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

Retinol-binding protein (RBP), retinol and β-carotene in the bovine uterus and plasma during the oestrous cycle and the relationship between systemic progesteroneand RBP on Day 7

Lisa M. Costello A B D , Padraic O’Boyle A , James D. Godkin C , Michael G. Diskin A , Ailish C. Hynes B and Dermot G. Morris A E
+ Author Affiliations
- Author Affiliations

A Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc, Mellows Campus, Athenry, Galway, Ireland.

B Department of Physiology, National University of Ireland, Galway, University Road, Galway, Ireland.

C Department of Animal Science, University of Tennessee, Knoxville, TN 37996, USA.

D Present address: Abbott Ireland Diagnostic Division, Finisklin Industrial Estate, Sligo, County Sligo, Ireland.

E Corresponding author. Email: dermot.morris@teagasc.ie

Reproduction, Fertility and Development 22(8) 1198-1205 https://doi.org/10.1071/RD10034
Submitted: 25 February 2010  Accepted: 17 May 2010   Published: 1 October 2010

Abstract

In the dairy cow, low systemic concentrations of progesterone are known to be a major factor associated with early embryo loss. Endometrial expression of the gene encoding retinol-binding protein (RBP) is sensitive to small changes in progesterone on Day 7 of the oestrous cycle. The objectives of the present study were to measure RBP concentrations in bovine uterine flushings and plasma across different days of the oestrous cycle and to examine the relationship between uterine RBP and systemic concentrations of progesterone. Uterine flushings and plasma were collected from cows on Days 3, 7, 11 and 15 of the oestrous cycle. Uterine RBP concentrations were five- to 15-fold higher (P < 0.001) on Day 15 compared with the other days and twofold higher (P < 0.001) in the uterine horn ipsilateral to the corpus luteum on Day 15. RBP concentrations were similar in flushings and plasma across Days 3–11; however, Day 15 RBP concentrations were six- to 15-fold higher (P < 0.001) in uterine flushings. No significant relationship was found between the concentration of systemic progesterone and RBP concentrations on Day 7. Overall, the results of the present study indicate a local controlling mechanism operating at the level of the endometrium to regulate RBP secretion, most likely progesterone.

Additional keywords: embryo loss, fertility, uterine fluid.


Acknowledgements

The authors thank A. Glynn, B. Coen, L. Kerrigan, P. Joyce, W. Connolly and J. Nally for technical assistance and A. Monaghan and M. Shields for care of the animals.


References

Adams, K. L. , Bazer, F. W. , and Roberts, R. M. (1981). Progesterone-induced secretion of a retinol-binding protein in the pig uterus. J. Reprod. Fertil. 62, 39–47.
CrossRef | PubMed | CAS |

Anderson, G. W. , Gwazdauskas, F. C. , and Guise, M. B. (1985). Column chromatography and electrophoresis of bovine uterine lumenal protiens collected during the estrous cycle. Anim. Reprod. Sci. 9, 11–24.
CrossRef | CAS |

Bartol, F. F. , Thatcher, W. W. , Bazer, F. W. , Kimball, F. A. , Chenault, J. R. , Wilcox, C. J. , and Roberts, R. M. (1981). Effects of the estrous cycle and early pregnancy on bovine uterine, luteal, and follicular responses. Biol. Reprod. 25, 759–776.
CrossRef | PubMed | CAS |

Chandra Roy, S. , Uma Suganthi, R. , and Ghosh, J. (2006). Changes in uterine protein secretion during luteal and folicualr phases and detection of phosphatases during luteal of estrous cycle in buffaloes (Bubalus bubalis). Theriogenology 65, 1292–1301.
CrossRef | PubMed |

Chiamenti, A. , Aguiar Filho, C. , Freitas Neto, L. M. , Chaves, R. M. , Paula-Lopes, F. F. , Lima, P. F. , Goncalves, P. B. , and Oliveira, M. A. (2009). Effects of retinoids on the in vitro development of Capra hircus embryos to blastocysts in two different culture systems. Reprod. Domest. Anim. ,
CrossRef | PubMed |

Eberhardt, D. M. , Will, W. A. , and Godkin, J. D. (1999). Retinol administration to superovulated ewes improves in vitro embryonic viability. Biol. Reprod. 60, 1483–1487.
CrossRef | PubMed | CAS |

Ellington, J. E. (1991). The bovine oviduct and its role in reproduction: a review of the literature. Cornell Vet. 81, 313–328.
PubMed | |  CAS |

Fazleabas, A. T. , Donnelly, K. M. , Mavrogianis, P. A. , and Verhage, H. G. (1994). Retinol-binding protein in the baboon (Papio anubis) uterus: immunohistochemical characterization and gene expression. Biol. Reprod. 50, 1207–1215.
CrossRef | PubMed | CAS |

Fischer B., and Beier H. M. (1986). Uterine environment in early pregnancy. In ‘Embryo Mortality in the Cow’. (Eds J. M. Sreenan and M. G. Diskin.) pp. 93–108. (Martinus Nijhoff: Dordrecht.)

Gabler, C. , Killian, G. J. , and Einspanier, R. (2001). Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle. Reproduction 122, 121–130.
CrossRef | PubMed | CAS |

Garrett, J. E. , Geisert, R. D. , Zavy, M. T. , and Morgan, G. L. (1988). Evidence for maternal regulation of early conceptus growth and development in beef cattle. J. Reprod. Fertil. 84, 437–446.
CrossRef | PubMed | CAS |

Geisert, R. D. , Morgan, G. L. , Short, E. C., Jr , and Zavy, M. T. (1992). Endocrine events associated with endometrial function and conceptus development in cattle. Reprod. Fertil. Dev. 4, 301–305.
CrossRef | PubMed | CAS |

Gygi, S. P. , Rochon, Y. , Franza, B. R. , and Aebersold, R. (1999). Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720–1730.
PubMed | |  CAS |

Hack, C. J. (2004). Integrated transcriptome and proteome data: the challenges ahead. Brief. Funct. Genomic. Proteomic. 3, 212–219.
CrossRef | CAS | PubMed |

Haliloglu, S. , Baspinar, N. , Serpek, B. , Erdem, H. , and Bulut, Z. (2002). Vitamin A and beta-carotene levels in plasma, corpus luteum and follicular fluid of cyclic and pregnant cattle. Reprod. Domest. Anim. 37, 96–99.
CrossRef | PubMed | CAS |

Harney, J. P. , Ott, T. L. , Geisert, R. D. , and Bazer, F. W. (1993). Retinol-binding protein gene expression in cyclic and pregnant endometrium of pigs, sheep, and cattle. Biol. Reprod. 49, 1066–1073.
CrossRef | PubMed | CAS |

Hidalgo, C. , Diez, C. , Duque, P. , Prendes, J. M. , and Rodriguez, A. , et al. (2005). Oocytes recovered from cows treated with retinol become unviable as blastocysts produced in vitro. Reproduction 129, 411–421.
CrossRef | PubMed | CAS |

Hurley, W. L. , and Doane, R. M. (1989). Recent developments in the roles of vitamins and minerals in reproduction. J. Dairy Sci. 72, 784–804.
CrossRef | CAS | PubMed |

Jensen, S. K. , Johannsen, A. K. , and Hermansen, J. E. (1999). Quantitative secretion and maximal secretion capacity of retinol, beta-carotene and alpha-tocopherol into cows’ milk. J. Dairy Res. 66, 511–522.
CrossRef | PubMed | CAS |

Johnston, L. A. , and Chew, B. P. (1984). Peripartum changes of plasma and milk vitamin A and beta-carotene among dairy cows with or without mastitis. J. Dairy Sci. 67, 1832–1840.
CrossRef | PubMed | CAS |

Jukola, E. , Hakkarainen, J. , Saloniemi, H. , and Sankari, S. (1996). Blood selenium, vitamin E, vitamin A, and beta-carotene concentrations and udder health, fertility treatments, and fertility. J. Dairy Sci. 79, 838–845.
CrossRef | PubMed | CAS |

Kalter, H. , and Warkany, J. (1959). Experimental production of congenital maiformations in mammals by metabolic procedure. Physiol. Rev. 39, 69–115.
PubMed | |  CAS |

Kindahl, H. , Edqvist, L.-E. , Grandstrom, E. , and Bane, A. (1976). The release of prostaglandin F2α as reflected by 15-keto 13, 14-dihydroprostaglandin F2α in the peripheral circulation during normal luteolysis in heifers. Prostaglandins 11, 871–878.
CrossRef | PubMed | CAS |

Lindberg, L. A. , Sinkkonen, H. , Poso, A. R. , Tesfa, A. T. , and Schroder, J. (1999). Production of monoclonal antibodies and enzyme immunoassay to bovine retinol-binding protein and determination of retinol-binding protein serum levels and retinol concentrations in serum and liver in dairy cows before and after parturition. Res. Vet. Sci. 66, 259–263.
CrossRef | PubMed | CAS |

Liu, K. H. , and Godkin, J. D. (1992). Characterization and immunolocalization of bovine uterine retinol-binding protein. Biol. Reprod. 47, 1099–1104.
CrossRef | PubMed | CAS |

Liu, K. H. , Baumbach, G. A. , Gillevet, P. M. , and Godkin, J. D. (1990). Purification and characterization of bovine placental retinol-binding protein. Endocrinology 127, 2696–2704.
CrossRef | PubMed | CAS |

Livingston, T. , Eberhardt, D. , Edwards, J. L. , and Godkin, J. (2004). Retinol improves bovine embryonic development in vitro. Reprod. Biol. Endocrinol. 2, 83.
CrossRef | PubMed |

MacKenzie, S. H. , Roberts, M. P. , Liu, K. H. , Dore, J. J. , and Godkin, J. D. (1997). Bovine endometrial retinol-binding protein secretion, messenger ribonucleic acid expression, and cellular localization during the estrous cycle and early pregnancy. Biol. Reprod. 57, 1445–1450.
CrossRef | PubMed | CAS |

McDowell, K. J. , Adams, M. H. , Franklin, K. M. , and Baker, C. B. (1995). Changes in equine endometrial retinol-binding protein RNA during the estrous cycle and early pregnancy and with exogenous steroids. Biol. Reprod. 52, 438–443.
CrossRef | PubMed | CAS |

McNeill, R. E. , Diskin, M. G. , Sreenan, J. M. , and Morris, D. G. (2006a). Associations between milk progesterone concentration on different days and with embryo survival during the early luteal phase in dairy cows. Theriogenology 65, 1435–1441.
CrossRef | PubMed | CAS |

McNeill, R. E. , Sreenan, J. M. , Diskin, M. G. , Cairns, M. T. , Fitzpatrick, R. , Smith, T. J. , and Morris, D. G. (2006b). Effect of systemic progesterone concentration on the expression of progesterone-responsive genes in the bovine endometrium during the early luteal phase. Reprod. Fertil. Dev. 18, 573–583.
CrossRef | PubMed | CAS |

Milne, D. B. , and Botnen, J. (1986). Retinol, alpha-tocopherol, lycopene, and alpha- and beta-carotene simultaneously determined in plasma by isocratic liquid chromatography. Clin. Chem. 32, 874–876.
PubMed | |  CAS |

Miyamoto, T. , Katoh, N. , Motoi, Y. , Ohashi, T. , Nagasawa, S. , and Shimbayashi, K. (1989). Retinol transport system in cattle and purification of retinol-binding protein from bovine serum. Nippon Juigaku Zasshi 51, 408–415.
PubMed | |  CAS |

Miyamoto, Y. , Sharzynski, D. J. , and Okuda, K. (2000). Is tumor necrosis factor alpha a trigger for the initiation of endometrial prostaglandin F2-alpha release at luteolysis in cattle. Biol. Reprod. 62, 1109–1115.
CrossRef | PubMed | CAS |

Morris, D. G. , and Diskin, M. G. (2008). Effect of progesterone on embryo survival. Animal 2, 1112–1119.
CrossRef | CAS |

Murray, F. A., Jr , Bazer, F. W. , Wallace, H. D. , and Warnick, A. C. (1972). Quantitative and qualitative variation in the secretion of protein by the porcine uterus during the estrous cycle. Biol. Reprod. 7, 314–320.
PubMed | |  CAS |

Newcomer, M. E. , and Ong, D. E. (2000). Plasma retinol binding protein: structure and function of the prototypic lipocalin. Biochim. Biophys. Acta 1482, 57–64.
PubMed | |  CAS |

Parkinson, T. J. , and Lamming, G. E. (1990). Interrelationship between progesterone, 13,14-dihydro-15-keto PGF-2alpha (PGFM) and LH in cyclic and early pregnant cows. J. Reprod. Fertil. 90, 221–233.
CrossRef | PubMed | CAS |

Pope, W. F. , Maurer, R. R. , and Stormshak, F. (1982). Distribution of progesterone in the uterus, broad ligament, and uterine arteries of beef cows. Anat. Rec. 203, 245–249.
CrossRef | PubMed | CAS |

Ross, A. C. (1991). Vitamin A: current understanding of the mechanisms of action. Nutr. Today 26, 6–12.
CrossRef |

Shaw, D. W. , Farin, P. W. , Washburn, S. P. , and Britt, J. H. (1995). Effect of retinol palmitate on ovulation rate and embryo quality in superovulated cattle. Theriogenology 44, 51–58.
CrossRef | CAS |

Signorella, A. P. , and Hymer, W. C. (1984). An enzyme-linked immunosorbent assay for rat prolactin. Anal. Biochem. 136, 372–381.
CrossRef | PubMed | CAS |

Sreenan J. M., Diskin M. G., and Morris D. G. (2001). Embryo survival rate in cattle: a major limitation to the achievement of high fertility. In ‘Fertility in the High Producing Dairy Cow, Vol. 1. BSAS Occasional Publication No. 1’. (Ed. M. G. Diskin.) pp. 93–104. (British Society of Animal Science: Penicuik.)

Starbuck G. R., Darwash A. O., Mann G. E., and Lamming G. E. (2001). The detection and treatment of post insemination progesterone insufficiency in dairy cows. In ‘Fertility in the High Producing Dairy Cow, Vol. 2. BSAS Occasional Publication No. 2’. (Ed. M. G. Diskin.) pp. 447–450. (British Society of Animal Science: Penicuik.)

Stronge, A. J. , Sreenan, J. M. , Diskin, M. G. , Mee, J. F. , Kenny, D. A. , and Morris, D. G. (2005). Post-insemination milk progesterone concentration and embryo survival in dairy cows. Theriogenology 64, 1212–1224.
CrossRef | PubMed | CAS |

Thomas, P. G. A. , Leslie, M. V. , and Hansen, P. J. (1992). Retinol-binding protein is produced by the bovine endometrium and accumulates in a progesterone-dependent manner. Anim. Reprod. Sci. 27, 55–66.
CrossRef | CAS |

Trout, W. E. , Hall, J. A. , Stallings-Mann, M. L. , Galvin, J. M. , Anthony, R. V. , and Roberts, R. M. (1992). Steroid regulation of the synthesis and secretion of retinol-binding protein by the uterus of the pig. Endocrinology 130, 2557–2564.
CrossRef | PubMed | CAS |

Vizcarra, J. A. , Wettemann, R. P. , Braden, T. D. , Turzillo, A. M. , and Nett, T. M. (1997). Effect of gonadotropin-releasing hormone (GnRH) pulse frequency on serum and pituitary concentrations of luteinizing hormone and follicle-stimulating hormone, GnRH receptors, and messenger ribonucleic acid for gonadotropin subunits in cows. Endocrinology 138, 594–601.
CrossRef | PubMed | CAS |

Waters, K. M. , Pounds, J. G. , and Thrall, B. D. (2006). Data merging for integrated microarray and proteomic analysis. Brief. Funct. Genomic. Proteomic. 5, 261–272.
CrossRef | CAS | PubMed |

Wijayagunawardane, M. P. , Cerbito, W. A. , Miyamoto, A. , Acosta, T. J. , Takagi, M. , Miyazawa, K. , and Sato, K. (1996). Oviductal progesterone concentration and its spatial distribution in cyclic and early pregnant cows. Theriogenology 46, 1149–1158.
CrossRef | PubMed | CAS |

Wolf, G. (1984). Multiple functions of vitamin A. Physiol. Rev. 64, 873–937.
PubMed | |  CAS |

Zile, M. H. (1998). Vitamin A and embryonic development: an overview. J. Nutr. 128, 455S–458S.
PubMed | |  CAS |



Rent Article (via Deepdyve) Export Citation Cited By (11)