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Vertebrate reproductive science and technology
RESEARCH FRONT

Maternal recognition of pregnancy in the horse: a mystery still to be solved

C. Klein A B and M. H. T. Troedsson A
+ Author Affiliations
- Author Affiliations

A University of Kentucky, Department of Veterinary Science, 108 Gluck Equine Research Center, Lexington, KY 40546, USA.

B Corresponding author. Email: claudia.klein@uky.edu

Reproduction, Fertility and Development 23(8) 952-963 https://doi.org/10.1071/RD10294
Submitted: 4 November 2010  Accepted: 31 May 2011   Published: 30 September 2011

Abstract

Maternal recognition of pregnancy in the horse is the sum of events leading to maintenance of pregnancy; in a narrow sense, maternal recognition of pregnancy refers to the physiological process by which the lifespan of the corpus luteum is prolonged. The horse is one of the few domestic species in which the conceptus-derived pregnancy recognition signal has not been identified. The presence of the conceptus reduces pulsatile prostaglandin F secretion by the endometrium during early gestation in the mare, partly attributed to the reduced expression of cyclooxygenase-2. Cyclooxygenase-2 has therefore been suggested as one of the regulators of endometrial prostaglandin F release modified by the antiluteolytic factor secreted by the conceptus. In addition, altered oxytocin responsiveness has been implicated in the adjustment of prostaglandin release in pregnant mares. While conceptus mobility has proven to be essential for establishment of pregnancy, conceptus-derived oestrogens and prostaglandins, principally prostaglandin E2, have not been confirmed as the critical antiluteolytic factor. Various ways to induce prolonged luteal function in the non-pregnant mare will be highlighted in the current review, specifically, how they may pertain to the process of maternal recognition of pregnancy. Furthermore, recently published microarray experiments comparing the transcriptome of pregnant and non-pregnant endometria and different stages of conceptus development will be reviewed. Findings include the prevention of conceptus adhesion, the provision of nutrients to the conceptus and the avoidance of immunological rejection, among others.

Additional keywords: conceptus, equine, luteloysis, uterus.


References

Ababneh, M. M., Troedsson, M. H., Michelson, J. R., and Seguin, B. E. (2000). Partial characterization of an equine conceptus prostaglandin inhibitory factor. J. Reprod. Fertil. Suppl. 56, 607–613.
| 20681176PubMed |

Ababneh, M. M., Ababneh, H., and Shidaifat, F. (2011). Expression of cytosolic phospholipase A2 in equine endometrium during the oestrous cycle and early pregnancy. Reprod. Domest. Anim. 46, 268–274.
Expression of cytosolic phospholipase A2 in equine endometrium during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Wnt7w%3D&md5=3cf40cde1c0a867e860a27e1ca5543f3CAS |

Akinlosotu, B. A., Diehl, J. R., and Gimenez, T. (1986). Sparing effects of intrauterine treatment with prostaglandin E2 on luteal function in cycling gilts. Prostaglandins 32, 291–299.
Sparing effects of intrauterine treatment with prostaglandin E2 on luteal function in cycling gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtlGmtw%3D%3D&md5=e00463ee1bd804bfc46af522e7edd897CAS | 3467392PubMed |

Albihn, A., Waelchli, R. O., Samper, J., Oriol, J. G., Croy, B. A., and Betteridge, K. J. (2003). Production of capsular material by equine trophoblast transplanted into immunodeficient mice. Reproduction 125, 855–863.
Production of capsular material by equine trophoblast transplanted into immunodeficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFeltLY%3D&md5=44344c4b93095d8a0bd7463b33f103bfCAS | 12773108PubMed |

Allen, W. R., and Stewart, F. (2001). Equine placentation. Reprod. Fertil. Dev. 13, 623–634.
Equine placentation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383lvFyqtA%3D%3D&md5=48a6ef97f4d8f49e2509a0c5d8a80924CAS | 11999314PubMed |

Arar, S., Chan, K. H., Quinn, B. A., Waelchli, R. O., Hayes, M. A., Betteridge, K. J., and Monteiro, M. A. (2007). Desialylation of core type 1 O-glycan in the equine embryonic capsule coincides with immobilization of the conceptus in the uterus. Carbohydr. Res. 342, 1110–1115.
Desialylation of core type 1 O-glycan in the equine embryonic capsule coincides with immobilization of the conceptus in the uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktF2mtL8%3D&md5=60f1cf07adfd9c8e542e16a11d99f51fCAS | 17335787PubMed |

Austin, K. J., Bany, B. M., Belden, E. L., Rempel, L. A., Cross, J. C., and Hansen, T. R. (2003). Interferon-stimulated gene-15 (Isg15) expression is up-regulated in the mouse uterus in response to the implanting conceptus. Endocrinology 144, 3107–3113.
Interferon-stimulated gene-15 (Isg15) expression is up-regulated in the mouse uterus in response to the implanting conceptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvF2ktLo%3D&md5=8303e467ac54dc481e0ff0621ea3708eCAS | 12810567PubMed |

Austin, K. J., Carr, A. L., Pru, J. K., Hearne, C. E., George, E. L., Belden, E. L., and Hansen, T. R. (2004). Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy. Endocrinology 145, 967–975.
Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFSktA%3D%3D&md5=6e8d2ce496a3a49e90fbc95153775649CAS | 14563704PubMed |

Bae, S. E., and Watson, E. D. (2003). A light microscopic and ultrastructural study on the presence and location of oxytocin in the equine endometrium. Theriogenology 60, 909–921.
A light microscopic and ultrastructural study on the presence and location of oxytocin in the equine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVejtrc%3D&md5=0c124cab31fb6eff6c023d42ce711a98CAS | 12935868PubMed |

Baker, C. B., Adams, M. H., and McDowell, K. J. (1991). Lack of expression of alpha or omega interferons by the horse conceptus. J. Reprod. Fertil. Suppl. 44, 439–443.
| 1:CAS:528:DyaK38XltVGjtbc%3D&md5=d3c598479983f6256685403e8f7e237bCAS | 1724463PubMed |

Bazer, F. W., and Thatcher, W. W. (1977). Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2α by the uterine endometrium. Prostaglandins 14, 397–401.
Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F by the uterine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXls1WrtL8%3D&md5=e7e4766e636a4b58925542de3ebb4f30CAS | 897228PubMed |

Bebington, C., Bell, S. C., Doherty, F. J., Fazleabas, A. T., and Fleming, S. D. (1999). Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy. Biol. Reprod. 60, 920–928.
Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVGqsbg%3D&md5=4c830b85123e23bb3c91a21f852ef3a4CAS | 10084967PubMed |

Behrendt-Adam, C. Y., Adams, M. H., Simpson, K. S., and McDowell, K. J. (1999). Oxytocin-neurophysin I mRNA abundance in equine uterine endometrium. Domest. Anim. Endocrinol. 16, 183–192.
Oxytocin-neurophysin I mRNA abundance in equine uterine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjslCls74%3D&md5=8b4409687f7e99afe3251d5e76730eddCAS | 10343920PubMed |

Berg, S. L., and Ginther, O. J. (1978). Effect of estrogens on uterine tone and life span of the corpus luteum in mares. J. Anim. Sci. 47, 203–208.
| 1:CAS:528:DyaE1cXlslChsbc%3D&md5=73322df458be3f2d679717b8b0bc5f5dCAS | 711640PubMed |

Berglund, L. A., Sharp, D. C., Vernon, M. W., and Thatcher, W. W. (1982). Effect of pregnancy and collection technique on prostaglandin F in the uterine lumen of Pony mares. J. Reprod. Fertil. Suppl. 32, 335–341.
| 1:STN:280:DyaL3s7mtl2ltQ%3D%3D&md5=087ba4e3e75c4e35f06aee529fafda1fCAS | 6962869PubMed |

Betteridge, K. J., Eaglesome, M. D., Mitchell, D., Flood, P. F., and Beriault, R. (1982). Development of horse embryos up to twenty two days after ovulation: observations on fresh specimens. J. Anat. 135, 191–209.
| 1:STN:280:DyaL3s%2FjtVGnsg%3D%3D&md5=a76a31c3e7989ee066694ce4964527b2CAS | 7130052PubMed |

Boerboom, D., Brown, K. A., Vaillancourt, D., Poitras, P., Goff, A. K., Watanabe, K., Dore, M., and Sirois, J. (2004). Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy. Biol. Reprod. 70, 391–399.
Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslyquw%3D%3D&md5=d481e954ddde22919001cca326a91e45CAS | 14561653PubMed |

Budik, S., Lussy, H., and Aurich, C. (2010). Quantification of different type I interferons in equine embryos at days 10–16 of gestation. Anim. Reprod. Sci. 121S, S307–S308.

Burns, P. D., Graf, G. A., Hayes, S. H., and Silvia, W. J. (1997). Cellular mechanisms by which oxytocin stimulates uterine PGF2 alpha synthesis in bovine endometrium: roles of phospholipases C and A2. Domest. Anim. Endocrinol. 14, 181–191.
Cellular mechanisms by which oxytocin stimulates uterine PGF2 alpha synthesis in bovine endometrium: roles of phospholipases C and A2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1yltr8%3D&md5=4954d9830cd3b44605239d04399873e0CAS | 9171976PubMed |

Christenson, L. K., Farley, D. B., Anderson, L. H., and Ford, S. P. (1994). Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2. Prostaglandins 47, 61–75.
Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht1Gqs7w%3D&md5=af323a5207f8cb120fa8f076c4a98a9cCAS | 8140263PubMed |

Cochet, M., Vaiman, D., and Lefevre, F. (2009). Novel interferon delta genes in mammals: cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening. Gene 433, 88–99.
Novel interferon delta genes in mammals: cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFehuro%3D&md5=1adc4da311555a592d2962c9552c05cbCAS | 19110041PubMed |

Cooke, R. G., and Ahmad, N. (1994). Prostaglandin E2 alpha-induced release of oxytocin from ovine corpora lutea in vitro. Prostaglandins 48, 257–261.
Prostaglandin E2 alpha-induced release of oxytocin from ovine corpora lutea in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmslarsbc%3D&md5=ff5eb3f4adb3375923756028619200b2CAS | 7878193PubMed |

Douglas, R. H., and Ginther, O. J. (1976). Concentration of prostaglandins F in uterine venous plasma of anesthetized mares during the estrous cycle and early pregnancy. Prostaglandins 11, 251–260.
Concentration of prostaglandins F in uterine venous plasma of anesthetized mares during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhsVymtr0%3D&md5=8225cb64fbeb60f0d1bfb84c520f3e8dCAS | 1265294PubMed |

Ealy, A. D., Eroh,, M. L., and Sharp, D. C., (2010). Prostaglandin H synthase Type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture. Anim. Reprod. Sci. 117, 99–105.
Prostaglandin H synthase Type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyjt7nI&md5=4060fb5dc2b541d5cfd1cac156dfc638CAS | 19443143PubMed |

Fairclough, R. J., Moore, L. G., McGowan, L. T., Peterson, A. J., Smith, J. F., Tervit, H. R., and Watkins, W. B. (1980). Temporal relationship between plasma concentrations of 13,14-dihydro-15-keto-prostaglandin F and neurophysin I/II around luteolysis in sheep. Prostaglandins 20, 199–208.
Temporal relationship between plasma concentrations of 13,14-dihydro-15-keto-prostaglandin F and neurophysin I/II around luteolysis in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXls1Ghu74%3D&md5=603af1b85f141ba4186a6b066cd02733CAS | 7191132PubMed |

Fazleabas, A. T., Geisert, R. D., Bazer, F. W., and Roberts, R. M. (1983). Relationship between release of plasminogen activator and estrogen by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biol. Reprod. 29, 225–238.
| 1:CAS:528:DyaL3sXlsleltrk%3D&md5=62f1fe5ae424eb02d76ad1816d1438b9CAS | 6225472PubMed |

Fields, P. A., Eldridge, R. K., Fuchs, A. R., Roberts, R. F., and Fields, M. J. (1983). Human placental and bovine corpora luteal oxytocin. Endocrinology 112, 1544–1546.
Human placental and bovine corpora luteal oxytocin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXksVyitrg%3D&md5=f93035bd7debb982c8083db3f12ba8cfCAS | 6832059PubMed |

Flood, P. F., Betteridge, K. J., and Diocee, M. S. (1982). Transmission electron microscopy of horse embryos 3–16 days after ovulation. J. Reprod. Fertil. Suppl. 32, 319–327.
| 1:STN:280:DyaL3s7mtl2ltw%3D%3D&md5=ad5c63f01b2932373a8320a3882f8eb8CAS | 6962867PubMed |

Gastal, M. O., Gastal, E. L., Kot, K., and Ginther, O. J. (1996). Factors related to the time of fixation of the conceptus in mares. Theriogenology 46, 1171–1180.
Factors related to the time of fixation of the conceptus in mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVOgtg%3D%3D&md5=a80946caeb5d28db96fa2f636aef7f7aCAS | 16727980PubMed |

Gastal, M. O., Gastal, E. L., Torres, C. A., and Ginther, O. J. (1998). Effect of PGE2 on uterine contractility and tone in mares. Theriogenology 50, 989–999.
Effect of PGE2 on uterine contractility and tone in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Ohuw%3D%3D&md5=d846d8318a2826ab64a57db41877b9abCAS | 10734418PubMed |

Gilbert, C. L., Lamming, G. E., Parkinson, T. J., Flint, A. P., and Wathes, D. C. (1989). Oxytocin infusion from day 10 after oestrus extends the luteal phase in non-pregnant cattle. J. Reprod. Fertil. 86, 203–210.
Oxytocin infusion from day 10 after oestrus extends the luteal phase in non-pregnant cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktFyjs7k%3D&md5=c9192df3acfb3b24da103d8caa717199CAS | 2754640PubMed |

Ginther, O. J. (1974). Internal regulation of physiological processes through local venoarterial pathways: a review. J. Anim. Sci. 39, 550–564.
| 1:STN:280:DyaE2M%2FhtFamsQ%3D%3D&md5=038ba4c543078d43b5c86f9358ad2728CAS | 4213194PubMed |

Ginther, O. J. (1983a). Fixation and orientation of the early equine conceptus. Theriogenology 19, 613–623.
Fixation and orientation of the early equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVGrsQ%3D%3D&md5=cc952279531e1986b802962a535fe467CAS | 16725809PubMed |

Ginther, O. J. (1983b). Mobility of the early equine conceptus. Theriogenology 19, 603–611.
Mobility of the early equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVGrsA%3D%3D&md5=eebd32b4f08a1e7333469e0b7b39316aCAS | 16725808PubMed |

Ginther, O. J. (1984). Mobility of twin embryonic vesicles in mares. Theriogenology 22, 83–95.
Mobility of twin embryonic vesicles in mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVOisw%3D%3D&md5=6c566e39afe13c8066ceb35b6ff33615CAS | 16725939PubMed |

Goff, A. K., Pontbriand, D., and Sirois, J. (1987). Oxytocin stimulation of plasma 15-keto-13,14-dihydro prostaglandin F-2 alpha during the oestrous cycle and early pregnancy in the mare. J. Reprod. Fertil. Suppl. 35, 253–260.
| 1:CAS:528:DyaL2sXmt12qtbs%3D&md5=564d021b89099c5f40d062360803f840CAS | 3479581PubMed |

Goff, A. K., Leduc, S., Poitras, P., and Vaillancourt, D. (1993a). Steroid synthesis by equine conceptuses between days 7 and 14 and endometrial steroid metabolism. Domest. Anim. Endocrinol. 10, 229–236.
Steroid synthesis by equine conceptuses between days 7 and 14 and endometrial steroid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXps1ajsw%3D%3D&md5=b6f9aa3c7a196e4d684517f2da706f84CAS | 8252843PubMed |

Goff, A. K., Sirois, J., and Pontbriand, D. (1993b). Effect of oestradiol on oxytocin-stimulated prostaglandin F2α release in mares. J. Reprod. Fertil. 98, 107–112.
Effect of oestradiol on oxytocin-stimulated prostaglandin F release in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlWrt7c%3D&md5=0d5e6ec153e19c0e0a57ea22ed4c9432CAS | 8345453PubMed |

Gross, T. S., Thatcher, W. W., Hansen, P. J., Johnson, J. W., and Helmer, S. D. (1988). Presence of an intracellular endometrial inhibitor of prostaglandin synthesis during early pregnancy in the cow. Prostaglandins 35, 359–378.
Presence of an intracellular endometrial inhibitor of prostaglandin synthesis during early pregnancy in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvFyqsLs%3D&md5=9fe2fdc2c4bfa525b03eefc9b8c4d937CAS | 3131835PubMed |

Hama, K., Aoki, J., Bandoh, K., Inoue, A., Endo, T., Amano, T., Suzuki, H., and Arai, H. (2006). Lysophosphatidic receptor, LPA3, is positively and negatively regulated by progesterone and estrogen in the mouse uterus. Life Sci. 79, 1736–1740.
Lysophosphatidic receptor, LPA3, is positively and negatively regulated by progesterone and estrogen in the mouse uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1ajtLw%3D&md5=0210c638988b0416be6e8b82b1c270d2CAS | 16815476PubMed |

Henry, G. E., Momin, R. A., Nair, M. G., and DeWitt, D. L. (2002). Antioxidant and cyclooxygenase activities of fatty acids found in food. J. Agric. Food Chem. 50, 2231–2234.
Antioxidant and cyclooxygenase activities of fatty acids found in food.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlOkt7w%3D&md5=6f090bb46dca282cf04b2e5d65382370CAS | 11929276PubMed |

Hicks, B. A., Etter, S. J., Carnahan, K. G., Joyce, M. M., Assiri, A. A., Carling, S. J., Kodali, K., Johnson, G. A., Hansen, T. R., Mirando, M. A., Woods, G. L., Vanderwall, D. K., and Ott, T. L. (2003). Expression of the uterine Mx protein in cyclic and pregnant cows, gilts, and mares. J. Anim. Sci. 81, 1552–1561.
| 1:CAS:528:DC%2BD3sXksFeqtLs%3D&md5=5b52777f1702f9b0fb0b184bfd888ad9CAS | 12817504PubMed |

Kindahl, H., Knudsen, O., Madej, A., and Edqvist, L. E. (1982). Progesterone, prostaglandin F-2 alpha, PMSG and oestrone sulphate during early pregnancy in the mare. J. Reprod. Fertil. Suppl. 32, 353–359.
| 1:STN:280:DyaL3s7mtl2ksg%3D%3D&md5=8b84508e5ddd9f0c349563475db4ddd5CAS | 6300390PubMed |

Klein, C., and Troedsson, M. H. (2011). Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse. Biol. Reprod. 84, 872–885.
Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGju7Y%3D&md5=c011f7018ba1750d236a3c60975e3901CAS | 21209420PubMed |

Klein, C., Scoggin, K. E., Ealy, A. D., and Troedsson, M. H. (2010). Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol. Reprod. 83, 102–113.
Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLc%3D&md5=c188ccb956c7e6b2beb5aff4c1a46fc0CAS | 20335638PubMed |

Klein, C., Scoggin, K. E., and Troedsson, M. H. T. (2011). The expression of interferon-stimulated gene 15 in equine endometrium. Reprod. Domest. Anim. 46, 692–698.
The expression of interferon-stimulated gene 15 in equine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2hsL3N&md5=e1b742da96dedac32072d4679ac3bce6CAS | 21241378PubMed |

Lefevre, F., and Boulay, V. (1993). A novel and atypical type one interferon gene expressed by trophoblast during early pregnancy. J. Biol. Chem. 268, 19760–19768.
| 1:CAS:528:DyaK2cXlt1aqsg%3D%3D&md5=287558bb8f0f0991e4a47e55aeb2455aCAS | 7690039PubMed |

Leith, G. S., and Ginther, O. J. (1984). Characterization of intrauterine mobility of the early equine conceptus. Theriogenology 22, 401–408.
Characterization of intrauterine mobility of the early equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVOnsA%3D%3D&md5=ca7bf92f48289ce6538e7a17f90401f5CAS | 16725972PubMed |

Lin, L. L., Wartmann, M., Lin, A. Y., Knopf, J. L., Seth, A., and Davis, R. J. (1993). cPLA2 is phosphorylated and activated by MAP kinase. Cell 72, 269–278.
cPLA2 is phosphorylated and activated by MAP kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVGjt74%3D&md5=9da18531fd1b0a43608d157348c74335CAS | 8381049PubMed |

McCracken, J. A., Custer, E. E., and Lamsa, J. C. (1999). Luteolysis: a neuroendocrine-mediated event. Physiol. Rev. 79, 263–323.
| 1:CAS:528:DyaK1MXivFektLg%3D&md5=31f2b681ced2221ce3324c06d9239e7aCAS | 10221982PubMed |

McDowell, K. J., Sharp, D. C., Grubaugh, W., Thatcher, W. W., and Wilcox, C. J. (1988). Restricted conceptus mobility results in failure of pregnancy maintenance in mares. Biol. Reprod. 39, 340–348.
Restricted conceptus mobility results in failure of pregnancy maintenance in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls1ektr8%3D&md5=bb7d73717fc1478f44511948f0c20786CAS | 3179385PubMed |

Merkl, M., Ulbrich, S. E., Otzdorff, C., Herbach, N., Wanke, R., Wolf, E., Handler, J., and Bauersachs, S. (2010). Microarray analysis of equine endometrium at Days 8 and 12 of pregnancy. Biol. Reprod. 83, 874–886.
Microarray analysis of equine endometrium at Days 8 and 12 of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGls7%2FF&md5=a18340f71ae697286e564aeb59d2cddeCAS | 20631402PubMed |

Monti, E., Preti, A., Rossi, E., Ballabio, A., and Borsani, G. (1999). Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases. Genomics 57, 137–143.
Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitFOms7Y%3D&md5=5233fef7898c2ebd32ee7f4dbf9aae4fCAS | 10191093PubMed |

Nie, G. J. (2001). Use of a glass ball to suppress behavioral estrus in mares. Proceedings of the 47th AAEP Annual Convention, San Diego, California, USA, 24–28 November.

Needleman, P., Turk, J., Jakschik, B. A., Morrison, A. R., and Lefkowith, J. B. (1986). Arachidonic acid metabolism. Annu. Rev. Biochem. 55, 69–102.
Arachidonic acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltFaru7g%3D&md5=0267a43e22d47978ddc29633ef408838CAS | 3017195PubMed |

Neely, D. P., Stabenfeldt, G. H., and Sauter, C. L. (1979). The effect of exogenous oxytocin on luteal function in mares. J. Reprod. Fertil. 55, 303–308.
The effect of exogenous oxytocin on luteal function in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhvFyisbo%3D&md5=09dc7a9fe27692f07033cf1cab542716CAS | 571469PubMed |

Oriol, J. G., Betteridge, K. J., Clarke, A. J., and Sharom, F. J. (1993a). Mucin-like glycoproteins in the equine embryonic capsule. Mol. Reprod. Dev. 34, 255–265.
Mucin-like glycoproteins in the equine embryonic capsule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVGlsr8%3D&md5=c41d2b759c081c5164d9374673d0cbf5CAS | 8471247PubMed |

Oriol, J. G., Sharom, F. J., and Betteridge, K. J. (1993b). Developmentally regulated changes in the glycoproteins of the equine embryonic capsule. J. Reprod. Fertil. 99, 653–664.
Developmentally regulated changes in the glycoproteins of the equine embryonic capsule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFentbc%3D&md5=4a1ff13a25e73f67d364ff45710891dcCAS | 8107051PubMed |

Pace-Asciak, C., and Wolfe, L. S. (1968). Inhibition of prostaglandin synthesis by oleic, linoleic and linolenic acids. Biochim. Biophys. Acta 152, 784–787.
| 1:CAS:528:DyaF1cXktlCjs7o%3D&md5=e7c8f1c9ea7855c42c59e5961d923e7aCAS | 5660093PubMed |

Pope, W. F., Maurer, R. R., and Stormshak, F. (1982). Intrauterine migration of the porcine embryo: influence of estradiol-17 beta and histamine. Biol. Reprod. 27, 575–579.
Intrauterine migration of the porcine embryo: influence of estradiol-17 beta and histamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XmtVyksLY%3D&md5=5e40832899b2abaaabdd7903b9baa6c7CAS | 6814544PubMed |

Pratt, B. R., Butcher, R. L., and Inskeep, E. K. (1977). Antiluteolytic effect of the conceptus and of PGE2 in ewes. J. Anim. Sci. 45, 784–791.
| 1:CAS:528:DyaE1cXhs1eqsQ%3D%3D&md5=c8b138e54b5786acf95123c61b6961e4CAS | 924907PubMed |

Raeside, J. I., Christie, H. L., Renaud, R. L., Waelchli, R. O., and Betteridge, K. J. (2004). Estrogen metabolism in the equine conceptus and endometrium during early pregnancy in relation to estrogen concentrations in yolk-sac fluid. Biol. Reprod. 71, 1120–1127.
Estrogen metabolism in the equine conceptus and endometrium during early pregnancy in relation to estrogen concentrations in yolk-sac fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7s%3D&md5=83d5a793e0484e2b6988c899068d0405CAS | 15163615PubMed |

Rivera del Alamo, M. M., Reilas, T., Kindahl, H., and Katila, T. (2008). Mechanisms behind intrauterine device-induced luteal persistence in mares. Anim. Reprod. Sci. 107, 94–106.
Mechanisms behind intrauterine device-induced luteal persistence in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlyhs7o%3D&md5=a8d5ed517f408d11fa79cbb5d06c2e33CAS | 17643876PubMed |

Rivera del Alamo, M. M., Reilas, T., Kindahl, H., Rodríguez-Gil, J. E., Rigau, T., and Katila, T. (2010). The luteostatic effect of intrauterine devices in mares is associated with endometrial expression of COX-2. Anim. Reprod. Sci. 121, 227–228.
The luteostatic effect of intrauterine devices in mares is associated with endometrial expression of COX-2.Crossref | GoogleScholarGoogle Scholar |

Rout, U. K., Wang, J., Paria, B. C., and Armant, D. R. (2004). Alpha5beta1, alphaVbeta3 and the platelet-associated integrin alphaIIbbeta3 coordinately regulate adhesion and migration of differentiating mouse trophoblast cells. Dev. Biol. 268, 135–151.
| 1:CAS:528:DC%2BD2cXitFKgu70%3D&md5=2df220282a8d18086d91cf80029a6c50CAS | 15031111PubMed |

Sharp, D. C., McDowell, K. J., Weithenauer, J., Franklin, K., Mirando, M., and Bazer, F. W. (1989a). Is an interferon-like protein involved in the maternal recognition of pregnancy in mares? Equine Vet. J. 21, 7–9.
Is an interferon-like protein involved in the maternal recognition of pregnancy in mares?Crossref | GoogleScholarGoogle Scholar |

Sharp, D. C., McDowell, K. J., Weithenauer, J., and Thatcher, W. W. (1989b). The continuum of events leading to maternal recognition of pregnancy in mares. J. Reprod. Fertil. Suppl. 37, 101–107.
| 1:CAS:528:DyaL1MXitVKntbs%3D&md5=c79d6fae5675c79c64c63577ed6fbc78CAS | 2810225PubMed |

Sharp, D. C., Thatcher, M. J., Salute, M. E., and Fuchs, A. R. (1997). Relationship between endometrial oxytocin receptors and oxytocin-induced prostaglandin F2α release during the oestrous cycle and early pregnancy in pony mares. J. Reprod. Fertil. 109, 137–144.
Relationship between endometrial oxytocin receptors and oxytocin-induced prostaglandin F release during the oestrous cycle and early pregnancy in pony mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gmu7c%3D&md5=753f3cfb7997d7c19be1f2a5c955d1afCAS | 9068425PubMed |

Short, R. V. (1969). Implantation and the maternal recognition of pregnancy. In ‘Ciba Foundation Symposium on Foetal Autonomy’. (Eds G. E. W. Wolstenholme and M. O’Connor.) pp. 2–26. (London, Churchill.)

Silva, L. A., Gastal, E. L., Beg, M. A., and Ginther, O. J. (2005). Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares. Biol. Reprod. 72, 755–761.
Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVeisbo%3D&md5=208ef98244e55862e1970e3aee239605CAS | 15576822PubMed |

Starbuck, G. R., Stout, T. A., Lamming, G. E., Allen, W. R., and Flint, A. P. (1998). Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy. J. Reprod. Fertil. 113, 173–179.
Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFOnu78%3D&md5=bbdb1da6ea52d3939c2ddf564e9b8505CAS | 9861156PubMed |

Stock, A. E., Emeny, R. T., Sirois, J., and Fortune, J. E. (1995). Oxytocin in mares: lack of evidence for oxytocin production by or action on preovulatory follicles. Domest. Anim. Endocrinol. 12, 133–142.
Oxytocin in mares: lack of evidence for oxytocin production by or action on preovulatory follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvVOit7c%3D&md5=1481e22c4c7ae3ed2553239e2e757059CAS | 7600764PubMed |

Stout, T. A., and Allen, W. R. (2001). Role of prostaglandins in intrauterine migration of the equine conceptus. Reproduction 121, 771–775.
Role of prostaglandins in intrauterine migration of the equine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVait7w%3D&md5=ca4d2c87c9fd8a18d9e097ee4fec5a96CAS | 11427165PubMed |

Stout, T. A., and Allen, W. R. (2002). Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares. Reproduction 123, 261–268.
Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFChtr8%3D&md5=6605fefdbb01358e732dc2c819190361CAS | 11866693PubMed |

Stout, T. A., Lamming, G. E., and Allen, W. R. (1999). Oxytocin administration prolongs luteal function in cyclic mares. J. Reprod. Fertil. 116, 315–320.
Oxytocin administration prolongs luteal function in cyclic mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOltbw%3D&md5=b180336fb26cf10422d16521f0c04025CAS | 10615256PubMed |

Stout, T. A., Meadows, S., and Allen, W. R. (2005). Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim. Reprod. Sci. 87, 269–281.
Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M3mvVWitQ%3D%3D&md5=3fea41ddf6ccc1981d6a92d87b2eda74CAS | 15911176PubMed |

Tabibzadeh, S. (1998). Molecular control of the implantation window. Hum. Reprod. Update 4, 465–471.
Molecular control of the implantation window.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7kvFynsQ%3D%3D&md5=a387ffe66ae9b190592b6a56da5d76eeCAS | 10027597PubMed |

Tamby, J. P., Charpigny, G., Reinaud, P., and Martal, J. (1993). Phospholipase A2 activity in endometrium from early pregnant and non-pregnant ewes. Prostaglandins 46, 407–415.
Phospholipase A2 activity in endometrium from early pregnant and non-pregnant ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXisVaitQ%3D%3D&md5=574de809b2078af01513e3fc54d29d6fCAS | 8278618PubMed |

Tetzke, T. A., Ismail, S., Mikuckis, G., and Evans, J. W. (1987). Patterns of oxytocin secretion during the oestrous cycle of the mare. J. Reprod. Fertil. Suppl. 35, 245–252.
| 1:CAS:528:DyaL2sXmt12mtrs%3D&md5=cee2328254d70c3ab918a985d98f7592CAS | 3479579PubMed |

Thatcher, W. W., Meyer, M. D., and Danet-Desnoyers, G. (1995). Maternal recognition of pregnancy. J. Reprod. Fertil. Suppl. 49, 15–28.
| 1:CAS:528:DyaK2MXmslWit7o%3D&md5=c9110b671c127bb28c700f7a6f35556fCAS | 7623310PubMed |

Tremoleda, J. L., Stout, T. A., Lagutina, I., Lazzari, G., Bevers, M. M., Colenbrander, B., and Galli, C. (2003). Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biol. Reprod. 69, 1895–1906.
Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCns7k%3D&md5=099ca974c068499e2c1fea9ae9104963CAS | 12904313PubMed |

Vanderwall, D. K., Woods, G. L., Weber, J. A., and Lichtenwalner, A. B. (1993). Uterine transport of prostaglandin E(2)-releasing simulated embryonic vesicles in mares. Theriogenology 40, 13–20.
Uterine transport of prostaglandin E(2)-releasing simulated embryonic vesicles in mares.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVSmsw%3D%3D&md5=74affc677be0f472247f6867b6610e83CAS | 16727290PubMed |

Vanderwall, D. K., Woods, G. L., Weber, J. A., and Lichtenwalner, A. B. (1994). Corpus luteal function in nonpregnant mares following intrauterine administration of prostaglandin E(2) or estradiol-17beta. Theriogenology 42, 1069–1083.
Corpus luteal function in nonpregnant mares following intrauterine administration of prostaglandin E(2) or estradiol-17beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1Giu7o%3D&md5=fa6b55ced02abf6473673209465e1b91CAS | 16727611PubMed |

Vanderwall, D. K., Silvia, W. J., and Fitzgerald, B. P. (1998). Concentrations of oxytocin in the intercavernous sinus of mares during luteolysis: temporal relationship with concentrations of 13,14-dihydro-15-keto-prostaglandin F2α. J. Reprod. Fertil. 112, 337–346.
Concentrations of oxytocin in the intercavernous sinus of mares during luteolysis: temporal relationship with concentrations of 13,14-dihydro-15-keto-prostaglandin F.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVensLg%3D&md5=abd2d2d5dad6d8e78545c5c8df133e4cCAS | 9640273PubMed |

Vanderwall, D. K., Rasmussen, D. M., and Woods, G. L. (2007). Effect of repeated administration of oxytocin during diestrus on duration of function of corpora lutea in mares. J. Am. Vet. Med. Assoc. 231, 1864–1867.
Effect of repeated administration of oxytocin during diestrus on duration of function of corpora lutea in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVChug%3D%3D&md5=984f008019107cb9dfd3e89199ae125fCAS | 18081527PubMed |

Vernon, M. W., Strauss, S., Simonelli, M., Zavy, M. T., and Sharp, D. C. (1979). Specific PGF-2 alpha binding by the corpus luteum of the pregnant and non-pregnant mare. J. Reprod. Fertil. Suppl. 27, 421–429.
| 289819PubMed |

Vernon, M. W., Zavy, M. T., Asquith, R. L., and Sharp, D. C. (1981). Prostaglandin F2α in the equine endometrium: steroid modulation and production capacities during the estrous cycle and early pregnancy. Biol. Reprod. 25, 581–589.
Prostaglandin F in the equine endometrium: steroid modulation and production capacities during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XpvF0%3D&md5=f1a4d6d94979206f5b5c60ddd45374bcCAS | 6946841PubMed |

Wathes, D. C., and Swann, R. W. (1982). Is oxytocin an ovarian hormone? Nature 297, 225–227.
Is oxytocin an ovarian hormone?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XkvVGltr4%3D&md5=c170b7562c7cc37744412404831a386bCAS | 7078636PubMed |

Watson, E. D. (1991). Do mares possess an intracellular endometrial inhibitor of prostaglandin synthesis during early pregnancy? Theriogenology 36, 67–71.
Do mares possess an intracellular endometrial inhibitor of prostaglandin synthesis during early pregnancy?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvF2nur0%3D&md5=26a735ad5e1a421228579d55c96f763dCAS | 16726978PubMed |

Watson, E. D., and Sertich, P. L. (1989). Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares. J. Reprod. Fertil. 87, 331–336.
Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvVyiu7Y%3D&md5=cc33628ddc586a859438a02ce0c6b70dCAS | 2621704PubMed |

Watson, E. D., and Sertich, P. L. (1992). Effect of repeated collection of multiple endometrial biopsy specimens on subsequent pregnancy in mares. J. Am. Vet. Med. Assoc. 201, 438–440.
| 1:STN:280:DyaK38znt1Chsw%3D%3D&md5=10531dcf50dc41207ed2036c46d625a4CAS | 1506247PubMed |

Watson, E. D., Buckingham, J., and Bjorksten, T. S. (1999). Immunolocalisation of oxytocin in the equine ovary. Equine Vet. J. 31, 174–175.
Immunolocalisation of oxytocin in the equine ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3ivVCntw%3D%3D&md5=e81379954462064d7c3262b641d11b06CAS | 10213431PubMed |

Weber, J. A., Freeman, D. A., Vanderwall, D. K., and Woods, G. L. (1991a). Prostaglandin E2 hastens oviductal transport of equine embryos. Biol. Reprod. 45, 544–546.
Prostaglandin E2 hastens oviductal transport of equine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvF2msLs%3D&md5=4a97793513a7e67eaf437ed609ffff7bCAS | 1751628PubMed |

Weber, J. A., Freeman, D. A., Vanderwall, D. K., and Woods, G. L. (1991b). Prostaglandin E2 secretion by oviductal transport-stage equine embryos. Biol. Reprod. 45, 540–543.
Prostaglandin E2 secretion by oviductal transport-stage equine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvF2msLo%3D&md5=ac88159a8c355ac35ccd6a656da51e68CAS | 1751627PubMed |

Weber, J. A., Woods, G. L., Freeman, D. A., and Vanderwall, D. K. (1992). Prostaglandin E2-specific binding to the equine oviduct. Prostaglandins 43, 61–65.
Prostaglandin E2-specific binding to the equine oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XnslSmsA%3D%3D&md5=e84594237cfb7ec662a6073ca2d99bc2CAS | 1546174PubMed |

Weems, Y. S., Nett, T. M., Rispoli, L. A., Davis, T. L., Johnson, D. L., Uchima, T., Raney, A., Lennon, E., Pang, J., Harbert, T., Bowers, G., Goto, K., Ong, A., Tsutahara, N., Randel, R. D., and Weems, C. W. (2010). Prostaglandin E1 (PGE1), but not prostaglandin E2 (PGE2), alters luteal and endometrial luteinizing hormone (LH) occupied and unoccupied LH receptors and mRNA for LH receptors in ovine luteal tissue to prevent luteolysis. Prostaglandins Other Lipid Mediat. 91, 42–50.
Prostaglandin E1 (PGE1), but not prostaglandin E2 (PGE2), alters luteal and endometrial luteinizing hormone (LH) occupied and unoccupied LH receptors and mRNA for LH receptors in ovine luteal tissue to prevent luteolysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12gsro%3D&md5=346d3d85f0e627c314621987b59fac3eCAS | 20060488PubMed |

Wilsher, S., and Allen, W. R. (2011). Intrauterine administration of plant oils inhibits luteolysis in the mare. Equine Vet. J. 43, 99–105.
Intrauterine administration of plant oils inhibits luteolysis in the mare.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FjvFaqsA%3D%3D&md5=c351f0dd7f716993ba2755e171d8d9e8CAS | 21143640PubMed |

Woodley, S. L., Burns, P. J., Douglas, R. H., and Oxender, W. D. (1979). Prolonged interovulatory interval after oestradiol treatment in mares. J. Reprod. Fertil. Suppl. 27, 205–209.
| 289791PubMed |

Zavy, M. T., Bazer, F. W., Sharp, D. C., Frank, M., and Thatcher, W. W. (1978). Uterine luminal prostaglandin F in cycling mares. Prostaglandins 16, 643–650.
Uterine luminal prostaglandin F in cycling mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlt1egtw%3D%3D&md5=3cff6adf2f858dbc147e8c650fa11455CAS | 725092PubMed |