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Center for Animal Biotechnology and Genomics, Albert B. Alkek Institute of Biosciences and Technology, Texas A&M University System Health Science Center, and Department of Animal Science, Texas A&M University (T.E.S., A.G.S., M.M.J., F.W.B.), College Station, Texas 77843-2471; the Department of Urology, M.D. Anderson Cancer Center, University of Texas (C.A.W., G.J.), Houston, Texas 77030-4095; and the Department of Animal and Dairy Science, Auburn University (A.A.W., F.F.B.), Auburn, Alabama 36849-5415
Address all correspondence and requests for reprints to: Dr. Thomas E. Spencer, Center for Animal Biotechnology and Genomics, 444 Kleberg Center, Texas A&M University, College Station, Texas 77843-2471. E-mail: tspencer{at}ansc.tamu.edu
Prolonged exposure of the developing neonatal ovine uterus to a progestin from birth prevents uterine gland development and creates an adult endometrial phenotype characterized by the absence of glandular epithelium, the uterine gland knockout (UGKO) phenotype. This study used endometrium from normal and UGKO sheep to identify messenger RNAs (mRNAs) expressed differentially in the endometrial epithelium using the molecular techniques of mRNA differential display PCR (DD-PCR) and suppression subtractive complementary DNA (cDNA) hybridization (SSH). Sequence analyses of DD- and SSH-identified and cloned cDNAs indicated similarity of some to known mRNAs, including ß-lactoglobulin, alkaline phosphatase, type B and D endogenous sheep retroviruses, gp330/megalin, matrix Gla protein, and others. Other cDNAs were not similar to any known sequences and are considered novel, although some of these match human expressed sequence tags. In situ hybridization analyses of uteri from cyclic and pregnant ewes indicated that all DD-PCR- and SSH-identified mRNAs were expressed in either the endometrial lumenal and/or glandular epithelium, although some were also expressed in other uterine cell types. Northern and in situ hybridization analyses revealed that patterns of mRNA expression for most clones were affected by the day of the estrous cycle and pregnancy in a manner consistent with regulation by progesterone. Studies demonstrate the utility of the ovine UGKO model as a tool with which to identify known and novel uterine epithelial-specific genes. Cloned cDNAs identified here are expressed sequence tags useful for comparative and physical genetic mapping and may be used to reveal new factors and pathways regulating endometrial function.
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  M. C. Satterfield, G. Song, K. J. Kochan, P. K. Riggs, R. M. Simmons, C. G. Elsik, D. L. Adelson, F. W. Bazer, H. Zhou, and T. E. Spencer Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation Physiol Genomics, October 1, 2009; 39(2): 85 - 99. [Abstract] [Full Text] [PDF]
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 R. M. Simmons, D. W. Erikson, J. Kim, R. C. Burghardt, F. W. Bazer, G. A. Johnson, and T. E. Spencer Insulin-Like Growth Factor Binding Protein-1 in the Ruminant Uterus: Potential Endometrial Marker and Regulator of Conceptus Elongation Endocrinology, September 1, 2009; 150(9): 4295 - 4305. [Abstract] [Full Text] [PDF]
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 J. F Trott, K. C Horigan, J. M Gloviczki, K. M Costa, B. A Freking, C. Farmer, K. Hayashi, T. Spencer, J. E Morabito, and R. C Hovey Tissue-specific regulation of porcine prolactin receptor expression by estrogen, progesterone, and prolactin J. Endocrinol., July 1, 2009; 202(1): 153 - 166. [Abstract] [Full Text] [PDF]
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 H. Gao, G. Wu, T. E. Spencer, G. A. Johnson, and F. W. Bazer Select Nutrients in the Ovine Uterine Lumen. V. Nitric Oxide Synthase, GTP Cyclohydrolase, and Ornithine Decarboxylase in Ovine Uteri and Peri-Implantation Conceptuses Biol Reprod, July 1, 2009; 81(1): 67 - 76. [Abstract] [Full Text] [PDF]
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H. Gao, G. Wu, T. E. Spencer, G. A. Johnson, and F. W. Bazer Select Nutrients in the Ovine Uterine Lumen. VI. Expression of FK506-Binding Protein 12-Rapamycin Complex-Associated Protein 1 (FRAP1) and Regulators and Effectors of mTORC1 and mTORC2 Complexes in Ovine Uteri and Conceptuses Biol Reprod, July 1, 2009; 81(1): 87 - 100. [Abstract] [Full Text] [PDF]
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H. Gao, G. Wu, T. E. Spencer, G. A. Johnson, and F. W. Bazer Select Nutrients in the Ovine Uterine Lumen. IV. Expression of Neutral and Acidic Amino Acid Transporters in Ovine Uteri and Peri-Implantation Conceptuses Biol Reprod, June 1, 2009; 80(6): 1196 - 1208. [Abstract] [Full Text] [PDF]
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K. Hayashi, D. W. Erikson, S. A. Tilford, B. M. Bany, J. A. Maclean II, E. B. Rucker III, G. A. Johnson, and T. E. Spencer Wnt Genes in the Mouse Uterus: Potential Regulation of Implantation Biol Reprod, May 1, 2009; 80(5): 989 - 1000. [Abstract] [Full Text] [PDF]
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 S. Bauersachs, S. E. Ulbrich, V. Zakhartchenko, M. Minten, M. Reichenbach, H.-D. Reichenbach, H. Blum, T. E. Spencer, and E. Wolf The endometrium responds differently to cloned versus fertilized embryos PNAS, April 7, 2009; 106(14): 5681 - 5686. [Abstract] [Full Text] [PDF]
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H. Gao, G. Wu, T. E. Spencer, G. A. Johnson, and F. W. Bazer Select Nutrients in the Ovine Uterine Lumen. III. Cationic Amino Acid Transporters in the Ovine Uterus and Peri-Implantation Conceptuses Biol Reprod, March 1, 2009; 80(3): 602 - 609. [Abstract] [Full Text] [PDF]
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H. Gao, G. Wu, T. E. Spencer, G. A. Johnson, and F. W. Bazer Select Nutrients in the Ovine Uterine Lumen. II. Glucose Transporters in the Uterus and Peri-Implantation Conceptuses Biol Reprod, January 1, 2009; 80(1): 94 - 104. [Abstract] [Full Text] [PDF]
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M. C. Satterfield, K. Hayashi, G. Song, S. G. Black, F. W. Bazer, and T. E. Spencer Progesterone Regulates FGF10, MET, IGFBP1, and IGFBP3 in the Endometrium of the Ovine Uterus Biol Reprod, December 1, 2008; 79(6): 1226 - 1236. [Abstract] [Full Text] [PDF]
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 E. van Esch, J. M. Cline, E. Buse, and G. F. Weinbauer The Macaque Endometrium, with Special Reference to the Cynomolgus Monkey (Macaca fascicularis) Toxicol Pathol, December 1, 2008; 36(7_suppl): 67S - 100S. [Abstract] [Full Text] [PDF]
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K. A. Dunlap, D. W. Erikson, R. C. Burghardt, F. J. White, K. M. Reed, J. L. Farmer, T. E. Spencer, R. R. Magness, F. W. Bazer, K. J. Bayless, et al. Progesterone and Placentation Increase Secreted Phosphoprotein One (SPP1 or Osteopontin) in Uterine Glands and Stroma for Histotrophic and Hematotrophic Support of Ovine Pregnancy Biol Reprod, November 1, 2008; 79(5): 983 - 990. [Abstract] [Full Text] [PDF]
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G. Song, M. C. Satterfield, J. Kim, F. W. Bazer, and T. E. Spencer Gastrin-Releasing Peptide (GRP) in the Ovine Uterus: Regulation by Interferon Tau and Progesterone Biol Reprod, August 1, 2008; 79(2): 376 - 386. [Abstract] [Full Text] [PDF]
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J. Kim, G. Song, H. Gao, J. L. Farmer, M. C. Satterfield, R. C. Burghardt, G. Wu, G. A. Johnson, T. E. Spencer, and F. W. Bazer Insulin-Like Growth Factor II Activates Phosphatidylinositol 3-Kinase-Protooncogenic Protein Kinase 1 and Mitogen-Activated Protein Kinase Cell Signaling Pathways, and Stimulates Migration of Ovine Trophectoderm Cells Endocrinology, June 1, 2008; 149(6): 3085 - 3094. [Abstract] [Full Text] [PDF]
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 T. E Spencer, O. Sandra, and E. Wolf Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches Reproduction, February 1, 2008; 135(2): 165 - 179. [Abstract] [Full Text] [PDF]
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S. K Lewis, J. L Farmer, R. C Burghardt, G. R Newton, G. A Johnson, D. L Adelson, F. W Bazer, and T. E Spencer Galectin 15 (LGALS15): A Gene Uniquely Expressed in the Uteri of Sheep and Goats that Functions in Trophoblast Attachment Biol Reprod, December 1, 2007; 77(6): 1027 - 1036. [Abstract] [Full Text] [PDF]
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M. C. Satterfield, K. A. Dunlap, K. Hayashi, R. C. Burghardt, T. E. Spencer, and F. W. Bazer Tight and Adherens Junctions in the Ovine Uterus: Differential Regulation by Pregnancy and Progesterone Endocrinology, August 1, 2007; 148(8): 3922 - 3931. [Abstract] [Full Text] [PDF]
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K. Hayashi, R. C. Burghardt, F. W. Bazer, and T. E. Spencer WNTs in the Ovine Uterus: Potential Regulation of Periimplantation Ovine Conceptus Development Endocrinology, July 1, 2007; 148(7): 3496 - 3506. [Abstract] [Full Text] [PDF]
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 P. R. Murcia, F. Arnaud, and M. Palmarini The Transdominant Endogenous Retrovirus enJS56A1 Associates with and Blocks Intracellular Trafficking of Jaagsiekte Sheep Retrovirus Gag J. Virol., February 15, 2007; 81(4): 1762 - 1772. [Abstract] [Full Text] [PDF]
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M. C. Satterfield, F. W. Bazer, and T. E. Spencer Progesterone Regulation of Preimplantation Conceptus Growth and Galectin 15 (LGALS15) in the Ovine Uterus Biol Reprod, August 1, 2006; 75(2): 289 - 296. [Abstract] [Full Text] [PDF]
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G. Song, T. E. Spencer, and F. W. Bazer Progesterone and Interferon-{tau} Regulate Cystatin C in the Endometrium Endocrinology, July 1, 2006; 147(7): 3478 - 3483. [Abstract] [Full Text] [PDF]
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K. Hayashi and T. E. Spencer WNT Pathways in the Neonatal Ovine Uterus: Potential Specification of Endometrial Gland Morphogenesis by SFRP2 Biol Reprod, April 1, 2006; 74(4): 721 - 733. [Abstract] [Full Text] [PDF]
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C. A. Gray, C. A. Abbey, P. D. Beremand, Y. Choi, J. L. Farmer, D. L. Adelson, T. L. Thomas, F. W. Bazer, and T. E. Spencer Identification of Endometrial Genes Regulated by Early Pregnancy, Progesterone, and Interferon Tau in the Ovine Uterus Biol Reprod, February 1, 2006; 74(2): 383 - 394. [Abstract] [Full Text] [PDF]
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K. Hayashi and T. E. Spencer Estrogen Disruption of Neonatal Ovine Uterine Development: Effects on Gene Expression Assessed by Suppression Subtraction Hybridization Biol Reprod, October 1, 2005; 73(4): 752 - 760. [Abstract] [Full Text] [PDF]
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K. A. Dunlap, M. Palmarini, D. L. Adelson, and T. E. Spencer Sheep Endogenous Betaretroviruses (enJSRVs) and the Hyaluronidase 2 (HYAL2) Receptor in the Ovine Uterus and Conceptus Biol Reprod, August 1, 2005; 73(2): 271 - 279. [Abstract] [Full Text] [PDF]
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J. Hu and T. E. Spencer Carbonic Anhydrase Regulate Endometrial Gland Development in the Neonatal Uterus Biol Reprod, July 1, 2005; 73(1): 131 - 138. [Abstract] [Full Text] [PDF]
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 S Bauersachs, S E Ulbrich, K Gross, S E M Schmidt, H H D Meyer, R Einspanier, H Wenigerkind, M Vermehren, H Blum, F Sinowatz, et al. Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes J. Mol. Endocrinol., June 1, 2005; 34(3): 889 - 908. [Abstract] [Full Text] [PDF]
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K. Hayashi, K. D Carpenter, T. H Welsh Jr, R. C Burghardt, L. J Spicer, and T. E Spencer The IGF system in the neonatal ovine uterus Reproduction, March 1, 2005; 129(3): 337 - 347. [Abstract] [Full Text] [PDF]
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K. Y Lee and F. J DeMayo Animal models of implantation Reproduction, December 1, 2004; 128(6): 679 - 695. [Abstract] [Full Text] [PDF]
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J. Hu, X. Zhang, W. B. Nothnick, and T. E. Spencer Matrix Metalloproteinases and Their Tissue Inhibitors in the Developing Neonatal Mouse Uterus Biol Reprod, November 1, 2004; 71(5): 1598 - 1604. [Abstract] [Full Text] [PDF]
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M. Mura, P. Murcia, M. Caporale, T. E. Spencer, K. Nagashima, A. Rein, and M. Palmarini Late viral interference induced by transdominant Gag of an endogenous retrovirus PNAS, July 27, 2004; 101(30): 11117 - 11122. [Abstract] [Full Text] [PDF]
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J. Hu, C. A. Gray, and T. E. Spencer Gene Expression Profiling of Neonatal Mouse Uterine Development Biol Reprod, June 1, 2004; 70(6): 1870 - 1876. [Abstract] [Full Text] [PDF]
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C. A. Gray, D. L. Adelson, F. W. Bazer, R. C. Burghardt, E. N. T. Meeusen, and T. E. Spencer Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm PNAS, May 25, 2004; 101(21): 7982 - 7987. [Abstract] [Full Text] [PDF]
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 M. Palmarini, M. Mura, and T. E. Spencer Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation J. Gen. Virol., January 1, 2004; 85(1): 1 - 13. [Abstract] [Full Text] [PDF]
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 T. E. Spencer and F. W. Bazer Uterine and placental factors regulating conceptus growth in domestic animals J Anim Sci, January 1, 2004; 82(13_suppl): E4 - 13. [Abstract] [Full Text] [PDF]
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S. Kim, Y. Choi, F. W. Bazer, and T. E. Spencer Identification of Genes in the Ovine Endometrium Regulated by Interferon {tau} Independent of Signal Transducer and Activator of Transcription 1 Endocrinology, December 1, 2003; 144(12): 5203 - 5214. [Abstract] [Full Text] [PDF]
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J. Carlson, M. Lyon, J. Bishop, A. Vaiman, E. Cribiu, J.-F. Mornex, S. Brown, D. Knudson, J. DeMartini, and C. Leroux Chromosomal Distribution of Endogenous Jaagsiekte Sheep Retrovirus Proviral Sequences in the Sheep Genome J. Virol., September 1, 2003; 77(17): 9662 - 9668. [Abstract] [Full Text] [PDF]
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K. Hayashi, K. D. Carpenter, C. A. Gray, and T. E. Spencer The Activin-Follistatin System in the Neonatal Ovine Uterus Biol Reprod, September 1, 2003; 69(3): 843 - 850. [Abstract] [Full Text] [PDF]
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K. D. Carpenter, K. Hayashi, and T. E. Spencer Ovarian Regulation of Endometrial Gland Morphogenesis and Activin-Follistatin System in the Neonatal Ovine Uterus Biol Reprod, September 1, 2003; 69(3): 851 - 860. [Abstract] [Full Text] [PDF]
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K. D. Carpenter, C. A. Gray, T. M. Bryan, T. H. Welsh Jr., and T. E. Spencer Estrogen and Antiestrogen Effects on Neonatal Ovine Uterine Development Biol Reprod, August 1, 2003; 69(2): 708 - 717. [Abstract] [Full Text] [PDF]
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T. E. Spencer, M. Mura, C. A. Gray, P. J. Griebel, and M. Palmarini Receptor Usage and Fetal Expression of Ovine Endogenous Betaretroviruses: Implications for Coevolution of Endogenous and Exogenous Retroviruses J. Virol., December 6, 2002; 77(1): 749 - 753. [Abstract] [Full Text] [PDF]
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A. Alberti, C. Murgia, S.-L. Liu, M. Mura, C. Cousens, M. Sharp, A. D. Miller, and M. Palmarini Envelope-Induced Cell Transformation by Ovine Betaretroviruses J. Virol., May 3, 2002; 76(11): 5387 - 5394. [Abstract] [Full Text] [PDF]
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M. Palmarini, C. A. Gray, K. Carpenter, H. Fan, F. W. Bazer, and T. E. Spencer Expression of Endogenous Betaretroviruses in the Ovine Uterus: Effects of Neonatal Age, Estrous Cycle, Pregnancy, and Progesterone J. Virol., December 1, 2001; 75(23): 11319 - 11327. [Abstract] [Full Text]
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 M. Palmarini and H. Fan Retrovirus-Induced Ovine Pulmonary Adenocarcinoma, an Animal Model for Lung Cancer J Natl Cancer Inst, November 7, 2001; 93(21): 1603 - 1614. [Abstract] [Full Text] [PDF]
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C. A. Gray, F. F. Bartol, B. J. Tarleton, A. A. Wiley, G. A. Johnson, F. W. Bazer, and T. E. Spencer Developmental Biology of Uterine Glands Biol Reprod, November 1, 2001; 65(5): 1311 - 1323. [Abstract] [Full Text] [PDF]
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C. A. Gray, K. M. Taylor, W. S. Ramsey, J. R. Hill, F. W. Bazer, F. F. Bartol, and T. E. Spencer Endometrial Glands Are Required for Preimplantation Conceptus Elongation and Survival Biol Reprod, June 1, 2001; 64(6): 1608 - 1613. [Abstract] [Full Text]
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K. M. Taylor, C. Chen, C. A. Gray, F. W. Bazer, and T. E. Spencer Expression of Messenger Ribonucleic Acids for Fibroblast Growth Factors 7 and 10, Hepatocyte Growth Factor, and Insulin-Like Growth Factors and Their Receptors in the Neonatal Ovine Uterus Biol Reprod, April 1, 2001; 64(4): 1236 - 1246. [Abstract] [Full Text]
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C. A. Gray, F. W. Bazer, and T. E. Spencer Effects of Neonatal Progestin Exposure on Female Reproductive Tract Structure and Function in the Adult Ewe Biol Reprod, March 1, 2001; 64(3): 797 - 804. [Abstract] [Full Text]
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M. Palmarini, C. Hallwirth, D. York, C. Murgia, T. de Oliveira, T. Spencer, and H. Fan Molecular Cloning and Functional Analysis of Three Type D Endogenous Retroviruses of Sheep Reveal a Different Cell Tropism from That of the Highly Related Exogenous Jaagsiekte Sheep Retrovirus J. Virol., September 1, 2000; 74(17): 8065 - 8076. [Abstract] [Full Text]
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C. Chen, T. E. Spencer, and F. W. Bazer Fibroblast Growth Factor-10: A Stromal Mediator of Epithelial Functionin the Ovine Uterus Biol Reprod, September 1, 2000; 63(3): 959 - 966. [Abstract] [Full Text]
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M. D. Stewart, G. A. Johnson, C. A. Gray, R. C. Burghardt, L. A. Schuler, M. M. Joyce, F. W. Bazer, and T. E. Spencer Prolactin Receptor and Uterine Milk Protein Expression in the Ovine Endometrium During the Estrous Cycle and Pregnancy Biol Reprod, June 1, 2000; 62(6): 1779 - 1789. [Abstract] [Full Text]
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K. M. Taylor, C. A. Gray, M. M. Joyce, M. D. Stewart, F. W. Bazer, and T. E. Spencer Neonatal Ovine Uterine Development Involves Alterations in Expression of Receptors for Estrogen, Progesterone, and Prolactin Biol Reprod, April 1, 2000; 63(4): 1192 - 1204. [Abstract] [Full Text]
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C. Allison Gray, F. F. Bartol, K. M. Taylor, A. A. Wiley, W. S. Ramsey, T. L. Ott, F. W. Bazer, and T. E. Spencer Ovine Uterine Gland Knock-Out Model: Effects of Gland Ablation on the Estrous Cycle Biol Reprod, February 1, 2000; 62(2): 448 - 456. [Abstract] [Full Text]
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