FSH and progesterone concentrations during follicular deviation in the first post-ovulatory wave in Nelore (Bos indicus) heifers. Anim. Reprod. Sci. 98, 189–196.
Follicular dynamics and plasma FSH and progesterone concentrations during follicular deviation in the first post-ovulatory wave in Nelore (Bos indicus) heifers.CrossRef | 1:CAS:528:DC%2BD2sXit1Gnu74%3D&md5=8b91d19195af55ac363908d9d9540f20CAS |

Diskin, M. G., Austin, E. J., and Roche, J. F. (2002). Exogenous hormonal manipulation of ovarian activity in cattle. Domest. Anim. Endocrinol. 23, 211–228.
Exogenous hormonal manipulation of ovarian activity in cattle.CrossRef | 1:CAS:528:DC%2BD38Xls1Wktb8%3D&md5=1dba7a99fe86b0909d001e0d4ba3e768CAS |

Ereno, R. L., Loureiro, B., Castilho, A. C. S., Machado, F. M., Pegorer, M. F., Satrapa, R. A., Nogueira, M. F. G., Buratini, J., and Barros, C. M. (2015). Expression of mRNA encoding the LH receptor (LHR) and LHR binding protein in granulosa cells from Nelore (Bos indicus) heifers around follicle deviation. Reprod. Domest. Anim. 50, 952–957.
Expression of mRNA encoding the LH receptor (LHR) and LHR binding protein in granulosa cells from Nelore (Bos indicus) heifers around follicle deviation.CrossRef | 1:CAS:528:DC%2BC2MXhvVCjtL7J&md5=2ee2bb27bc1bf5678754d37ab6e22e35CAS |

Gimenes, L. U., Sá Filho, M. F., Carvalho, N. A., Torres-Júnior, J. R., Souza, A. H., Madureira, E. H., Trinca, L. A., Sartorelli, E. S., Barros, C. M., Carvalho, J. B., Mapletoft, R. J., and Baruselli, P. S. (2008). Follicle deviation and ovulatory capacity in Bos indicus heifers. Theriogenology 69, 852–858.
Follicle deviation and ovulatory capacity in Bos indicus heifers.CrossRef | 1:CAS:528:DC%2BD1cXktFCltr4%3D&md5=77181e3ba8c63787eefd91c5f973d7abCAS |

Ginther, O. J., Wiltbank, M. C., Fricke, P. M., Gibbons, J. R., and Kot, K. (1996). Selection of the dominant follicle in cattle. Biol. Reprod. 55, 1187–1194.
Selection of the dominant follicle in cattle.CrossRef | 1:CAS:528:DyaK2sXkvV2gtA%3D%3D&md5=619a59f37b49ac11b890cdbf83e0b38cCAS |

Ginther, O. J., Kot, K., Kulick, L. J., and Wiltbank, M. C. (1997). Emergence and deviation of follicles during the development of follicular waves in cattle. Theriogenology 48, 75–87.
Emergence and deviation of follicles during the development of follicular waves in cattle.CrossRef | 1:STN:280:DC%2BD28zgtVylsg%3D%3D&md5=fdfee736b4670c517f66b7bf1abaf417CAS |

Ginther, O. J., Bergfelt, D. R., Kulick, L. J., and Kot, K. (1999). Selection of the dominant follicle in cattle: establishment of follicle deviation in less than 8 hours through depression of FSH concentrations. Theriogenology 52, 1079–1093.
Selection of the dominant follicle in cattle: establishment of follicle deviation in less than 8 hours through depression of FSH concentrations.CrossRef | 1:CAS:528:DyaK1MXotFaitrg%3D&md5=8af0d591015c167373a79d8e393a09bcCAS |

Ginther, O. J., Beg, M. A., Bergfelt, D. R., Donadeu, F. X., and Kot, K. (2001a). Follicle selection in monovular species. Biol. Reprod. 65, 638–647.
Follicle selection in monovular species.CrossRef | 1:CAS:528:DC%2BD3MXmtFenu70%3D&md5=e89d3a6f02f816980d1ee9834a25b93fCAS |

Ginther, O. J., Bergfelt, D. R., Beg, M. A., and Kot, K. (2001b). Follicle selection in cattle: role of luteinizing hormone. Biol. Reprod. 64, 197–205.
Follicle selection in cattle: role of luteinizing hormone.CrossRef | 1:CAS:528:DC%2BD3MXhtFClug%3D%3D&md5=ddb5faa0c6ef6e3c41a660fa2279d576CAS |

Ginther, O. J., Beg, M. A., Donadeu, F. X., and Gerfelt, D. R. (2003). Mechanism of follicle deviation in monovular farm species. Anim. Reprod. Sci. 78, 239–257.
Mechanism of follicle deviation in monovular farm species.CrossRef | 1:CAS:528:DC%2BD3sXksF2gtro%3D&md5=aaa7452c0604b3adf853d0117fd51b3fCAS |

Hastings, N., Donn, S., Derecka, K., Flint, A. P., and Woolliams, J. A. (2006). Polymorphisms within the coding region of the bovine luteinizing hormone receptor gene and their association with fertility traits. Anim. Genet. 37, 583–585.
Polymorphisms within the coding region of the bovine luteinizing hormone receptor gene and their association with fertility traits.CrossRef | 1:CAS:528:DC%2BD2sXmvFKisQ%3D%3D&md5=92eca92bef3d47a1ad1b7d2ef12f508cCAS |

Jiang, J. Y., Macchiarelli, G., Tsang, B. K., and Sato, E. (2003). Capillary angiogenesis and degeneration in bovine ovarian antral follicles. Reproduction 125, 211–223.
Capillary angiogenesis and degeneration in bovine ovarian antral follicles.CrossRef | 1:CAS:528:DC%2BD3sXisVKlt7w%3D&md5=1888e3c39a9ec55b4f3cd07681f630f6CAS |

Jolly, P. D., Tisdall, D. J., Heath, D. A., Lun, S., and McNatty, K. P. (1994). Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3′,5′-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia. Biol. Reprod. 51, 934–944.
Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3′,5′-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia.CrossRef | 1:CAS:528:DyaK2cXmsVKktb4%3D&md5=039cd331b12316d6db3d92fc5d67510aCAS |

Kawate, N. (2004). Studies on the regulation of expression of luteinizing hormone receptor in the ovary and the mechanism of follicular cyst formation in ruminants. J. Reprod. Dev. 50, 1–8.
Studies on the regulation of expression of luteinizing hormone receptor in the ovary and the mechanism of follicular cyst formation in ruminants.CrossRef | 1:CAS:528:DC%2BD2cXjvVGgsrw%3D&md5=0189919b7faf74202384cc97c37a8785CAS |

Kawate, N., and Okuda, K. (1998). Coodinated expression of splice variants for luteinizing hormone receptor messenger RNA during the development of bovine corpora lutea. Mol. Reprod. Dev. 51, 66–75.
Coodinated expression of splice variants for luteinizing hormone receptor messenger RNA during the development of bovine corpora lutea.CrossRef | 1:CAS:528:DyaK1cXltVGrsLw%3D&md5=756cf91fb4388781aaf8801c3764aab6CAS |

Kawate, N., Tamada, H., Inaba, T., and Sawada, T. (2002). Expression of a cloned full-length cDNA encoding bovine luteinizing hormone receptor in COS-7 cells. J. Reprod. Dev. 48, 531–538.
Expression of a cloned full-length cDNA encoding bovine luteinizing hormone receptor in COS-7 cells.CrossRef | 1:CAS:528:DC%2BD3sXntF2r&md5=f22621ed8faea74f76e7a028d3f7b7b8CAS |

Kayani, A. R., Glister, C., and Knight, P. G. (2009). Evidence for an inhibitory role of bone morphogenetic protein(s) in the follicular–luteal transition in cattle. Reproduction 137, 67–78.
Evidence for an inhibitory role of bone morphogenetic protein(s) in the follicular–luteal transition in cattle.CrossRef | 1:CAS:528:DC%2BD1MXovVKgsLg%3D&md5=0670602d5fac5dfee0be8fb18e442581CAS |

Korbie, D. J., and Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat. Protoc. 3, 1452–1456.
Touchdown PCR for increased specificity and sensitivity in PCR amplification.CrossRef | 1:CAS:528:DC%2BD1cXhtVOnsL7F&md5=81d19832c698a0cc0c26d82717d922d9CAS |

Kulick, L. J., Kot, K., Wiltbank, M. C., and Ginther, O. J. (1999). Follicular and hormonal dynamics during the first follicular wave in heifers. Theriogenology 52, 913–921.
Follicular and hormonal dynamics during the first follicular wave in heifers.CrossRef | 1:CAS:528:DyaK1MXns1Ohur4%3D&md5=7e6a6affc308255ebac27bd18d3dd0e9CAS |

Kulick, L. J., Bergfelt, D. R., Kot, K., and Ginther, O. J. (2001). Follicle selection in cattle: follicle deviation and codominance within sequential waves. Biol. Reprod. 65, 839–846.
Follicle selection in cattle: follicle deviation and codominance within sequential waves.CrossRef | 1:CAS:528:DC%2BD3MXmtFems7c%3D&md5=22d1c789102fd11b931bd53fa1599c7cCAS |

Lehmann, T., Biernacka-Lukanty, J., and Trzeciak, W. H. (2000). Expression of three negative regulators of CYP17 gene transcription in adrenocortical cells. Endocr. Res. 26, 1019–1026.
Expression of three negative regulators of CYP17 gene transcription in adrenocortical cells.CrossRef | 1:CAS:528:DC%2BD3MXotlKgsA%3D%3D&md5=88d7930d9231abb76855a4979492a12fCAS |

Loosfelt, H., Misrahi, M., Atger, M., Salesse, R., Thi, M. T. V. H.-L., Jolivet, A., Guiochon-Mantel, A., Sar, S., Jallal, B., Garnier, J., and Milgron, E. (1989). Cloning and sequencing of porcine LH–hCG receptor cDNA: variants lacking transmembrane domain. Science 245, 525–528.
Cloning and sequencing of porcine LH–hCG receptor cDNA: variants lacking transmembrane domain.CrossRef | 1:CAS:528:DyaK3cXksFegsbw%3D&md5=0986fdc46c96e1d9221d574b90633019CAS |

Madhra, M., Gay, E., Fraser, H. M., and Duncan, W. C. (2004). Alternative splicing of the human luteal LH receptor during luteolysis and maternal recognition of pregnancy. Mol. Hum. Reprod. 10, 599–603.
Alternative splicing of the human luteal LH receptor during luteolysis and maternal recognition of pregnancy.CrossRef | 1:CAS:528:DC%2BD2cXlsl2rsLo%3D&md5=43f267ca4839bda29d7d12993278ef3bCAS |

Mamluk, R., Wolfenson, D., and Meidan, R. (1998). LH receptor mRNA and cytochrome P450 side-chain cleavage expression in bovine theca and granulosa cells luteinized by LH or forskolin. Domest. Anim. Endocrinol. 15, 103–114.
LH receptor mRNA and cytochrome P450 side-chain cleavage expression in bovine theca and granulosa cells luteinized by LH or forskolin.CrossRef | 1:CAS:528:DyaK1cXitFektLc%3D&md5=9e81e1b204c68ec33a17206fab23090eCAS |

Mihm, M., Good, T. E., Ireland, J. L., Ireland, J. J., Knight, P. G., and Roche, J. F. (1997). Decline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers. Biol. Reprod. 57, 1328–1337.
Decline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers.CrossRef | 1:CAS:528:DyaK2sXnvVWgu7s%3D&md5=b91752a929abe47eedf19a1e6f6130a8CAS |

Mihm, M., Austin, E. J., Good, T. E., Ireland, J. L., Knight, P. G., Roche, J. F., and Ireland, J. J. (2000). Identification of potential intrafollicular factors involved in selection of dominant follicles in heifers. Biol. Reprod. 63, 811–819.
Identification of potential intrafollicular factors involved in selection of dominant follicles in heifers.CrossRef | 1:CAS:528:DC%2BD3cXmtFCiu7w%3D&md5=de45bdc4658abf6fcd631a60331683f6CAS |

Minegishi, T., Tano, M., Abe, Y., Nakamura, K., Ibuki, Y., and Miyamoto, K. (1997). Expression of luteinizing hormone/human chorionic gonadotrophin (LH/HCG) receptor mRNA in the human ovary. Mol. Hum. Reprod. 3, 101–107.
Expression of luteinizing hormone/human chorionic gonadotrophin (LH/HCG) receptor mRNA in the human ovary.CrossRef | 1:CAS:528:DyaK2sXis1Gqs7g%3D&md5=8b6edfcccc38626a3771757c56c5ac02CAS |

Müller, T., Gromoll, J., and Simoni, M. (2003). Absence of exon 10 of the human luteinizing hormone (LH) receptor impairs LH, but not human chorionic gonadotropin action. J. Clin. Endocrinol. Metab. 88, 2242–2249.
Absence of exon 10 of the human luteinizing hormone (LH) receptor impairs LH, but not human chorionic gonadotropin action.CrossRef |

Nogueira, M. F. G., Buratini, J., Price, C. A., Castilho, A. C. S., Pinto, M. G. L., and Barros, C. M. (2007). Expression of LH receptor mRNA splice variants in bovine granulosa cells: changes with follicle size and regulation by FSH in vitro. Mol. Reprod. Dev. 74, 680–686.
Expression of LH receptor mRNA splice variants in bovine granulosa cells: changes with follicle size and regulation by FSH in vitro.CrossRef | 1:CAS:528:DC%2BD2sXltVGrtro%3D&md5=c74a78709678f1dd313f6f2894caa032CAS |

Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.CrossRef |

Puett, D., Angelova, K., da Costa, M. R., Warrenfeltz, S. W., and Fanelli, F. (2010). The luteinizing hormone receptor: insights into structure–function relationships and hormone-receptor-mediated changes in gene expression in ovarian cancer cells. Mol. Cell. Endocrinol. 329, 47–55.
The luteinizing hormone receptor: insights into structure–function relationships and hormone-receptor-mediated changes in gene expression in ovarian cancer cells.CrossRef | 1:CAS:528:DC%2BC3cXht1Srur%2FI&md5=d571cddb778920bea6eff19d373fc90aCAS |

Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.CrossRef | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=b0465bfb122d6cd96afdfbdf998ea00dCAS |

Rhodes, R. C., Randel, R. D., and Harms, P. G. (1978). Reproductive studies of Brahman cattle IV. Luteinizing hormone levels in ovariectomized Brahman, Brahman × Hereford and Hereford cows following a 20 mg dose of estradiol-17β. Theriogenology 10, 429–437.
Reproductive studies of Brahman cattle IV. Luteinizing hormone levels in ovariectomized Brahman, Brahman × Hereford and Hereford cows following a 20 mg dose of estradiol-17β.CrossRef | 1:CAS:528:DyaE1MXhsVKisLw%3D&md5=94edaa7ad15dc096d8953fe48f827595CAS |

Rhodes, F. M., Peterson, A. J., and Jolly, P. D. (2001). Gonadotrophin responsiveness, aromatase activity and insulin-like growth factor binding protein content of bovine ovarian follicles during the first follicular wave. Reproduction 122, 561–569.
Gonadotrophin responsiveness, aromatase activity and insulin-like growth factor binding protein content of bovine ovarian follicles during the first follicular wave.CrossRef | 1:CAS:528:DC%2BD3MXotFGltbg%3D&md5=39237934c1cf42e7756e81904e22e0dcCAS |

Robert, C., Gagné, D., Lussier, J. G., Bousquet, D., Barnes, F. L., and Sirard, M.-A. (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.
Presence of LH receptor mRNA in granulosa cells as a potential marker of oocyte developmental competence and characterization of the bovine splicing isoforms.CrossRef | 1:CAS:528:DC%2BD3sXjtVWqtbo%3D&md5=d8d1316d9bd1ccdc09b54d7d9d3e27f1CAS |

Roberts, A. J., and Echternkamp, S. E. (1994). In vitro production of estradiol by bovine granulosa cells: evaluation of culture condition, stage of follicular development, and location of cells within follicles. Biol. Reprod. 51, 273–282.
In vitro production of estradiol by bovine granulosa cells: evaluation of culture condition, stage of follicular development, and location of cells within follicles.CrossRef | 1:CAS:528:DyaK2cXltVSit7k%3D&md5=9525b7b5843e1bb0ec8b57bd6e8dd2ddCAS |

Rodrigues, H. D., Kinder, J. E., and Fitzpatrick, L. A. (2002). Estradiol regulation of luteinizing hormone secretion in heifers of two breed types that reach puberty at different ages. Biol. Reprod. 66, 603–609.
Estradiol regulation of luteinizing hormone secretion in heifers of two breed types that reach puberty at different ages.CrossRef | 1:CAS:528:DC%2BD38XhvVeitLg%3D&md5=3eab3cc2e12cc3c7e018f6c32646fd7dCAS |

Rouillier, P., Matton, P., Sirard, M. A., and Guilbault, L. A. (1996). Follicle-stimulating hormone-induced estradiol and progesterone production by bovine antral and mural granulosa cells cultured in vitro in a completely defined medium. J. Anim. Sci. 74, 3012–3019.
Follicle-stimulating hormone-induced estradiol and progesterone production by bovine antral and mural granulosa cells cultured in vitro in a completely defined medium.CrossRef | 1:CAS:528:DyaK2sXksFGmtg%3D%3D&md5=17368abc111b413c3440e57e9b89ca6bCAS |

Rouillier, P., Matton, P., Dufour, M., Sirard, M. A., and Guilbault, L. A. (1998). Steroid production, cell proliferation, and apoptosis in cultured bovine antral and mural granulosa cells: development of an in vitro model to study estradiol production. Mol. Reprod. Dev. 50, 170–177.
Steroid production, cell proliferation, and apoptosis in cultured bovine antral and mural granulosa cells: development of an in vitro model to study estradiol production.CrossRef | 1:CAS:528:DyaK1cXislWksL8%3D&md5=d551f4a14342aad7c08d4b17991ac7cfCAS |

Sangsritavong, S., Combs, D. K., Sartori, R., Armentano, L. E., and Wiltbank, M. C. (2002). High feed intake increases liver blood flow and metabolism of progesterone and estradiol-17beta in dairy cattle. J. Dairy Sci. 85, 2831–2842.
High feed intake increases liver blood flow and metabolism of progesterone and estradiol-17beta in dairy cattle.CrossRef | 1:CAS:528:DC%2BD38Xptlagsbc%3D&md5=009defb50c627304374268019ce57f1bCAS |

Sartorelli, E. S., Carvalho, L. M., Bergfelt, D. R., Ginther, O. J., and Barros, C. M. (2005). Morphological characterization of follicle deviation in Nelore (Bos indicus) heifers and cows. Theriogenology 63, 2382–2394.
Morphological characterization of follicle deviation in Nelore (Bos indicus) heifers and cows.CrossRef |

Sartori, R., and Barros, C. M. (2011). Reproductive cycles in Bos indicus cattle. Anim. Reprod. Sci. 124, 244–250.
Reproductive cycles in Bos indicus cattle.CrossRef | 1:CAS:528:DC%2BC3MXlvFWhur4%3D&md5=a8b9fcf10504bb9b3c69e7cb6b341b5eCAS |

Schoenemann, H. M., Humphrey, W. D., Crowder, M. E., Nett, T. M., and Reeves, J. J. (1985). Pituitary luteinizing hormone-releasing hormone receptors in ovariectomized cows after challenge with ovarian steroids. Biol. Reprod. 32, 574–583.
Pituitary luteinizing hormone-releasing hormone receptors in ovariectomized cows after challenge with ovarian steroids.CrossRef | 1:CAS:528:DyaL2MXhvFygsb8%3D&md5=434d7c5e5d45372b98ecc5e251be27dbCAS |

Simões, R. A. L., Satrapa, R. A., Rosa, F. S., Piagentini, M., Castilho, A. C. S., Ereno, R. L., Trinca, L. A., Nogueira, M. F. G., Buratini, J., and Barros, C. M. (2012). Ovulation rate and its relationship with follicle diameter and gene expression of the LH receptor (LHR) in Nelore cows. Theriogenology 77, 139–147.
Ovulation rate and its relationship with follicle diameter and gene expression of the LH receptor (LHR) in Nelore cows.CrossRef |

Sirard, M. A., Robert, C., Gagne, D., Bousquet, D., and Barnes, F. L. (2000). Splicing isoforms of the bovine LH receptor in granulosa cells of follicles with oocytes of different developmental competencies. Theriogenology 53, 412.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=bb3fb25b0d27e6d57e84605483303a88CAS |

Viana, J. H. M., Ferreira, A. M., Sá, W. F., and Camargo, L. S. A. (2000). Follicular dynamics in zebu cattle. Pesqui. Agropecu. Bras. 35, 2501–2509.
Follicular dynamics in zebu cattle.CrossRef |

Viana, J. H., Palhao, M. P., Siqueira, L. G., Fonseca, J. F., and Camargo, L. S. (2010). Ovarian follicular dynamics, follicle deviation, and oocyte yield in Gyr breed (Bos indicus) cows undergoing repeated ovum pick-up. Theriogenology 73, 966–972.
Ovarian follicular dynamics, follicle deviation, and oocyte yield in Gyr breed (Bos indicus) cows undergoing repeated ovum pick-up.CrossRef | 1:STN:280:DC%2BC3c3gsVShtg%3D%3D&md5=200df9c4af46c3e73c9eda139570b77eCAS |

Viana, J. H., Dorea, M. D., Siqueira, L. G., Arashiro, E. K., Camargo, L. S., Fernandes, C. A., and Palhão, M. P. (2013). Occurrence and characteristics of residual follicles formed after transvaginal ultrasound-guided follicle aspiration in cattle. Theriogenology 79, 267–273.
Occurrence and characteristics of residual follicles formed after transvaginal ultrasound-guided follicle aspiration in cattle.CrossRef | 1:CAS:528:DC%2BC38XhslSmtb7P&md5=797b6dff1ff24e7cb727bbc3f3734b5bCAS |

Wohlres-Viana, S., Arashiro, E. K. N., Reis, D. R. L., Fernandes, L. E., Peixoto, M. G. C. D., Machado, M. A., and Viana, J. H. M. (2016). Polymorphisms and alternative splicing of the luteinizing hormone receptor of dairy cattle. Genet. Mol. Res. 15, gmr.15017046.
Polymorphisms and alternative splicing of the luteinizing hormone receptor of dairy cattle.CrossRef |

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.
Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave.CrossRef | 1:CAS:528:DyaK2MXotFyisrk%3D&md5=1ac063c64493dfe94e4cce2b4758aa7fCAS |

Zhang, F. P., Kero, J., and Huhtaniemi, I. (1998). The unique exon 10 of the human luteinizing hormone receptor is necessary for expression of the receptor protein at the plasma membrane in the human luteinizing hormone receptor, but deleterious when inserted into the human follicle-stimulating hormone receptor. Mol. Cell. Endocrinol. 142, 165–174.
The unique exon 10 of the human luteinizing hormone receptor is necessary for expression of the receptor protein at the plasma membrane in the human luteinizing hormone receptor, but deleterious when inserted into the human follicle-stimulating hormone receptor.CrossRef | 1:CAS:528:DyaK1cXkvFOksLo%3D&md5=fe401deb625a46cb11eda54e15b3753fCAS |



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