Insulin-like growth factor and insulin-like growth factor-binding proteins in the bovine uterus throughout the oestrous cycle
Lisa M. Costello A B C , Padraic O’Boyle A , Michael G. Diskin A , Ailish C. Hynes B and Dermot G. Morris A D
+ Author Affiliations
- Author Affiliations
A Animal and Bioscience Research Department, Animal & Grassland Research and Innovation Centre, Teagasc, Mellows Campus, Athenry, Co. Galway, Ireland.
B Department of Physiology, National University of Ireland, Galway, University Road, Co. Galway, Ireland.
C Present address: Abbott Ireland Diagnostic Division, Finisklin Industrial Estate, Sligo, Co. Sligo, Ireland.
D Corresponding author. Email: dermot.morris@teagasc.ie
Reproduction, Fertility and Development 26(4) 599-608 https://doi.org/10.1071/RD13105
Submitted: 23 August 2012 Accepted: 30 March 2013 Published: 23 April 2013
Abstract
The aims of the present study were to assess several components of the insulin-like growth factor (IGF) system in bovine uterine flushings across different days of the oestrous cycle and to examine the relationship between the IGF system and systemic progesterone concentrations. Uterine flushings and plasma were collected from cows on Days 3, 7, 11 and 15 of the oestrous cycle. The IGF-1 concentration was more than 5-fold higher in the uterus compared with plasma on Days 7 and 11 of the cycle, with values similar on Days 3 and 15. Similarly, uterine concentrations of IGF-binding protein (IGFBP)-2 and IGFBP-3 were up to 10- and 4-fold higher than in plasma, respectively, suggesting synthesis and/or transportation of the IGFBPs into the uterus. In addition, concentrations of IGFBP-2 and IGFBP-3 were higher in the uterine horns, ipsilateral to the corpus luteum, on Day 15. This difference could indicate a local controlling mechanism with progesterone possibly playing a role in regulating the concentration of IGFBPs between the uterine horns. There was no significant relationship between systemic progesterone concentrations and IGFBP concentrations on Day 7 of the oestrous cycle. The present study shows that uterine concentrations of IGFBPs are cycle stage specific and also suggests IGF-dependent and -independent functions for IGFBPs during a time of major change in the developing embryo.
Additional keywords: immunoblotting, ligand blot, plasma, progesterone.
References
Andress, D. L. (1998). Insulin-like growth factor-binding protein-5 (IGFBP-5) stimulates phosphorylation of the IGFBP-5 receptor. Am. J. Physiol. 274, E744–E750.| 1:CAS:528:DyaK1cXislyis74%3D&md5=748426513f5e67822435ff5db64bb579CAS | 9575837PubMed |
Badinga, L., Song, S., Simmen, R. C., Clarke, J. B., Clemmons, D. R., and Simmen, F. A. (1999). Complex mediation of uterine endometrial epithelial cell growth by insulin-like growth factor-II (IGF-II) and IGF-binding protein-2. J. Mol. Endocrinol. 23, 277–285.
| Complex mediation of uterine endometrial epithelial cell growth by insulin-like growth factor-II (IGF-II) and IGF-binding protein-2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks1WktQ%3D%3D&md5=e2866c92b7ffcac04130a11084f2259cCAS | 10601973PubMed |
Bilby, T. R., Guzeloglu, A., Kamimura, S., Pancarci, S. M., Michel, F., Head, H. H., and Thatcher, W. W. (2004). Pregnancy and bovine somatotropin in nonlactating dairy cows: I. Ovarian, conceptus, and insulin-like growth factor system responses. J. Dairy Sci. 87, 3256–3267.
| Pregnancy and bovine somatotropin in nonlactating dairy cows: I. Ovarian, conceptus, and insulin-like growth factor system responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotFyktLk%3D&md5=649f33c41de64cd04a2899261cac4067CAS | 15377605PubMed |
Cann, C. H., Fairclough, R. J., Browne, C. A., and Gow, C. B. (1998). Uterine luminal content of insulin-like growth factor (IGF)-I and endometrial expression of mRNA encoding IGF-binding proteins 1 and 2 during the oestrous cycle and early pregnancy in the ewe. Reprod. Fertil. Dev. 10, 155–163.
| Uterine luminal content of insulin-like growth factor (IGF)-I and endometrial expression of mRNA encoding IGF-binding proteins 1 and 2 during the oestrous cycle and early pregnancy in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFCltr8%3D&md5=747da37ed0d2414c650cb44ce6a675ddCAS | 9801267PubMed |
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 progesteroneand 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 progesteroneand RBP on Day 7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1aktLjI&md5=0b7e167b65a0d996f82117c78d30735fCAS | 20883645PubMed |
Dunn, J. D., Johnson, B. J., Kayser, J. P., Waylan, A. T., Sissom, E. K., and Drouillard, J. S. (2003). Effects of flax supplementation and a combined trenbolone acetate and estradiol implant on circulating insulin-like growth factor-I and muscle insulin like growth factor-I messanger RNA levels in beef cattle. J. Anim. Sci. 81, 3028–3034.
| 1:CAS:528:DC%2BD3sXpslSjsrs%3D&md5=ebe08f7b92e2503b7d007afe91cee493CAS | 14677858PubMed |
Geisert, R. D., Lee, C. Y., Simmen, F. A., Zavy, M. T., Fliss, A. E., Bazer, F. W., and Simmen, R. C. (1991). Expression of messenger RNAs encoding insulin-like growth factor-I, -II, and insulin-like growth factor binding protein-2 in bovine endometrium during the estrous cycle and early pregnancy. Biol. Reprod. 45, 975–983.
| Expression of messenger RNAs encoding insulin-like growth factor-I, -II, and insulin-like growth factor binding protein-2 in bovine endometrium during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XjsFSlsg%3D%3D&md5=fdc03dd887812df0d6afd7be50507ad0CAS | 1725270PubMed |
Giudice, L. C., Milkowski, D. A., Fielder, P. J., and Irwin, J. C. (1991). Characterization of the steroid-dependence of insulin-like growth factor-binding protein-2 synthesis and mRNA expression in cultured human endometrial stromal cells. Hum. Reprod. 6, 632–640.
| 1:CAS:528:DyaK3MXlvF2lsL0%3D&md5=539627a4b067efa674aa8ff195111287CAS | 1719019PubMed |
Giudice, L. C., Dsupin, B. A., and Irwin, J. C. (1992). Steroid and peptide regulation of insulin-like growth factor-binding proteins secreted by human endometrial stromal cells is dependent on stromal differentiation. J. Clin. Endocrinol. Metab. 75, 1235–1241.
| Steroid and peptide regulation of insulin-like growth factor-binding proteins secreted by human endometrial stromal cells is dependent on stromal differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs12hsg%3D%3D&md5=531d5ead160079452e9db9f961ab547fCAS | 1385468PubMed |
Herrler, A., Lucas-Hahn, A., and Niemann, H. (1992). Effects of insulin-like growth factor-I on in vitro production of bovine embryos. Theriogenology 37, 1213–1224.
| Effects of insulin-like growth factor-I on in vitro production of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1Ckurw%3D&md5=710c7e6a4386c9696c154779ab99083eCAS |
Hettmer, S., Dannecker, L., Foell, J., Elmlinger, M. W., and Dannecker, G. E. (2005). Effects of insulin-like growth factors and insulin-like growth factor binding protein-2 on the in vitro proliferation of peripheral blood mononuclear cells. Hum. Immunol. 66, 95–103.
| Effects of insulin-like growth factors and insulin-like growth factor binding protein-2 on the in vitro proliferation of peripheral blood mononuclear cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2ntbo%3D&md5=e0a95f41cec8c59dc1ab54b8c2b3ced1CAS | 15694994PubMed |
Hossenlopp, P., Seurin, D., Segovia-Quinson, B., Hardouin, S., and Binoux, M. (1986). Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal. Biochem. 154, 138–143.
| Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkslGgsbc%3D&md5=079a90e4660016e00380534a4f2a4c4bCAS | 2422981PubMed |
Hwa, V., Oh, Y., and Rosenfeld, R. G. (1999). The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20, 761–787.
| The insulin-like growth factor-binding protein (IGFBP) superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntV2itA%3D%3D&md5=ae760b190c29ac43f80580f1852f7cf7CAS | 10605625PubMed |
Jones, J. I., and Clemmons, D. R. (1995). Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3–34.
| 1:CAS:528:DyaK2MXltlKhu7g%3D&md5=92f4c6e9e525b8da56f26db688ead668CAS | 7758431PubMed |
Jones, J. I., Gockerman, A., Busby, W. H., Camacho-Hubner, C., and Clemmons, D. R. (1993a). Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I. J. Cell Biol. 121, 679–687.
| Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitVKjtro%3D&md5=f560895e05338def6e195bce8c25b371CAS | 7683690PubMed |
Jones, J. I., Gockerman, A., Busby, W. H., Wright, G., and Clemmons, D. R. (1993b). Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc. Natl Acad. Sci. USA 90, 10 553–10 557.
| Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXisVehsw%3D%3D&md5=597b7f534daf75e9bfc2b190f796e8d0CAS |
Kawashima, C., Kida, K., Hayashi, K. G., Amaya Montoya, C., Kaneko, E., Matsunaga, N., Shimizu, T., Matsui, M., Miyake, Y., Schams, D., and Miyamoto, A. (2007). Changes in plasma metabolic hormone concentrations during the ovarian cycles of Japanese black and holstein cattle. J. Reprod. Dev. 53, 247–254.
| Changes in plasma metabolic hormone concentrations during the ovarian cycles of Japanese black and holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslOjsL0%3D&md5=45cc38c143fe0c5e3385a65aed3b60b3CAS | 17132912PubMed |
Kaye, P. L., Bell, K. L., Beebe, L. F., Dunglison, G. F., Gardner, H. G., and Harvey, M. B. (1992). Insulin and the insulin-like growth factors (IGFs) in preimplantation development. Reprod. Fertil. Dev. 4, 373–386.
| Insulin and the insulin-like growth factors (IGFs) in preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsVersA%3D%3D&md5=02c2b36e1a07d7acab7dc5be03a352a6CAS | 1461989PubMed |
Keller, M. L., Roberts, A. J., and Seidel, G. E. (1998). Characterization of insulin-like growth factor-binding proteins in the uterus and conceptus during early conceptus elongation in cattle. Biol. Reprod. 59, 632–642.
| Characterization of insulin-like growth factor-binding proteins in the uterus and conceptus during early conceptus elongation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVSrur8%3D&md5=d149b5d35728058e02071a9a8fc2662fCAS | 9716564PubMed |
Kirby, C. J., Thatcher, W. W., Collier, R. J., Simmen, F. A., and Lucy, M. C. (1996). Effects of growth hormone and pregnancy on expression of growth hormone receptor, insulin-like growth factor-I, and insulin-like growth factor binding protein-2 and -3 genes in bovine uterus, ovary, and oviduct. Biol. Reprod. 55, 996–1002.
| Effects of growth hormone and pregnancy on expression of growth hormone receptor, insulin-like growth factor-I, and insulin-like growth factor binding protein-2 and -3 genes in bovine uterus, ovary, and oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlamurY%3D&md5=94ffd36bcaff5341ac3a3a23d27b47f7CAS | 8902209PubMed |
Klauke, M., and Hoffman, B. (1992). Progesterone and estrogen receptors in the myometrium of the cow during the estrous cycle and pregnancy and of the sheep at the time of parturition. Anim. Reprod. Sci. 29, 195–203.
| Progesterone and estrogen receptors in the myometrium of the cow during the estrous cycle and pregnancy and of the sheep at the time of parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXntlygtg%3D%3D&md5=93238a3c21def71c00ef0ace6b233fc7CAS |
Liu, H. C., He, Z. Y., Mele, C., Damario, M., Davis, O., and Rosenwaks, Z. (1997). Hormonal regulation of expression of messenger RNA encoding insulin-like growth factor binding proteins in human endometrial stromal cells cultured in vitro. Mol. Hum. Reprod. 3, 21–26.
| Hormonal regulation of expression of messenger RNA encoding insulin-like growth factor binding proteins in human endometrial stromal cells cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhvVeisLk%3D&md5=3afa2bbaece72b53ecce7ca0f07f52c7CAS | 9239705PubMed |
Matsui, M., Takahashi, Y., Hishinuma, M., and Kanagawa, H. (1995). Insulin and insulin-like growth factor-I (IGF-I) stimulate the development of bovine embryos fertilized in vitro. J. Vet. Med. Sci. 57, 1109–1111.
| Insulin and insulin-like growth factor-I (IGF-I) stimulate the development of bovine embryos fertilized in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtFyqt78%3D&md5=dec89c1e28b609742fa8fbf570995e0aCAS | 8720059PubMed |
McCarthy, S. D., Roche, J. F., and Forde, N. (2012). Temporal changes in endometrial gene expression and protein localization of members of the IGF family in cattle: effects of progesterone and pregnancy. Physiol. Genomics 44, 130–140.
| Temporal changes in endometrial gene expression and protein localization of members of the IGF family in cattle: effects of progesterone and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlslOgsrk%3D&md5=affc02fbb23e945c61c8e0fecf70b2f4CAS | 22085906PubMed |
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=8d0ee5cd8dd3237f0acd36b85730eccaCAS | 16836964PubMed |
Mohan, S., Baylink, D. J., and Pettis, J. L. (1996). Insulin-like growth factor (IGF)-binding proteins in serum–do they have additional roles besides modulating the endocrine IGF actions? J. Clin. Endocrinol. Metab. 81, 3817–3820.
| Insulin-like growth factor (IGF)-binding proteins in serum–do they have additional roles besides modulating the endocrine IGF actions?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntVCkurY%3D&md5=750058c7e011b2d8c636c0c1b32dba8eCAS | 8923818PubMed |
Molnar, P., and Murphy, L. J. (1994). Effects of oestrogen on rat uterine expression of insulin-like growth factor-binding proteins. J. Mol. Endocrinol. 13, 59–67.
| Effects of oestrogen on rat uterine expression of insulin-like growth factor-binding proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsV2gt7w%3D&md5=fd00767abce2cd83d77dfe75ba04aa5dCAS | 7528021PubMed |
Moore, M. G., Wetterau, L. A., Francis, M. J., Peehl, D. M., and Cohen, P. (2003). Novel stimulatory role for insulin-like growth factor binding protein-2 in prostate cancer cells. Int. J. Cancer 105, 14–19.
| Novel stimulatory role for insulin-like growth factor binding protein-2 in prostate cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVWku7c%3D&md5=f0c3d1939f52166d0053e44f2ff4955dCAS | 12672024PubMed |
Moyano, P., and Rotwein, P. (2004). Mini-review: estrogen action in the uterus and insulin-like growth factor-I. Growth Horm. IGF Res. 14, 431–435.
| Mini-review: estrogen action in the uterus and insulin-like growth factor-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFOgur0%3D&md5=43a67a4fd59c91099807f68cd749f8a7CAS | 15519250PubMed |
Nicholas, B., Scougall, R. K., Armstrong, D. G., and Webb, R. (2002). Changes in insulin-like growth factor binding protein (IGFBP) isoforms during bovine follicular development. Reproduction 124, 439–446.
| Changes in insulin-like growth factor binding protein (IGFBP) isoforms during bovine follicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2htL8%3D&md5=fd5362e99cee348a2f30139be85f9a72CAS | 12201817PubMed |
Oh, Y., Muller, H. L., Pham, H., and Rosenfeld, R. G. (1993). Demonstration of receptors for insulin-like growth factor binding protein-3 on Hs578T human breast cancer cells. J. Biol. Chem. 268, 26 045–26 048.
| 1:CAS:528:DyaK3sXmsVKqurk%3D&md5=e83fbf6c8c4f887d12a9b41457d850bbCAS |
Palma, G. A., Muller, M., and Brem, G. (1997). Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro. J. Reprod. Fertil. 110, 347–353.
| Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKrsLw%3D&md5=958271037866ccf13386bb7795e49cfcCAS | 9306989PubMed |
Pershing, R. A., Lucy, M. C., Thatcher, W. W., and Badinga, L. (2002). Effects of BST on oviductal and uterine genes encoding components of the IGF system in lactating dairy cows. J. Dairy Sci. 85, 3260–3267.
| Effects of BST on oviductal and uterine genes encoding components of the IGF system in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1aqsA%3D%3D&md5=ac68a2959b8d925ae49cbc96ce23b6fbCAS | 12512599PubMed |
Pershing, R. A., Dinges, A. C., Thatcher, W. W., and Badinga, L. (2003). Plasma and uterine insulin-like growth factor-I (IGF-I) and IGF-binding proteins in lactating dairy cows treated with bovine somatotropin. J. Anim. Vet. Adv. 2, 67–73.
Peterson, A. J., Ledgard, A. M., and Hodgkinson, S. C. (1998a). Oestrogen regulation of insulin-like growth factor binding protein-3 (IGFBP-3) and expression of IGFBP-3 messenger RNA in the ovine endometrium. Reprod. Fertil. Dev. 10, 241–247.
| Oestrogen regulation of insulin-like growth factor binding protein-3 (IGFBP-3) and expression of IGFBP-3 messenger RNA in the ovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFSjsrk%3D&md5=e46c3722a22c32265ed8bb83adf3f18dCAS | 11596870PubMed |
Peterson, A. J., Ledgard, A. M., and Hodgkinson, S. C. (1998b). The proteolysis of insulin-like growth factor binding proteins in ovine uterine luminal fluid. Reprod. Fertil. Dev. 10, 309–314.
| The proteolysis of insulin-like growth factor binding proteins in ovine uterine luminal fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVKgtLY%3D&md5=3255a530848bae334fba932dcac37a89CAS | 10355682PubMed |
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. 249, 245–250.
| Distribution of progesterone in the uterus, broad ligament, and uterine arteries of beef cows.Crossref | GoogleScholarGoogle Scholar |
Pushpakumara, P. G., Robinson, R. S., Demmers, K. J., Mann, G. E., Sinclair, K. D., Webb, R., and Wathes, D. C. (2002). Expression of the insulin-like growth factor (IGF) system in the bovine oviduct at oestrus and during early pregnancy. Reproduction 123, 859–868.
| Expression of the insulin-like growth factor (IGF) system in the bovine oviduct at oestrus and during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVCiu7c%3D&md5=56c45ac8fafc4dfbdfb40ceaa59bd850CAS | 12052240PubMed |
Rajaram, S., Baylink, D. J., and Mohan, S. (1997). Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr. Rev. 18, 801–831.
| Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFeq&md5=f35e59ce499edee8e2fcfffc312ff6c7CAS | 9408744PubMed |
Rauschnabel, U., Koscielniak, E., Ranke, M. B., Schuett, B., and Elmlinger, M. W. (1999). RGD specific binding of IGFBP-2 to alpha 5 beta 1 integrin of Ewing sarcoma cells. Growth Horm. IGF Res. 9, 369–374.
Rechler, M. M. 1993. Insulin-like growth factor binding proteins. In ‘Advances in Research and Applications. Vitamins and Hormones’. (Eds G. D. Aurbach and D. B. McCormick.) pp. 1–114. (Academic Press: London.)
Robinson, R. S., Mann, G. E., Gadd, T. S., Lamming, G. E., and Wathes, D. C. (2000). The expression of the IGF system in the bovine uterus throughout the oestrous cycle and early pregnancy. J. Endocrinol. 165, 231–243.
| The expression of the IGF system in the bovine uterus throughout the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFegtr8%3D&md5=90f8027535b881639386ac1f1f4dddd7CAS | 10810287PubMed |
Simmen, F. A., Simmen, R. C., Geisert, R. D., Martinat-Botte, F., Bazer, F. W., and Terqui, M. (1992). Differential expression, during the estrous cycle and pre- and postimplantation conceptus development, of messenger ribonucleic acids encoding components of the pig uterine insulin-like growth factor system. Endocrinology 130, 1547–1556.
| Differential expression, during the estrous cycle and pre- and postimplantation conceptus development, of messenger ribonucleic acids encoding components of the pig uterine insulin-like growth factor system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvVymu78%3D&md5=34abf7a9ced8cba7b124a307d2f16f02CAS | 1537304PubMed |
Tseng, L., Gao, J., Mazella, J., Zhu, H. H., and Lane, B. (1997). Differentiation-dependent and cell-specific regulation of the hIGFBP-1 gene in human endometrium. Ann. N. Y. Acad. Sci. 828, 27–37.
| Differentiation-dependent and cell-specific regulation of the hIGFBP-1 gene in human endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvFyks7s%3D&md5=2403cccf5becf0dc12d64696c36f66d3CAS | 9329821PubMed |
Vizcarra, J. A., Wettemann, R. P., Braden, T. D., Turzillo, A. M., and Nett, T. M. (1997). Effect of gonadotrophin-releasing hormone (GnRH) pulse frequency on serum and pituitary concentrations of luteinizing hormone and follicle-stimulating hormone, GnRH receptors and messenger ribonucleic acid for gonadotrophin subunits in cows. Endocrinology 138, 594–601.
| Effect of gonadotrophin-releasing hormone (GnRH) pulse frequency on serum and pituitary concentrations of luteinizing hormone and follicle-stimulating hormone, GnRH receptors and messenger ribonucleic acid for gonadotrophin subunits in cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ls1Kjsw%3D%3D&md5=3ea003b9628d4e90894b824613f29f29CAS | 9002991PubMed |
Wathes, D. C., Reynolds, T. S., Robinson, R. S., and Stevenson, K. R. (1998). Role of the insulin-like growth factor system in uterine function and placental development in ruminants. J. Dairy Sci. 81, 1778–1789.
| Role of the insulin-like growth factor system in uterine function and placental development in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvVyqs78%3D&md5=4e664a95de58d4794374d33d0e905473CAS | 9684184PubMed |
Watson, A. J., Hogan, A., Hahnel, A., Wiemer, K. E., and Schultz, G. A. (1992a). Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol. Reprod. Dev. 31, 87–95.
| Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvVymur8%3D&md5=0e933d128221fc503955219427766c98CAS | 1318055PubMed |
Watson, E. D., Skolnik, S. B., and Zanecosky, H. G. (1992b). Progesterone and estrogen receptor distribution in the endometrium of the mare. Theriogenology 38, 575–580.
| Progesterone and estrogen receptor distribution in the endometrium of the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1Cqsw%3D%3D&md5=632190f702cc8f8930c79b7b630feaf8CAS | 16727160PubMed |
Yaseen, M. A., Wrenzycki, C., Herrmann, D., Carnwath, J. W., and Niemann, H. (2001). Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction 122, 601–610.
| Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFGlur8%3D&md5=00f1a05be647a1e1cf221b18df24563cCAS | 11570968PubMed |
