Alterations in systemic concentrations of progesterone during the early luteal phase affect RBP4 expression in the bovine uterus
Michael P. Mullen A B E , Niamh Forde B , Mervyn H. Parr A B , Michael G. Diskin A , Dermot G. Morris A , Jarlath E. Nally B , Alexander C. O. Evans C D and Mark A. Crowe B D
+ Author Affiliations
- Author Affiliations
A Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc, Mellows Campus, Athenry, Co. Galway, Ireland.
B UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland.
C UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.
D UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin 4, Ireland.
E Corresponding author. Email: michael.mullen@teagasc.ie
Reproduction, Fertility and Development 24(5) 715-722 https://doi.org/10.1071/RD11246
Submitted: 27 September 2011 Accepted: 3 November 2011 Published: 6 December 2011
Abstract
Systemic progesterone affects the timing and duration of uterine endometrial gene and protein expression and has significant effects on conceptus development. The objective of the present study was to examine how changes in progesterone concentrations during the early luteal phase affect retinol-binding protein (RBP4) mRNA and protein concentrations in the uterus. Endometrial tissue and uterine flushings were recovered on Days 7 and 13 of the oestrous cycle in heifers with high, normal and low progesterone concentrations. RBP4 mRNA and protein concentrations were higher (P < 0.05) on Day 13 compared with Day 7 in heifers with high and control progesterone concentrations. However, there was no difference in RBP4 protein concentrations between Days 7 and 13 in heifers with low progesterone (P > 0.05). On Day 7, although heifers with low progesterone had lower RBP4 mRNA expression compared with controls (P < 0.05) there was no difference in protein concentrations between treatment groups. On Day 13, RBP4 mRNA was 2-fold higher (P < 0.001) in heifers with high and control progesterone compared with their low-progesterone counterparts and RBP4 protein concentrations were over 2-fold higher (P < 0.001) in heifers with high compared to low progesterone. In conclusion, progesterone modulates uterine RBP4 mRNA and protein abundance in a time- and concentration-dependent manner.
Additional keywords: embryo loss, endometrium, fertility, histotroph.
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.| Progesterone-induced secretion of a retinol-binding protein in the pig uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktlGrtLw%3D&md5=d0122463f7be7cc0d236a58fa7d8e2e6CAS | 7194913PubMed |
Bazer, F. W., Vallet, J. L., Ashworth, C. J., Anthony, R. V., and Roberts, R. M. (1987). The role of ovine conceptus secretory proteins in the establishment of pregnancy. Adv. Exp. Med. Biol. 230, 221–235.
| 1:CAS:528:DyaL1MXit12ju7o%3D&md5=bafb85307c53162ecbef9c9fc44c3530CAS | 3454121PubMed |
Beltman, M. E., Roche, J. F., Lonergan, P., Forde, N., and Crowe, M. A. (2009). Evaluation of models to induce low progesterone during the early luteal phase in cattle. Theriogenology 72, 986–992.
| Evaluation of models to induce low progesterone during the early luteal phase in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGlsrrP&md5=88f62c6dcef227981aea679437d03581CAS | 19716596PubMed |
Betteridge, K. J., Eaglesome, M. D., Randall, G. C., and Mitchell, D. (1980). Collection, description and transfer of embryos from cattle 10–16 days after oestrus. J. Reprod. Fertil. 59, 205–216.
| Collection, description and transfer of embryos from cattle 10–16 days after oestrus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c3ltFGhsQ%3D%3D&md5=a440ab2d5369a9a23182a775db00d673CAS | 7401037PubMed |
Carter, F., Forde, N., Duffy, P., Wade, M., Fair, T., Crowe, M. A., Evans, A. C. O., Kenny, D. A., Roche, J. F., and Lonergan, P. (2008). Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod. Fertil. Dev. 20, 368–375.
| Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVKksLg%3D&md5=fb0e332b80e7323eedc60036d56ef2c8CAS | 18402756PubMed |
Clemente, M., de La Fuente, J., Fair, T., Al Naib, A., Gutierrez-Adan, A., Roche, J. F., Rizos, D., and Lonergan, P. (2009). Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction 138, 507–517.
| Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrvL&md5=c2b93accf694e764a9eab6c4efb1a01cCAS | 19556439PubMed |
Costello, L. M., O'Boyle, P., Godkin, J. D., Diskin, M. G., Hynes, A. C., and Morris, D. G. (2010). Retinol-binding protein (RBP), retinol and beta-carotene in the bovine uterus and plasma during the oestrous cycle and the relationship between systemic progesterone and RBP on Day 7. Reprod. Fertil. Dev. 22, 1198–1205.
| Retinol-binding protein (RBP), retinol and beta-carotene in the bovine uterus and plasma during the oestrous cycle and the relationship between systemic progesterone and RBP on Day 7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1aktLjI&md5=9fa2d86ae56862b1b9c7a5badcd831a9CAS | 20883645PubMed |
Diskin, M. G., Murphy, J. J., and Sreenan, J. M. (2006). Embryo survival in dairy cows managed under pastoral conditions. Anim. Reprod. Sci. 96, 297–311.
| Embryo survival in dairy cows managed under pastoral conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28nitFGgsg%3D%3D&md5=f621fa13f142ae2bc5883fc87ec717b6CAS | 16963203PubMed |
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.
| Retinol administration to superovulated ewes improves in vitro embryonic viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVeit7Y%3D&md5=92ee48c13accf6e9b0717ae280ccf77fCAS | 10330109PubMed |
Faulkner, S., Elia, G., Hillard, M., O'Boyle, P., Dunn, M., and Morris, D. (2011). Immunodepletion of albumin and immunoglobulin G from bovine plasma. Proteomics 11, 2329–2335.
| Immunodepletion of albumin and immunoglobulin G from bovine plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVGns7w%3D&md5=d7a707bf0fd0b0271a3d4fde74667b86CAS | 21538883PubMed |
Flower, D. R. (1996). The lipocalin protein family: structure and function. Biochem. J. 318, 1–14.
| 1:CAS:528:DyaK28XltlKrtLc%3D&md5=de2cc2965de96e073ef02859b803616cCAS | 8761444PubMed |
Forde, N., Carter, F., Fair, T., Crowe, M. A., Evans, A. C. O., Spencer, T. E., Bazer, F. W., McBride, R., Boland, M. P., O’Gaora, P., Lonergan, P., and Roche, J. F. (2009). Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol. Reprod. 81, 784–794.
| Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyhsLbM&md5=d5b87f63f4bfb6dba0d5025dcdce42adCAS | 19553605PubMed |
Forde, N., Spencer, T. E., Bazer, F. W., Song, G., Roche, J. F., and Lonergan, P. (2010). Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol. Genomics 41, 53–62.
| Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlakt7jN&md5=56bdcbecc453981b4ab37f49892ef394CAS | 19996158PubMed |
Forde, N., Beltman, M. E., Duffy, G. B., Duffy, P., Mehta, J. P., O'Gaora, P., Roche, J. F., Lonergan, P., and Crowe, M. A. (2011). Changes in the endometrial transcriptome during the bovine oestrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biol. Reprod. 84, 266–278.
| Changes in the endometrial transcriptome during the bovine oestrous cycle: effect of low circulating progesterone and consequences for conceptus elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVeltr4%3D&md5=f5452608cf2c4895d4fb4fdcc1a16252CAS | 20881316PubMed |
Gray, C. A., Taylor, K. M., Ramsey, W. S., Hill, J. R., Bazer, F. W., Bartol, F. F., and Spencer, T. E. (2001). Endometrial glands are required for preimplantation conceptus elongation and survival. Biol. Reprod. 64, 1608–1613.
| Endometrial glands are required for preimplantation conceptus elongation and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgsbs%3D&md5=05e8407b7cf6158126811d3aed3c6062CAS | 11369585PubMed |
Gray, C. A., Burghardt, R. C., Johnson, G. A., Bazer, F. W., and Spencer, T. E. (2002). Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124, 289–300.
| Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVCitL8%3D&md5=8459ac1020520773b11d7c88fbd1e795CAS | 12141942PubMed |
Gray, C. A., Abbey, C. A., Beremand, P. D., Choi, Y., Farmer, J. L., Adelson, D. L., Thomas, T. L., Bazer, F. W., and Spencer, T. E. (2006). Identification of endometrial genes regulated by early pregnancy, progesterone and interferon tau in the ovine uterus. Biol. Reprod. 74, 383–394.
| Identification of endometrial genes regulated by early pregnancy, progesterone and interferon tau in the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1Kktg%3D%3D&md5=3d1ebd82d6acfd1ed3a5efa2a9f0f5e3CAS | 16251498PubMed |
Lawrence, J. L., Payton, R. R., Godkin, J. D., Saxton, A. M., Schrick, F. N., and Edwards, J. L. (2004). Retinol improves development of bovine oocytes compromised by heat stress during maturation. J. Dairy Sci. 87, 2449–2454.
| Retinol improves development of bovine oocytes compromised by heat stress during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotVyns70%3D&md5=9dc496ee57a52568139bcf127665a5c7CAS | 15328267PubMed |
Liu, K. H., and Godkin, J. D. (1992). Characterization and immunolocalization of bovine uterine retinol-binding protein. Biol. Reprod. 47, 1099–1104.
| Characterization and immunolocalization of bovine uterine retinol-binding protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjs1Kjtg%3D%3D&md5=bbffe23245531b63d959c6af8753ab16CAS | 1493174PubMed |
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.
| Purification and characterization of bovine placental retinol-binding protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlslOguw%3D%3D&md5=441d49d9a1d54db386c37709e0d908f5CAS | 2249622PubMed |
Livingston, T., Eberhardt, D., Edwards, J. L., and Godkin, J. (2004). Retinol improves bovine embryonic development in vitro. Reprod. Biol. Endocrinol. 2, 83.
| Retinol improves bovine embryonic development in vitro.Crossref | GoogleScholarGoogle Scholar | 15613237PubMed |
Mackenzie, S. H., Roberts, M. P., Liu, K. H., Dore, J. J. E., and Godkin, J. D. (1997). Bovine endometrial retinol-binding protein secretion, messenger ribonucleic acid expression and cellular localization during the oestrous cycle and early pregnancy. Biol. Reprod. 57, 1445–1450.
| Bovine endometrial retinol-binding protein secretion, messenger ribonucleic acid expression and cellular localization during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVWrurY%3D&md5=3a585ac7e2818137a33158fd69671aa0CAS | 9408253PubMed |
Mark, M., Ghyselinck, N. B., and Chambon, P. (2006). Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signalling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46, 451–480.
| Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signalling pathway during mouse embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKltbY%3D&md5=b5a0829b9d642394bd6e6a1d3790f0f7CAS | 16402912PubMed |
McNeill, R. E., Sreenan, J. M., Diskin, M. G., Cairns, M. T., Fitzpatrick, R., Smith, T. J., and Morris, D. G. (2006). 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.
| Effect of systemic progesterone concentration on the expression of progesterone-responsive genes in the bovine endometrium during the early luteal phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVWnt7o%3D&md5=171b790ba54582454f766cfe8fb72972CAS | 16836964PubMed |
Northey, D. L., and French, L. R. (1980). Effect of embryo removal and intrauterine infusion of embryonic homogenates on the lifespan of the bovine corpus luteum. J. Anim. Sci. 50, 298–302.
| 1:STN:280:DyaL3c7jslansQ%3D%3D&md5=6206540856470f54e1d2dfaf6beba0baCAS | 7358600PubMed |
Noy, N. (2000). Retinoid-binding proteins: mediators of retinoid action. Biochem. J. 348, 481–495.
| Retinoid-binding proteins: mediators of retinoid action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Smsr8%3D&md5=5df78cc9f28cf8cbdae0a7c10acd60efCAS | 10839978PubMed |
Ross, A. C. (1993). Cellular metabolism and activation of retinoids: roles of cellular retinoid-binding proteins. FASEB J. 7, 317–327.
| 1:CAS:528:DyaK3sXhvVyhtL4%3D&md5=724b67bfd6f6173142b500a9514022d2CAS | 8440409PubMed |
Satterfield, M. C., Gao, H., Li, X., Wu, G., Johnson, G. A., Spencer, T. E., and Bazer, F. W. (2010). Select nutrients and their associated transporters are increased in the ovine uterus following early progesterone administration. Biol. Reprod. 82, 224–231.
| Select nutrients and their associated transporters are increased in the ovine uterus following early progesterone administration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgsrjM&md5=4bf3c24bb8f83ad9d40a692811caf36eCAS | 19696016PubMed |
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.
| Effect of retinol palmitate on ovulation rate and embryo quality in superovulated cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Cjt7o%3D&md5=a1f7c6a95106d5be8f50bf9af30d7352CAS |
Simmons, R. M., Erikson, D. W., Kim, J., Burghardt, R. C., Bazer, F. W., Johnson, G. A., and Spencer, T. E. (2009). Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology 150, 4295–4305.
| Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyrtLfP&md5=63fe7588ab95921680053db39e7ecbb3CAS | 19497977PubMed |
Spencer, T. E., Johnson, G. A., Bazer, F. W., Burghardt, R. C., and Palmarini, M. (2006). Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod. Fertil. Dev. 19, 65–78.
| Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses.Crossref | GoogleScholarGoogle Scholar |
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. BSAS Occasional Publication No. 26 Volume 2’. (Ed. M. G. Diskin) pp. 447–450. (BSAS: Edinburgh, UK.)
Stronge, A. J. H., 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.
| Post-insemination milk progesterone concentration and embryo survival in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsVCgt7o%3D&md5=143645888555a9fed755eaf0856a22edCAS |
Thomas, P. G. A., Leslie, M. V., and Hansen, P. J. (1992). Retinol-binding protein is produced by the bovine endometrium and accumulates in uterine secretions in a progesterone-dependent manner. Anim. Reprod. Sci. 27, 55–66.
| Retinol-binding protein is produced by the bovine endometrium and accumulates in uterine secretions in a progesterone-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xit1yntrw%3D&md5=edaefc0cf028f3f409bd01381c4d5648CAS |
Vallet, J. L., Christenson, R. K., Trout, W. E., and Klemcke, H. G. (1998). Conceptus, progesterone and breed effects on uterine protein secretion in swine. J. Anim. Sci. 76, 2657–2670.
| 1:CAS:528:DyaK1cXntFWhu7Y%3D&md5=ca98de241350a4d520f5630c44b31bdfCAS | 9814907PubMed |
Zile, M. H. (2001). Vitamin A and embryonic development: an overview. J. Nutr. 131, 705–708.
| 1:CAS:528:DC%2BD3MXhvVOhs78%3D&md5=8a4d5a3934b64a203633e482b318ff45CAS | 11238746PubMed |
