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

Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses

Thomas E. Spencer A D , Greg A. Johnson B , Fuller W. Bazer A B , Robert C. Burghardt B and Massimo Palmarini C

A Center for Animal Biotechnology and Genomics, Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.

B Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843, USA.

C Institute of Comparative Medicine, University of Glasgow Veterinary School, Scotland, UK.

D Corresponding author. Email:

Reproduction, Fertility and Development 19(1) 65-78
Published: 12 December 2006


The present review highlights new information on pregnancy recognition and conceptus development and implantation in sheep with respect to regulation by progesterone, interferons and endogenous retroviruses. After formation of the corpus luteum, progesterone acts on the endometrium and stimulates blastocyst growth and elongation to a filamentous conceptus (embryo/fetus and associated extra-embryonic membranes). The envelope of endogenous retroviruses related to Jaagsiekte sheep retroviruses appears to intrinsically regulate mononuclear trophectoderm cell proliferation and differentiation into trophoblast giant binucleate cells. The mononuclear trophectoderm cells of elongating sheep conceptuses secrete interferon-τ, which acts on the endometrium to prevent development of the luteolytic mechanism by inhibiting transcription of the gene for the oestrogen receptor α in the luminal and superficial ductal glandular epithelia. These actions prevent oestrogen-induced transcription of the oxytocin receptor gene and, therefore, oxytocin-induced luteolytic pulses of prostaglandin F. Progesterone downregulation of its receptors in luminal and glandular epithelia correlates temporally with a reduction in anti-adhesive mucin 1and induction of secreted galectin 15 (LGALS15) and secreted phosphoprotein 1, which are proposed to regulate trophectoderm proliferation and adhesion. Interferon-τ acts on the endometrial lumenal epithelium to induce WNT7A and to stimulate LGALS15, cathepsin L and cystatin C, which are candidate regulators of conceptus development and implantation. The number of potential contributors to maternal recognition and establishment of pregnancy continues to grow and this highlights our limited appreciation of the complexity of the key molecules and signal transduction pathways that intersect during these key developmental processes. The goal of improving reproductive efficiency by preventing embryonic losses that occur during the peri-implantation period of pregnancy in domestic ruminants provides the challenge to increase our knowledge of endometrial function and conceptus development.

Additional keywords: endogenous viruses related to Jaagsiekte sheep retroviruses, uterus.


Afonso S.Romagnano L.Babiarz B.1997The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation.Development12434153425Pubmed Abstract

Aplin J. D.1997Adhesion molecules in implantation.Rev. Reprod.28493doi:10.1530/ROR.0.0020084Pubmed Abstract

Ashworth C. J.Bazer F. W.1989Changes in ovine conceptus and endometrial function following asynchronous embryo transfer or administration of progesterone.Biol. Reprod.40425433doi:10.1095/BIOLREPROD40.2.425Pubmed Abstract

Bazer F. W.1975Uterine protein secretions: relationship to development of the conceptus.J. Anim. Sci.4113761382Pubmed Abstract

Bazer F. W.Roberts R. M.Thatcher W. W.1979Actions of hormones on the uterus and effect on conceptus development.J. Anim. Sci.493545Pubmed Abstract

Bazer F. W.Thatcher W. W.Hansen P. J.Mirando M. A.Ott T. L.Plante C.1991Physiological mechanisms of pregnancy recognition in ruminants.J. Reprod. Fertil. Suppl.433947Pubmed Abstract

Bazer F. W.Spencer T. E.Ott T. L.1997Interferon tau: a novel pregnancy recognition signal.Am. J. Reprod. Immunol.37412420Pubmed Abstract

Bock M.Stoye J. P.2000Endogenous retroviruses and the human germline.Curr. Opin. Genet. Dev.10651655doi:10.1016/S0959-437X(00)00138-6Pubmed Abstract

Boeke J. D., and Stoye J. P. (1997). Retrotransposons, endogenous retroviruses and the evolution of retroelements. In ‘Retroviruses’. (Eds J. M. Coffin, S. H. Hughes and H. E. Varmus.) pp. 343–346. (Cold Spring Harbor Laboratory Press: Plainview, NY.)

Brayman M.Thathiah A.Carson D. D.2004MUC1: A multifunctional cell surface component of reproductive tissue epithelia.Reprod. Biol. Endocrinol.24doi:10.1186/1477-7827-2-4Pubmed Abstract

Burghardt R. C.Johnson G. A.Jaeger L. A.Ka H.Garlow J. E.Spencer T. E.Bazer F. W.2002Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals.Cells Tissues Organs172202217doi:10.1159/000066969

Cammas L.Reinaud P.Dubois O.Bordas N.Germain G.Charpigny G.2005Identification of differentially regulated genes during elongation and early implantation in the ovine trophoblast using complementary DNA array screening.Biol. Reprod.72960967doi:10.1095/BIOLREPROD.104.034801Pubmed Abstract

Carson D. D.Bagchi I.Dey S. K.Enders A. C.Fazleabas A. T.Lessey B. A.Yoshinaga K.2000Embryo implantation.Dev. Biol.223217237doi:10.1006/DBIO.2000.9767Pubmed Abstract

Charpigny G.Reinaud P.Tamby J. P.Creminon C.Martal J.Maclouf J.Guillomot M.1997Expression of cyclooxygenase-1 and -2 in ovine endometrium during the estrous cycle and early pregnancy.Endocrinology13821632171doi:10.1210/EN.138.5.2163Pubmed Abstract

Choi Y.Johnson G. A.Burghardt R. C.Berghman L. R.Joyce M. M.Taylor K. M.Stewart M. D.Bazer F. W.Spencer T. E.2001Interferon regulatory factor-two restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus.Biol. Reprod.6510381049doi:10.1095/BIOLREPROD65.4.1038Pubmed Abstract

Choi Y.Johnson G. A.Spencer T. E.Bazer F. W.2003Pregnancy and interferon tau regulate MHC class I and β-2-microglobulin expression in the ovine uterus.Biol. Reprod.6817031710doi:10.1095/BIOLREPROD.102.012708Pubmed Abstract

Degrelle S. A.Campion E.Cabau C.Piumi F.Reinaud P.Richard C.Renard J. P.Hue I.2005Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts.Dev. Biol.288448460doi:10.1016/J.YDBIO.2005.09.043Pubmed Abstract

DeMartini J. C.Carlson J. O.Leroux C.Spencer T.Palmarini M.2003Endogenous retroviruses related to Jaagsiekte sheep retrovirus.Curr. Top. Microbiol. Immunol.275117137Pubmed Abstract

Dunlap K. A.Palmarini M.Adelson D. L.Spencer T. E.2005Sheep endogenous betaretroviruses (enJSRVs) and the hyaluronidase 2 (HYAL2) receptor in the ovine uterus and conceptus.Biol. Reprod.73271279doi:10.1095/BIOLREPROD.105.039776Pubmed Abstract

Dunlap K. A.Palmarini M.Spencer T. E.2006aOvine endogenous betaretroviruses (enJSRVs) and placental morphogenesis.Placenta27Suppl. AS135S140doi:10.1016/J.PLACENTA.2005.12.009

Dunlap K. A.Palmarini M.Varela M.Burghardt R. C.Hayashi K.Farmer J. L.Spencer T. E2006bEndogenous retroviruses regulate peri-implantation placental growth and differentiation.Proc. Natl Acad. Sci. USA10314 39014 395

Dupressoir A.Marceau G.Vernochet C.Benit L.Kanellopoulos C.Sapin V.Heidmann T.2005Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae.Proc. Natl Acad. Sci. USA102725730
doi:10.1073/PNAS.0406509102Pubmed Abstract

Farin C. E.Imakawa K.Roberts R. M.1989In situ localization of mRNA for the interferon, ovine trophoblast protein-1, during early embryonic development of the sheep.Mol. Endocrinol.310991107Pubmed Abstract

Flechon J. E.Guillomot M.Charlier M.Flechon B.Martal J.1986Experimental studies on the elongation of the ewe blastocyst.Reprod. Nutr. Dev.2610171024Pubmed Abstract

Fleming J. A.Choi Y.Johnson G. A.Spencer T. E.Bazer F. W.2001Cloning of the ovine estrogen receptor-alpha promoter and functional regulation by ovine interferon-tau.Endocrinology14228792887doi:10.1210/EN.142.7.2879Pubmed Abstract

Fleming J. G.Spencer T. E.Safe S. H.Bazer F. W.2006Estrogen regulates transcription of the ovine oxytocin receptor gene through GC-rich SP1 promoter elements.Endocrinology147899911doi:10.1210/EN.2005-1120Pubmed Abstract

Garrett J. E.Geisert R. D.Zavy M. T.Gries L. K.Wettemann R. P.Buchanan D. S.1988Effect of exogenous progesterone on prostaglandin F2α release and the interestrous interval in the bovine.Prostaglandins368596doi:10.1016/0090-6980(88)90104-9Pubmed Abstract

Geisert R. D.Morgan G. L.Short E. C.JrZavy M. T.1992Endocrine events associated with endometrial function and conceptus development in cattle.Reprod. Fertil. Dev.4301305doi:10.1071/RD9920301Pubmed Abstract

Genbacev O. D.Prakobphol A.Foulk R. A.Krtolica A. R.Ilic al.2003Trophoblast L-selectin-mediated adhesion at the maternal–fetal interface.Science299405408doi:10.1126/SCIENCE.1079546Pubmed Abstract

Giancotti F. G.Ruoslahti E.1999Integrin signaling.Science28510281032doi:10.1126/SCIENCE.285.5430.1028Pubmed Abstract

Gray C. A.Taylor K. M.Ramsey W. S.Hill J. R.Bazer F. W.Bartol F. F.Spencer T. E.2001Endometrial glands are required for preimplantation conceptus elongation and survival.Biol. Reprod.6416081613doi:10.1095/BIOLREPROD64.6.1608Pubmed Abstract

Gray C. A.Burghardt R. C.Johnson G. A.Bazer F. W.Spencer T. E.2002Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation.Reproduction124289300doi:10.1530/REP.0.1240289Pubmed Abstract

Gray C. A.Adelson D. L.Bazer F. W.Burghardt R. C.Meeusen E. N.Spencer T. E.2004Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm.Proc. Natl Acad. Sci. USA10179827987doi:10.1073/PNAS.0402669101Pubmed Abstract

Gray C. A.Abbey C. A.Beremand P. D.Choi Y.Farmer J. L.Adelson D. L.Thomas T. L.Bazer F. W.Spencer T. E.2006Identification of endometrial genes regulated by early pregnancy, progesterone, and interferon tau in the ovine uterus.Biol. Reprod.74383394doi:10.1095/BIOLREPROD.105.046656Pubmed Abstract

Guillomot M.1995Cellular interactions during implantation in domestic ruminants.J. Reprod. Fertil. Suppl.493951Pubmed Abstract

Guillomot M.Michel C.Gaye P.Charlier N.Trojan J.Martal J.1990Cellular localization of an embryonic interferon, ovine trophoblastin and its mRNA in sheep embryos during early pregnancy.Biol. Cell.68205211doi:10.1016/0248-4900(90)90309-QPubmed Abstract

Hansen T. R.Austin K. J.Perry D. J.Pru J. K.Teixeira M. G.Johnson G. A.1999Mechanism of action of interferon-tau in the uterus during early pregnancy.J. Reprod. Fertil.54329339

Harris J. R.1991The evolution of placental mammals.FEBS Lett.29534
doi:10.1016/0014-5793(91)81370-NPubmed Abstract

Harris J. R.1998Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance.Bioessays20307316doi:10.1002/(SICI)1521-1878(199804)20:4<307::AID-BIES7>3.0.CO;2-MPubmed Abstract

Heyman Y.Camous S.Fevre J.Meziou W.Martal J.1984Maintenance of the corpus luteum after uterine transfer of trophoblastic vesicles to cyclic cows and ewes.J. Reprod. Fertil.70533540Pubmed Abstract

Hwang S. T.Singer M. S.Giblin P. A.Yednock T. A.Bacon K. B.Simon S. I.Rosen S. D.1996GlyCAM-1, a physiologic ligand for L-selectin, activates beta 2 integrins on naive peripheral lymphocytes.J. Exp. Med.18413431348doi:10.1084/JEM.184.4.1343Pubmed Abstract

Imakawa K.Helmer S. D.Nephew K. P.Meka C. S.Christenson R. K.1993A novel role for GM-CSF: enhancement of pregnancy specific interferon production, ovine trophoblast protein-1.Endocrinology13218691871doi:10.1210/EN.132.4.1869Pubmed Abstract

Johnson G. A.Spencer T. E.Burghardt R. C.Bazer F. W.1999aOvine osteopontin: I. Cloning and expression of messenger ribonucleic acid in the uterus during the periimplantation period.Biol. Reprod.61884891doi:10.1095/BIOLREPROD61.4.884Pubmed Abstract

Johnson G. A.Spencer T. E.Hansen T. R.Austin K. J.Burghardt R. C.Bazer F. W.1999bExpression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus.Biol. Reprod.61312318doi:10.1095/BIOLREPROD61.1.312Pubmed Abstract

Johnson G. A.Austin K. J.Collins A. M.Murdoch W. J.Hansen T. R.1999cEndometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows.Endocrine10243252doi:10.1385/ENDO:10:1:43Pubmed Abstract

Johnson G. A.Spencer T. E.Burghardt R. C.Joyce M. M.Bazer F. W.2000aInterferon-tau and progesterone regulate ubiquitin cross-reactive protein expression in the ovine uterus.Biol. Reprod.62622627doi:10.1095/BIOLREPROD62.3.622Pubmed Abstract

Johnson G. A.Spencer T. E.Burghardt R. C.Taylor K. M.Gray C. A.Bazer F. W.2000bProgesterone modulation of osteopontin gene expression in the ovine uterus.Biol. Reprod.6213151321doi:10.1095/BIOLREPROD62.5.1315Pubmed Abstract

Johnson G. A.Bazer F. W.Jaeger L. A.Ka H.Garlow J. E.Pfarrer C.Spencer T. E.Burghardt R. C.2001aMuc-1, integrin, and osteopontin expression during the implantation cascade in sheep.Biol. Reprod.65820828doi:10.1095/BIOLREPROD65.3.820Pubmed Abstract

Johnson G. A.Stewart M. D.Gray C. A.Choi Y.Burghardt R. C.Yu-Lee L. Y.Bazer F. W.Spencer T. E.2001bEffects of the estrous cycle, pregnancy, and interferon tau on 2′,5′-oligoadenylate synthetase expression in the ovine uterus.Biol. Reprod.6413921399doi:10.1095/BIOLREPROD64.5.1392Pubmed Abstract

Johnson G. A.Burghardt R. C.Bazer F. W.Spencer T. E.2003Osteopontin: roles in implantation and placentation.Biol. Reprod.6914581471doi:10.1095/BIOLREPROD.103.020651Pubmed Abstract

Kazemi M.Amann J. F.Keisler D. H.Ing N. H.Roberts R. M.Morgan G.Wooding F. B.1990A progesterone-modulated, low-molecular-weight protein from the uterus of the sheep is associated with crystalline inclusion bodies in uterine epithelium and embryonic trophectoderm.Biol. Reprod.438096doi:10.1095/BIOLREPROD43.1.80Pubmed Abstract

Kim S.Choi Y.Bazer F. W.Spencer T. E.2003aIdentification of genes in the ovine endometrium regulated by interferon tau independent of signal transducer and activator of transcription 1.Endocrinology14452035214doi:10.1210/EN.2003-0665Pubmed Abstract

Kim S.Choi Y.Spencer T. E.Bazer F. W.2003bEffects of the estrous cycle, pregnancy and interferon tau on expression of cyclooxygenase two (COX-2) in ovine endometrium.Reprod. Biol. Endocrinol.158doi:10.1186/1477-7827-1-58Pubmed Abstract

Kleemann D. O.Walker S. K.Seamark R. F.1994Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy.J. Reprod. Fertil.102411417Pubmed Abstract

Klein C.Bauersachs S.Ulbrich S. E.Einspanier R.Meyer H. al.2006Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the pre-attachment period.Biol. Reprod.74253264doi:10.1095/BIOLREPROD.105.046748Pubmed Abstract

Ko Y.Lee C. Y.Ott T. L.Davis M. A.Simmen R. C.Bazer F. W.Simmen F. A.1991Insulin-like growth factors in sheep uterine fluids: concentrations and relationship to ovine trophoblast protein-1 production during early pregnancy.Biol. Reprod.45135142doi:10.1095/BIOLREPROD45.1.135Pubmed Abstract

Lasky L. A.Singer M. S.Dowbenko D.Imai Y.Henzel W. al.1992An endothelial ligand for L-selectin is a novel mucin-like molecule.Cell69927938doi:10.1016/0092-8674(92)90612-GPubmed Abstract

Lawson R. A.Parr R. A.Cahill L. P.1983Evidence for maternal control of blastocyst growth after asynchronous transfer of embryos to the uterus of the ewe.J. Reprod. Fertil.67477483Pubmed Abstract

Lee R. S.Wheeler T. T.Peterson A. J.1998Large-format, two-dimensional polyacrylamide gel electrophoresis of ovine periimplantation uterine luminal fluid proteins: identification of aldose reductase, cytoplasmic actin, and transferrin as conceptus-synthesized proteins.Biol. Reprod.59743752doi:10.1095/BIOLREPROD59.4.743Pubmed Abstract

Lower R.Lower J.Kurth R.1996The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences.Proc. Natl Acad. Sci. USA9351775184doi:10.1073/PNAS.93.11.5177Pubmed Abstract

Mann G. E.Lamming G. E.1999The influence of progesterone during early pregnancy in cattle.Reprod. Domest. Anim.34269274

Mann G. E.Lamming G. E.2001Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows.Reproduction121175180
doi:10.1530/REP.0.1210175Pubmed Abstract

Mann G. E.Fray M. D.Lamming G. E.2006Effects of time of progesterone supplementation on embryo development and interferon-tau production in the cow.Vet. J.171500503doi:10.1016/J.TVJL.2004.12.005Pubmed Abstract

McCracken J. A.Custer E. E.Lamsa J. C.1999Luteolysis: a neuroendocrine-mediated event.Physiol. Rev.79263323Pubmed Abstract

Mi S.Lee X.Li X.Veldman G. M.Finnerty al.2000Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis.Nature403785789doi:10.1038/35001608Pubmed Abstract

Michael D. D.Alvarez I. M.Ocon O. M.Powell A. M.Talbot N. C.Johnson S. E.Ealy A. D.2006Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm.Endocrinology14735713579doi:10.1210/EN.2006-0234Pubmed Abstract

Mohamed O. A.Jonnaert M.Labelle-Dumais C.Kuroda K.Clarke H. J.Dufort D.2005Uterine Wnt/β-catenin signaling is required for implantation.Proc. Natl Acad. Sci. USA10285798584doi:10.1073/PNAS.0500612102Pubmed Abstract

Muir A.Lever A.Moffett A.2004Expression and functions of human endogenous retroviruses in the placenta: an update.Placenta25Suppl. AS16S25doi:10.1016/J.PLACENTA.2004.01.012Pubmed Abstract

Nephew K. P.McClure K. E.Ott T. L.Dubois D. H.Bazer F. W.Pope W. F.1991Relationship between variation in conceptus development and differences in estrous cycle duration in ewes.Biol. Reprod.44536539doi:10.1095/BIOLREPROD44.3.536Pubmed Abstract

Palmarini M.Fan H.2001Retrovirus-induced ovine pulmonary adenocarcinoma, an animal model for lung cancer.J. Natl Cancer Inst.9316031614Pubmed Abstract

Palmarini M.Gray C. A.Carpenter K.Fan H.Bazer F. W.Spencer T. E.2001Expression of endogenous betaretroviruses in the ovine uterus: effects of neonatal age, estrous cycle, pregnancy, and progesterone.J. Virol.7511 31911 327doi:10.1128/JVI.75.23.11319-11327.2001Pubmed Abstract

Palmarini M.Mura M.Spencer T. E.2004Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation.J. Gen. Virol.85113doi:10.1099/VIR.0.19547-0Pubmed Abstract

Prudhomme S.Bonnaud B.Mallet F.2005Endogenous retroviruses and animal reproduction.Cytogenet. Genome Res.110353364doi:10.1159/000084967Pubmed Abstract

Rai S. K.DeMartini J. C.Miller A. D.2000Retrovirus vectors bearing Jaagsiekte sheep retrovirus Env transduce human cells by using a new receptor localized to chromosome 3p21.3.J. Virol.7446984704doi:10.1128/JVI.74.10.4698-4704.2000Pubmed Abstract

Roberts R. M.Ealy A. D.Alexenko A. P.Han C. S.Ezashi T.1999Trophoblast interferons.Placenta20259264doi:10.1053/PLAC.1998.0381Pubmed Abstract

Rosen S. D.1993Ligands for L-selectin: where and how many?Res. Immunol.144699703doi:10.1016/S0923-2494(93)80054-3Pubmed Abstract

Rosenfeld C. S.Han C. S.Alexenko A. P.Spencer T. E.Roberts R. M.2002Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus.Biol. Reprod.67847853doi:10.1095/BIOLREPROD.102.004267Pubmed Abstract

Rote N. S.Chakrabarti S.Stetzer B. P.2004The role of human endogenous retroviruses in trophoblast differentiation and placental development.Placenta25673683doi:10.1016/J.PLACENTA.2004.02.008Pubmed Abstract

Satterfield M. C.Bazer F. W.Spencer T. E.2006Progesterone regulation of pre-implantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus.Biol. Reprod.75289296doi:10.1095/BIOLREPROD.106.052944

Sodek J.Ganss B.McKee M. D.2000Osteopontin.Crit. Rev. Oral Biol. Med.11279303Pubmed Abstract

Song G.Spencer T. E.Bazer F. W.2005Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau.Endocrinology14648254833doi:10.1210/EN.2005-0768Pubmed Abstract

Song G.Spencer T. E.Bazer F. W.2006Progesterone and interferon tau regulate cystatin C (CST3) in the endometrium.Endocrinology14734783483doi:10.1210/EN.2006-0122

Spencer T. E.Bazer F. W.2002Biology of progesterone action during pregnancy recognition and maintenance of pregnancy.Front. Biosci.718791898

Spencer T. E.Bazer F. W.2004Conceptus signals for establishment and maintenance of pregnancy.Reprod. Biol. Endocrinol.249
doi:10.1186/1477-7827-2-49Pubmed Abstract

Spencer T. E.Bartol F. F.Bazer F. W.Johnson G. A.Joyce M. M.1999aIdentification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus.Biol. Reprod.60241250doi:10.1095/BIOLREPROD60.2.241Pubmed Abstract

Spencer T. E.Gray A.Johnson G. A.Taylor K. M.Gertler A.Gootwine E.Ott T. L.Bazer F. W.1999bEffects of recombinant ovine interferon tau, placental lactogen, and growth hormone on the ovine uterus.Biol. Reprod.6114091418doi:10.1095/BIOLREPROD61.6.1409Pubmed Abstract

Spencer T. E.Stagg A. G.Joyce M. M.Jenster G.Wood C. G.Bazer F. W.Wiley A. A.Bartol F. F.1999cDiscovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model.Endocrinology14040704080doi:10.1210/EN.140.9.4070Pubmed Abstract

Spencer T. E.Mura M.Gray C. A.Griebel P. J.Palmarini M.2003Receptor usage and fetal expression of ovine endogenous betaretroviruses: implications for coevolution of endogenous and exogenous retroviruses.J. Virol.77749753doi:10.1128/JVI.77.1.749-753.2003Pubmed Abstract

Spencer T. E.Burghardt R. C.Johnson G. A.Bazer F. W.2004aConceptus signals for establishment and maintenance of pregnancy.Anim. Reprod. Sci.82–83537550doi:10.1016/J.ANIREPROSCI.2004.04.014Pubmed Abstract

Spencer T. E.Johnson G. A.Bazer F. W.Burghardt R. C.2004bImplantation mechanisms: insights from the sheep.Reproduction128657668doi:10.1530/REP.1.00398Pubmed Abstract

Spencer T. E.Johnson G. A.Burghardt R. C.Bazer F. W.2004cProgesterone and placental hormone actions on the uterus: insights from domestic animals.Biol. Reprod.71210doi:10.1095/BIOLREPROD.103.024133Pubmed Abstract

Sreenan J. M.Diskin M. G.1983Early embryonic mortality in the cow: its relationship with progesterone concentration.Vet. Rec.112517521Pubmed Abstract

Stark G. R.Kerr I. M.Williams B. R.Silverman R. H.Schreiber R. D.1998How cells respond to interferons.Annu. Rev. Biochem.67227264doi:10.1146/ANNUREV.BIOCHEM.67.1.227Pubmed Abstract

Villarreal L. P.Villareal L. P.1997On viruses, sex, and motherhood.J. Virol.71859865Pubmed Abstract

Wathes D. C.Lamming G. E.1995The oxytocin receptor, luteolysis and the maintenance of pregnancy.J. Reprod. Fertil. Suppl.495367Pubmed Abstract

Wooding F. B.1984Role of binucleate cells in fetomaternal cell fusion at implantation in the sheep.Am. J. Anat.170233250doi:10.1002/AJA.1001700208Pubmed Abstract

Wooding F. B.1992Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production.Placenta13101113Pubmed Abstract

Yang R. Y.Liu F. T.2003Galectins in cell growth and apoptosis.Cell. Mol. Life Sci.60267276doi:10.1007/S000180300022Pubmed Abstract

Export Citation