Effect of exogenous progesterone on embryo size and ewe uterine gene expression in an ovine ‘dam size’ model of maternal constraint
Lisanne M. Fermin A B , Sarah J. Pain A , Patrick C. H. Morel A , Kristene R. Gedye A , Paul R. Kenyon A and Hugh T. Blair A
+ Author Affiliations
- Author Affiliations
A Institute of Veterinary and Biomedical Sciences, Massey University, Private Bag 11-222, Palmerston North, 4442, New Zealand.
B Corresponding author. Email: l.m.fermin@massey.ac.nz
Reproduction, Fertility and Development 30(5) 766-778 https://doi.org/10.1071/RD17096
Submitted: 10 March 2017 Accepted: 15 October 2017 Published: 21 November 2017
Abstract
Progesterone (P4), acting via its receptor, regulates uterine function and histotroph production, which are crucial to embryo growth. This study aimed to examine exogenous P4 effects on embryo size and differential endometrial gene expression at Day 19 of gestation using a ‘dam size’ sheep model of maternal constraint. Purebred Suffolk (S, genotypically large) embryos were transferred into recipient groups of Cheviot (C, genotypically small) or Suffolk ewes that had, or had not, been pre-treated with P4 from Days 0 to 6 of pregnancy. At Day 19 S embryos were collected from four experimental groups: P4 pretreated S ewes (SP4; n = 5), untreated S ewes (SnP4; n = 15), P4 pretreated C ewes (CP4; n = 7) and untreated C ewes (CnP4; n = 21). Day-19 embryos from CP4 ewes were larger (P < 0.05) than those from CnP4 ewes and similar in size (P > 0.05) to embryos from SnP4 and SP4 ewes. Expression of mucin 1 (MUC1) and prostaglandin-endoperoxide synthase 2 (PTGS2) was upregulated in uterine horns ipsilateral to the corpus luteum from CP4 ewes. Prostaglandin receptor (PGR), MUC1 and PTGS2 expression was upregulated, whilst cathepsin L (CTSL) and radical S-adenosyl methionine domain-containing 2 (RSAD2) expression was downregulated in the ipsilateral horn of SP4 ewes. This suggests that pretreating ewes with exogenous P4 may alleviate early pregnancy maternal constraint via mechanisms that alter uterine function. However, further research is required to investigate the timing of P4 administration and its impact on conception rates.
Additional keywords: embryo growth, endometrium, gene expression, progesterone supplementation, sheep.
References
Allen, W. R., Wilsher, S., Turnbull, C., Stewart, F., Ousey, J., Rossdale, P. D., and Fowden, A. L. (2002). Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction 123, 445–453.| Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Cls70%3D&md5=40e3d705933370c062576f0914c185acCAS |
Barker, D. J. (1995). Fetal origins of coronary heart disease. BMJ 311, 171–174.
| Fetal origins of coronary heart disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzjvVSrtw%3D%3D&md5=64ccfb837ec75a2d467eaa06bdce6bfcCAS |
Bassett, J. M., Oxborrow, T. J., Smith, I. D., and Thorburn, G. D. (1969). The concentration of progesterone in the peripheral plasma of the pregnant ewe. J. Endocrinol. 45, 449–457.
| The concentration of progesterone in the peripheral plasma of the pregnant ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhsVyl&md5=5dff1cd96f97aa5e37431fd095d476e6CAS |
Burghardt, R. C., Johnson, G. A., Jaeger, L. A., Ka, H., Garlow, J. E., Spencer, T. E., and Bazer, F. W. (2002). Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals. Cells Tissues Organs 172, 202–217.
| Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsVSjur8%3D&md5=817c8d2d764ca9f4d81ed85b15d55c67CAS |
Carnegie, J. A., and Roberston, H. A. (1978). Conjugated and unconjugated estrogens in fetal and maternal fluids of the pregnant ewe: a possible role for estrone sulfate during early pregnancy. Biol. Reprod. 19, 202–211.
| Conjugated and unconjugated estrogens in fetal and maternal fluids of the pregnant ewe: a possible role for estrone sulfate during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXls1Sqtr0%3D&md5=a59943fe8f457d68dabc9b9f3e7d6c31CAS |
Carson, D. D., Bagchi, I., Dey, S. K., Enders, A. C., Fazleabas, A. T., Lessey, B. A., and Yoshinaga, K. (2000). Embryo implantation. Dev. Biol. 223, 217–237.
| Embryo implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFeqs7o%3D&md5=e523410a6fd850ab3ab09568dfa6564eCAS |
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=bfbd17e9ed72b8903108af0a26504061CAS |
Charpigny, G., Reinaud, P., Tamby, J.-P., Créminon, C., Martal, J., Maclouf, J., and Guillomot, M. (1997). Expression of cyclooxygenase-1 and -2 in ovine endometrium during the estrous cycle and early pregnancy. Endocrinology 138, 2163–2171.
| Expression of cyclooxygenase-1 and -2 in ovine endometrium during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislCls74%3D&md5=1c4962414caeef1b630d2fcd33937784CAS |
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=db02bbad50a0f9884f6fd189eae30497CAS |
Dorniak, P., Bazer, F. W., and Spencer, T. E. (2011). Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol. Reprod. 84, 1119–1127.
| Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFemur4%3D&md5=2b5e3d83d125cfe7eea8a5d2f29692b0CAS |
Dziuk, P. J. (1992). Embryonic development and fetal growth. Anim. Reprod. Sci. 28, 299–308.
| Embryonic development and fetal growth.Crossref | GoogleScholarGoogle Scholar |
Eggleston, D. L., Wilken, C., Van Kirk, E. A., Slaughter, R. G., Ji, T. H., and Murdoch, W. J. (1990). Progesterone induces expression of endometrial messenger RNA encoding for cyclooxygenase (sheep). Prostaglandins 39, 675–683.
| Progesterone induces expression of endometrial messenger RNA encoding for cyclooxygenase (sheep).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslWntLw%3D&md5=a42aa9e4b0d53d7c28d598de991625c2CAS |
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=a25fb39b733d5a86e4c067c2c956b833CAS |
Gardner, D. S., Buttery, P. J., Daniel, Z., and Symonds, M. E. (2007). Factors affecting birth weight in sheep: maternal environment. Reproduction 133, 297–307.
| Factors affecting birth weight in sheep: maternal environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1ais78%3D&md5=4214c76b27208170707f2cae43f01398CAS |
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.
| Evidence for maternal regulation of early conceptus growth and development in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtFKh&md5=3e3a725a1550a080ae3ea140d417d79dCAS |
Gluckman, P. D. (1986) The regulation of fetal growth. In ‘Control and Manipulation of Animal Growth’. (Eds P. J. Buttery, D. B. Lindsay and N. B. Haynes.) pp. 85–104. (Butterworths: London.)
Gluckman, P. D., and Hanson, M. A. (2004). Maternal constraint of fetal growth and its consequences. Semin. Fetal Neonatal Med. 9, 419–425.
| Maternal constraint of fetal growth and its consequences.Crossref | GoogleScholarGoogle Scholar |
Gray, C. A., Adelson, D. L., Bazer, F. W., Burghardt, R. C., Meeusen, E. N. T., and Spencer, T. E. (2004). Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. Proc. Natl. Acad. Sci. USA 101, 7982–7987.
| Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslCisLg%3D&md5=59826440661b0135f34ecec7d688d96cCAS |
Gray, C. A., Dunlap, K. A., Burghardt, R. C., and Spencer, T. E. (2005). Galectin-15 in ovine uteroplacental tissues. Reproduction 130, 231–240.
| Galectin-15 in ovine uteroplacental tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVSksbvE&md5=8b55cbf05866f0cf2e46dce7673344a8CAS |
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=3b32bf0dd4995070b5b5563b8f84d42eCAS |
Hartwich, K. M., Walker, S. K., Owens, J. A., and Seamark, R. F. (1995). Progesterone supplementation in the ewe alters cell allocation to the inner cell mass. Proc Aust Soc Med Res 26, 128.
Hey, N. A., Graham, R. A., Seif, M. W., and Aplin, J. D. (1994). The polymorphic epithelial mucin MUC1 in human endometrium is regulated with maximal expression in the implantation phase. J. Clin. Endocrinol. Metab. 78, 337–342.
| 1:CAS:528:DyaK2cXitFeksr8%3D&md5=85d3cce0a866a0772ee37256844285aeCAS |
Hoffman, L. H., Olson, G. E., Carson, D. D., and Chilton, B. S. (1998). Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium. Endocrinology 139, 266–271.
| Progesterone and implanting blastocysts regulate Muc1 expression in rabbit uterine epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFOrug%3D%3D&md5=8c548bc7576a6299ad63fe9340d21dbcCAS |
Hou, Q., and Gorski, J. (1993). Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc. Natl. Acad. Sci. USA 90, 9460–9464.
| Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1aksL0%3D&md5=17dae2675336e2c98e6361264393316bCAS |
Ing, N. H., Francis, H., McDonnell, J. J., Amann, J. F., and Roberts, R. M. (1989). Progesterone induction of the uterine milk proteins: major secretory proteins of sheep endometrium. Biol. Reprod. 41, 643–654.
| Progesterone induction of the uterine milk proteins: major secretory proteins of sheep endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkvV2mtA%3D%3D&md5=2bcd8531246f6b745e58302a5e401030CAS |
Jefferies, B. C. (1961). Body condition scoring and its use in management. Tasm. J. Agric. 32, 19–21.
Johnson, G. A., Bazer, F. W., Jaeger, L. A., Ka, H., Garlow, J. E., Pfarrer, C., Spencer, T. E., and Burghardt, R. C. (2001). Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep. Biol. Reprod. 65, 820–828.
| Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFems7k%3D&md5=620c06eed63512f8c4be2dee3cc4bda3CAS |
Joubert, D. M., and Hammond, J. (1954). Maternal effect on birth weight in South Devon - Dexter cattle crosses. Nature 174, 647–648.
| Maternal effect on birth weight in South Devon - Dexter cattle crosses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FhsFajug%3D%3D&md5=9d1e72d242f465d99de7658821b6e706CAS |
Joubert, D. M., and Hammond, J. (1958). A crossbreeding experiment with cattle, with special reference to the maternal effect in South Devon–Dexter crosses. J. Agric. Sci. 51, 325–341.
| A crossbreeding experiment with cattle, with special reference to the maternal effect in South Devon–Dexter crosses.Crossref | GoogleScholarGoogle Scholar |
Kapur, S., Tamada, H., Dey, S. K., and Andrews, G. K. (1992). Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol. Reprod. 46, 208–219.
| Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xnslajtw%3D%3D&md5=4f61ca9628bc4ed6a08640bea98cf477CAS |
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |
Kennedy, T. G., Gillio-Meina, C., and Phang, S. H. (2007). Prostaglandins and the initiation of blastocyst implantation and decidualization. Reproduction 134, 635–643.
| Prostaglandins and the initiation of blastocyst implantation and decidualization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCisg%3D%3D&md5=2ca1dc182cd178ee83460726eb9f7829CAS |
Kim, S., Choi, Y., Spencer, T. E., and Bazer, F. W. (2003). Effects of the estrous cycle, pregnancy and interferon tau on expression of cyclooxygenase two (COX-2) in ovine endometrium. Reprod. Biol. Endocrinol. 1, 58.
| Effects of the estrous cycle, pregnancy and interferon tau on expression of cyclooxygenase two (COX-2) in ovine endometrium.Crossref | GoogleScholarGoogle Scholar |
Kleemann, D. O., Walker, S. K., and Seamark, R. F. (1994). Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy. J. Reprod. Fertil. 102, 411–417.
| Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7msFeqtw%3D%3D&md5=0c278e0f781971f988f033f97b862bcbCAS |
Kleemann, D. O., Walker, S. K., Hartwich, K. M., Fong, L., Seamark, R. F., Robinson, J. S., and Owens, J. A. (2001). Fetoplacental growth in sheep administered progesterone during the first three days of pregnancy. Placenta 22, 14–23.
| Fetoplacental growth in sheep administered progesterone during the first three days of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlaksLg%3D&md5=41dca92e83ecb732d13d3a2fa279f78eCAS |
Ko, Y., Lee, C. Y., Ott, T. L., Davis, M. A., Simmen, R. C., Bazer, F. W., and Simmen, F. A. (1991). Insulin-like growth factors in sheep uterine fluids: concentrations and relationship to ovine trophoblast protein-1 production during early pregnancy. Biol. Reprod. 45, 135–142.
| Insulin-like growth factors in sheep uterine fluids: concentrations and relationship to ovine trophoblast protein-1 production during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1GmsLg%3D&md5=1b3da40aeb8c08152c9f986fab9f5f14CAS |
Letcher, R., Simmen, R. C., Bazer, F. W., and Simmen, F. A. (1989). Insulin-like growth factor-I expression during early conceptus development in the pig. Biol. Reprod. 41, 1143–1151.
| Insulin-like growth factor-I expression during early conceptus development in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtleisL8%3D&md5=c9378585c028c51a4bc2ad284be8e4e8CAS |
Lozano, J. M., Abecia, J. A., Forcada, F., Zarazaga, L., and Alfaro, B. (1998). Effect of undernutrition on the distribution of progesterone in the uterus of ewes during the luteal phase of the estrous cycle. Theriogenology 49, 539–546.
| Effect of undernutrition on the distribution of progesterone in the uterus of ewes during the luteal phase of the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFShu74%3D&md5=2ab301df368d88300a87d0efa1e8f348CAS |
Mann, G. E., and Lamming, G. E. (2001). Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121, 175–180.
| Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslaqsw%3D%3D&md5=1c430c522d506c172cf710274fbb3261CAS |
Mann, G. E., Fray, M. D., and Lamming, G. E. (2006). Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow. Vet. J. 171, 500–503.
| Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Kis70%3D&md5=63957190e9099279286de64d655a922bCAS |
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=65a4664887a93de4ad09dc86cbdf79cfCAS |
McCracken, J. A., Schramm, W., and Okulicz, W. C. (1984). Hormone receptor control of pulsatile secretion of PGF2α from the ovine uterus during luteolysis and its abrogation in early pregnancy. Anim. Reprod. Sci. 7, 31–55.
| Hormone receptor control of pulsatile secretion of PGF2α from the ovine uterus during luteolysis and its abrogation in early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVCiu7g%3D&md5=ca70ac353a7da063436cf8a9ee19a946CAS |
McMillan, W. H. (1987). Post-mating progesterone supplementation in ewes and hoggets. Proc. NZ. Soc. Anim. Prod. 47, 151–153.
Meikle, A., Tasende, C., Sosa, C., and Garófalo, E. G. (2004). The role of sex steroid receptors in sheep female reproductive physiology. Reprod. Fertil. Dev. 16, 385–394.
| The role of sex steroid receptors in sheep female reproductive physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVGjtbY%3D&md5=6769963c4f3ed44049177543984c16f7CAS |
Nephew, K. P., Mcclure, K. E., Ott, T. L., Dubois, D. H., Bazer, F. W., and Pope, W. F. (1991). Relationship between variation in conceptus development and differences in estrous cycle duration in ewes. Biol. Reprod. 44, 536–539.
| Relationship between variation in conceptus development and differences in estrous cycle duration in ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFGkurg%3D&md5=9ecdfa86eeb6798ee8d46b18641227edCAS |
Pant, H. C., Hopkinson, C. R. N., and Fitzpatrick, R. J. (1977). Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrous cycle. J. Endocrinol. 73, 247–255.
| Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXkvVWktb0%3D&md5=8c2a0f6c4aa04fcb65cdd5f6125ec530CAS |
Parr, R. A., Davis, I. F., Fairclough, R. J., and Miles, M. A. (1987). Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep. J. Reprod. Fertil. 80, 317–320.
| Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktVWjtb4%3D&md5=3397e40918bc2795a0cf1085fd302487CAS |
Parr, M. H., Scully, S., Lonergan, P., Evans, A. C. O., Crowe, M., and Diskin, M. G. (2017). Establishment of critical timing of progesterone supplementation on corpus luteum and embryo development in beef heifers. Anim. Reprod. Sci. 180, 1–9.
| Establishment of critical timing of progesterone supplementation on corpus luteum and embryo development in beef heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjs1Wltr8%3D&md5=b5e8f58987f2398c0a8ca4e93871c8cfCAS |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT–PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=91eac11c0ea6f3f03935d293079e5320CAS |
Raheem, K. A., Marei, W. F. A., Campbell, B. K., and Fouladi-Nashta, A. A. (2016). In vivo and in vitro studies of MUC1 regulation in sheep endometrium. Theriogenology 85, 1635–1643.
| In vivo and in vitro studies of MUC1 regulation in sheep endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisFOrt7Y%3D&md5=8ce1fea9672b0c864c8b02f12a7cf73eCAS |
Reynolds, T. S., Stevenson, K. R., and Wathes, D. C. (1997). Pregnancy-specific alterations in the expression of the insulin-like growth factor system during early placental development in the ewe. Endocrinology 138, 886–897.
| Pregnancy-specific alterations in the expression of the insulin-like growth factor system during early placental development in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Oks7s%3D&md5=f5842187af1e39b725007f6eb302128fCAS |
Robinson, J. S., Moore, V. M., Owens, J. A., and McMillen, I. C. (2000). Origins of fetal growth restriction. Eur. J. Obstet. Gynecol. Reprod. Biol. 92, 13–19.
| Origins of fetal growth restriction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FislSjuw%3D%3D&md5=091c3a3acf57e6e1b692698c13da3854CAS |
Salamonsen, L. A. (1999). Role of proteases in implantation. Rev. Reprod. 4, 11–22.
| Role of proteases in implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtVeht7o%3D&md5=373d7ab86b26c5944159111a28e3008eCAS |
Satterfield, M. C., Bazer, F. W., and Spencer, T. E. (2006). Progesterone regulation of preimplantation conceptus growth and Galectin 15 (LGALS15) in the ovine uterus. Biol. Reprod. 75, 289–296.
| Progesterone regulation of preimplantation conceptus growth and Galectin 15 (LGALS15) in the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVWgsbo%3D&md5=dcaa3d128df7f00be96a2c2426f42c4cCAS |
Satterfield, M. C., Hayashi, K., Song, G., Black, S. G., Bazer, F. W., and Spencer, T. E. (2008). Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus. Biol. Reprod. 79, 1226–1236.
| Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCltL3N&md5=2b7e24270241e3cc973e97049fe8e300CAS |
Satterfield, M. C., Song, G., Kochan, K. J., Riggs, P. K., Simmons, R. M., Elsik, C. G., Adelson, D. L., Bazer, F. W., Zhou, H., and Spencer, T. E. (2009). Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation. Physiol. Genomics 39, 85–99.
| Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlakt77J&md5=e6b7941876bf87540d6c42615e4d318bCAS |
Sequeira, M., Pain, S. J., Sartore, I., Meikle, A., Kenyon, P. R., and Blair, H. T. (2012). Expression of uterine progesterone receptor in Suffolk and Cheviot ewes at Day 19 of pregnancy, following embryo transfer. Proc. NZ. Soc. Anim. Prod. 72, 35–37.
Sequeira, M., Pain, S. J., de Brun, V., Meikle, A., Kenyon, P. R., and Blair, H. T. (2016). Gestation-related gene expression and protein localization in endometrial tissue of Suffolk and Cheviot ewes at gestation Day 19, after transfer of Suffolk or Cheviot embryos. Theriogenology 86, 1557–1565.
| Gestation-related gene expression and protein localization in endometrial tissue of Suffolk and Cheviot ewes at gestation Day 19, after transfer of Suffolk or Cheviot embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpvVWqt7c%3D&md5=7451504b4c903baed3afd2647b9c7938CAS |
Sharma, R. K. (2010) The effects of uterine environment upon embryonic, fetal, neonatal and post-natal development and glucose metabolism in sheep. Ph.D Thesis, Massey University, Palmerston North, New Zealand.
Sharma, R. K., Blair, H. T., Jenkinson, C. M. C., Kenyon, P. R., Cockrem, J. F., and Parkinson, T. J. (2012). Uterine environment as a regulator of birth weight and body dimensions of newborn lambs. J. Anim. Sci. 90, 1338–1348.
| Uterine environment as a regulator of birth weight and body dimensions of newborn lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFanurc%3D&md5=c48391214d97f62fe420fdd975d9da33CAS |
Sharma, R. K., Parkinson, T. J., Kenyon, P. R., Jenkinson, C. M. C., and Blair, H. T. (2013). Uterine environment and early embryonic development in sheep. Small Rumin. Res. 115, 67–70.
| Uterine environment and early embryonic development in sheep.Crossref | GoogleScholarGoogle Scholar |
Simmen, R. C. M., Simmen, F. A., Hofig, A., Farmer, S. J., and Bazer, F. W. (1990). Hormonal regulation of insulin-like growth factor gene expression in pig uterus. Endocrinology 127, 2166–2174.
| Hormonal regulation of insulin-like growth factor gene expression in pig uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1Cks78%3D&md5=a011ab099d73b101d3b5af6bb67da7bdCAS |
Simmen, R. C. M., Ko, Y., and Simmen, F. A. (1993). Insulin-like growth factors and blastocyst development. Theriogenology 39, 163–175.
| Insulin-like growth factors and blastocyst development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1WitrY%3D&md5=9d4ad1bd57ba9a893c7582a073dad691CAS |
Simmons, R. M., Satterfield, M. C., Welsh, T. H., Bazer, F. W., and Spencer, T. E. (2010). HSD11B1, HSD11B2, PTGS2, and NR3C1 expression in the peri-implantation ovine uterus: effects of pregnancy, progesterone, and interferon tau. Biol. Reprod. 82, 35–43.
| HSD11B1, HSD11B2, PTGS2, and NR3C1 expression in the peri-implantation ovine uterus: effects of pregnancy, progesterone, and interferon tau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgsrrM&md5=7db380c4a5587fe33fd139a0222a7d42CAS |
Song, G., Spencer, T. E., and Bazer, F. W. (2005). Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau. Endocrinology 146, 4825–4833.
| Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGqurzJ&md5=76c3a5259f94549b42d750dfd078abf0CAS |
Song, G., Bazer, F. W., and Spencer, T. E. (2007). Pregnancy and interferon tau regulate RSAD2 and IFIH1 expression in the ovine uterus. Reproduction 133, 285–295.
| Pregnancy and interferon tau regulate RSAD2 and IFIH1 expression in the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1ais74%3D&md5=f4ff7ae8ee0d2edce7ebcce9ba2e2529CAS |
Spencer, T. E., and Bazer, F. W. (1995). Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol. Reprod. 53, 1527–1543.
| Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsVeisL8%3D&md5=ec8e6a3a63c2c1f0efe1bba09cee0942CAS |
Spencer, T. E., and Bazer, F. W. (2004). Conceptus signals for establishment and maintenance of pregnancy. Reprod. Biol. Endocrinol. 2, 49–63.
| Conceptus signals for establishment and maintenance of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Spencer, T. E., Johnson, G. A., Burghardt, R. C., and Bazer, F. W. (2004). Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol. Reprod. 71, 2–10.
| Progesterone and placental hormone actions on the uterus: insights from domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKktL8%3D&md5=54afbfcb88397c2f8f85e4caba74a1c6CAS |
Spencer, T. E., Sandra, O., and Wolf, E. (2008). Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 135, 165–179.
| Genes involved in conceptus–endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1yrtL4%3D&md5=3b64ff9dc8399d2026fb89333ff07bfaCAS |
Stevenson, K. R., Gilmour, R. S., and Wathes, D. C. (1994). Localization of insulin-like growth factor-I (IGF-I) and -II messenger ribonucleic acid and type 1 IGF receptors in the ovine uterus during the estrous cycle and early pregnancy. Endocrinology 134, 1655–1664.
| Localization of insulin-like growth factor-I (IGF-I) and -II messenger ribonucleic acid and type 1 IGF receptors in the ovine uterus during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis1aiu7o%3D&md5=7869eb2498ccf19b0d30285d0bfc62d1CAS |
Stewart, M. D., Johnson, G. A., Gray, C. A., Burghardt, R. C., Schuler, L. A., Joyce, M. M., Bazer, F. W., and Spencer, T. E. (2000). Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol. Reprod. 62, 1779–1789.
| Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsF2htr4%3D&md5=c635a5d1bb6348bc457a977629d69709CAS |
Stringfellow, D. A., and Givens, M. D. (2013) ‘Manual of the International Embryo Transfer Society: a Procedural Guide and General Information for Use of Embryo Transfer Technology Emphasizing Sanitary Procedures’. 4th edn. (IETS: Champaign, IL, USA.)
Thorburn, G. D., Bassett, J. M., and Smith, I. D. (1969). Progesterone concentration in the peripheral plasma of sheep during the oestrous cycle. J. Endocrinol. 45, 459–469.
| Progesterone concentration in the peripheral plasma of sheep during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhsVyk&md5=779fe85eed01c2be7a0b758e998dce10CAS |
van Mourik, M. S. M., Macklon, N. S., and Heijnen, C. J. (2009). Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J. Leukoc. Biol. 85, 4–19.
| Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1yqtA%3D%3D&md5=fd73be0ab3221594ea61d6cfe6e1222dCAS |
Wales, R. G., and Cuneo, C. L. (1989). Morphology and chemical analysis of the sheep conceptus from the 13th to the 19th day of pregnancy. Reprod. Fertil. Dev. 1, 31–39.
| Morphology and chemical analysis of the sheep conceptus from the 13th to the 19th day of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1yks70%3D&md5=a5830858d859f2243b13a2f42115c526CAS |
Walker, S. K., Hartwich, K. M., and Seamark, R. F. (1996). The production of unusually large offspring following embryo manipulation: Concepts and challenges. Theriogenology 45, 111–120.
| The production of unusually large offspring following embryo manipulation: Concepts and challenges.Crossref | GoogleScholarGoogle Scholar |
Walton, A., and Hammond, J. (1938). The maternal effects on growth and conformation in Shire horse–Shetland pony crosses. Proc. R. Soc. Lond. B Biol. Sci. 125, 311–335.
| The maternal effects on growth and conformation in Shire horse–Shetland pony crosses.Crossref | GoogleScholarGoogle Scholar |
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=80ccc45e1c73f000fcadd158b51975c7CAS |
Watson, A. J., Hogan, A., Hahnel, A., Schultz, G. A., and Wiemer, K. E. (1992). 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=ef7199dfe704dbe52c64e23d5c6323f9CAS |
Weems, C. W., Weems, Y. S., Lee, C. N., and Vincent, D. L. (1989). Progesterone in uterine and arterial tissue and in jugular and uterine venous plasma of sheep. Biol. Reprod. 41, 1–6.
| Progesterone in uterine and arterial tissue and in jugular and uterine venous plasma of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXls1OlsLg%3D&md5=055da011db18b107d8c1c50666900cdcCAS |
Wheaton, J. E., Carlson, K. M., Windels, H. F., and Johnston, L. J. (1993). CIDR: A new progesterone-releasing intravaginal device for induction of estrus and cycle control in sheep and goats. Anim. Reprod. Sci. 33, 127–141.
| CIDR: A new progesterone-releasing intravaginal device for induction of estrus and cycle control in sheep and goats.Crossref | GoogleScholarGoogle Scholar |
Wilmut, I., and Sales, D. I. (1981). Effect of an asynchronous environment on embryonic development in sheep. J. Reprod. Fertil. 61, 179–184.
| Effect of an asynchronous environment on embryonic development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2Fps1Cgtg%3D%3D&md5=1912dcccdcab7e0079a4ae70a35ab4e8CAS |
Young, L. E., Tregaskes, D., Butterwith, S. C., Sinclair, K. D., and Wilmut, I. (1995). Advancing the uterine environment of early ovine embryos by asynchronous transfer for 3 days affects foetal size at Day 21. J. Reprod. Fertil. Abstr. Ser. 15, 18–19.
