Pregnancy recognition signaling mechanisms in ruminants and pigs

Journal of Animal Science and Biotechnology

Volumn 4, Issue 1, 2013, Pages

  Bazer, Fuller W ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Estrogen; Interferon Tau; Pregnancy; Prostaglandin F2

Indexed keywords

EID: 84894556424     PISSN: 16749782     EISSN: 20491891     Source Type: Journal    
DOI: 10.1186/2049-1891-4-23     Document Type: Review

References (81)

1. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nature Rev Immunol 2005, 5:375-386.
2. Roberts RM, Ezashi T, Rosenfeld CS, Ealy AD, Kubisch HM. Evolution of the interferon tau genes and their promoters, and maternal-trophoblast interactions in control of their expression. Reprod Suppl 2003, 61:239-251.
3. Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod 2010, 16:135-152. 10.1093/molehr/gap095, 2816171, 19880575.
4. Cencič A, Guillomot M, Koren S, LaBonnariére C. Trophoblastic interferons: Do they modulate uterine cellular markers at the time of conceptus attachment in the pig?. Placenta 2003, 24:862-869. 10.1016/S0143-4004(03)00135-8, 13129683.
5. Cencič A, LaBonnardiėre C. Trophoblastic interferon-gamma: current knowledge and possible role(s) in early pig pregnancy. Vet Res 2002, 33:139-157. 10.1051/vetres:2002003, 11944804.
6. Peyman JA, Hammond GL. Localization of interferon-γ receptor in first trimester placenta to trophoblasts but lack of stimulation of HLA-DRA, -DRB, or invariant chain mRNA expression by interferon-γ. J Immunol 1992, 149:2675-2680.
7. Der SD, Zhou A, Williams BR, Silverman RH. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 1998, 95:15623-15628. 10.1073/pnas.95.26.15623, 28094, 9861020.
8. Darnell JE, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994, 264:1415-1421. 10.1126/science.8197455, 8197455.
9. Mamane Y, Heylbroeck C, Genin P, Algarte M, Servant MJ, LePage C, DeLuca C, Kwon H, Lin R, Hiscott J. Interferon regulatory factors: the next generation. Gene 1999, 237:1-14. 10.1016/S0378-1119(99)00262-0, 10524230.
10. Taniguchi T, Takaoka A. The interferon-[alpha]/[beta] system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors. Current Opinion Immunol 2002, 14:111-116.
11. Stewart MD, Johnson GA, Bazer FW, Spencer TE. Interferon-tau regulation of IFN-stimulated gene expression in cell lines lacking specific IFN-signaling components. Endocrinology 2001, 142:1786-1794. 10.1210/en.142.5.1786, 11316742.
12. Stewart MD, Choi Y, Johnson GA, Yu-Lee LY, Bazer FW, Spencer TE. Roles of Stat1, Stat2, and interferon regulatory factor-9 (IRF-9) in interferon tau regulation of IRF-1. Biol Reprod 2002, 66:393-400. 10.1095/biolreprod66.2.393, 11804954.
13. Joshi S, Kaur S, Kroczynska B, Platanias LC. Mechanisms of mRNA translation of interferon stimulated genes. Cytokine 2010, 52:123-127. 10.1016/j.cyto.2010.03.019, 20409730.
14. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004, 75:163-189.
15. Wilson ME, Lewis GS, Bazer FW. Proteins of ovine blastocyst origin 1979, 101A. Quebec, Canada: Proc Soc Study Reprod.
16. Lewis GS, Basha SMM, Bazer FW, Roberts RM, Thatcher WW. Proteins originating from bovine and porcine blastocysts 1979, 313. Tucson, AZ: Proc Amer Soc Anim Sci.
17. Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at Day 13-21. J Reprod Fert 1982, 65:141-150.
18. Godkin JD, Bazer FW, Thatcher WW, Roberts RM. Proteins released by cultured day 15-16 conceptuses prolong luteal maintenance when introduced into the uterine lumen of cyclic ewes. J Reprod Fertil 1984, 71:57-64. 10.1530/jrf.0.0710057, 6726688.
19. Martal J, Lacroix MC, Loudes C, Saunier M, Winterberger-Torres S. Trophoblastin, an antiluteolytic protein present in early pregnancy in sheep. J Reprod Fertil 1979, 56:63-73. 10.1530/jrf.0.0560063, 469859.
20. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM. Interferon-like sequences of ovine trophoblast protein secreted by embryonic trophectoderm. Nature 1987, 330:377-379. 10.1038/330377a0, 2446135.
21. Roberts RM. Interferon tau. Nature 1993, 362:583-584.
22. Pontzer CH, Torres BA, Vallet JL, Bazer FW, Johnson HM. Antiviral activity of the pregnancy recognition hormone ovine trophoblast protein-1. Biochem Biophys Res Commun 1988, 152:801-807. 10.1016/S0006-291X(88)80109-8, 3365252.
23. Pontzer CH, Ott TL, Bazer FW, Johnson HM. Localization of the antiviral site on the pregnancy recognition hormone, ovine trophoblast protein-one. Proc Nat Acad Sci USA 1990, 87:5945-5949. 10.1073/pnas.87.15.5945, 54446, 2165611.
24. Pontzer CH, Bazer FW, Johnson HM. Antiproliferative activity of a pregnancy recognition hormone, ovine trophoblast protein-1. Cancer Res 1991, 51:19-26.
25. Jarpe MA, Pontzer CH, Ott TL, Bazer FW, Johnson HM. Predicted structural motif of interferon tau. Protein Eng 1994, 7:863-867. 10.1093/protein/7.7.863, 7971949.
26. Ott TL, Heeke GV, Johnson HM, Bazer FW. Cloning and expression in S. Cerevisiae of a synthetic gene for the pregnancy recognition hormone ovine trophoblast protein-1: purification and antiviral activity. J Interferon Res 1991, 11:357-364. 10.1089/jir.1991.11.357, 1800584.
27. VanHeeke G, Ott TL, Strauss A, Ammaturo D, Bazer FW. High yield expression and secretion of the pregnancy recognition hormone ovine interferon-τ by Pichia pastoris. J Interferon Res 1996, 16:119-126.
28. Bazer FW, Spencer TE, Ott TL. Interferon tau: a novel pregnancy recognition signal. Am J Reprod Immunol 1997, 37:412-420. 10.1111/j.1600-0897.1997.tb00253.x, 9228295.
29. McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiol Rev 1999, 79:263-323.
30. Bazer FW, Spencer TE, Johnson GA. Interferons and uterine receptivity. Sem Reprod Med 2009, 27:90-102.
31. Bazer FW, Spencer TE, Johnson GA, Burghardt RC. Uterine receptivity to implantation of blastocysts in mammals. Frontiers in Biosci 2011, S3:745-767.
32. Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. Interferons and progesterone for establishment and maintenance of pregnancy: Interactions among novel cell signaling pathways. Reprod Biol 2008, 8:179-211. 10.1016/S1642-431X(12)60012-6, 19092983.
33. Newton GR, Ott TL, Woldesenbet S, Shelton AH, Bazer FW. Biochemical and immunological properties of related small ruminant trophoblast interferons. Theriogenology 1996, 46:703-716. 10.1016/0093-691X(96)00222-1, 16727936.
34. Thatcher WW, Hansen PJ, Gross TS, Helmer SD, Plante C, Bazer FW. Antiluteolytic effects of bovine trophoblast protein-1. J Reprod Fertil 1989, 37:91-99.
35. Meyer MD, Drost M, Ott TL, Bazer FW, Badinga L, Li J, Roberts RM, Hansen PJ, Thatcher WW. Recombinant bovine and ovine interferon tau extend corpus luteum lifespan and reduce uterine secretion of prostaglandin F2α in cattle. J Dairy Sci 1995, 78:1921-1931. 10.3168/jds.S0022-0302(95)76817-5, 8550901.
36. Dorniak P, Bazer FW, Spencer TE. Physiology and endocrinology symposium: biological role of interferon tau in endometrial function and conceptus elongation. J Anim Sci 2013, 91:1627-1638. 10.2527/jas.2012-5845, 23097402.
37. Alfaidy N, Li W, MacIntosh T, Yang K, Challis J. Late gestation increase in 11beta-hydroxysteroid dehydrogenase 1 expression in human fetal membranes: a novel intrauterine source of cortisol. J Clin Endocrinol Metab 2003, 88:5033-5038. 10.1210/jc.2002-021915, 14557491.
38. Alfaidy N, Xiong ZG, Myatt L, Lye SJ, MacDonald JF, Challis JR. Prostaglandin F2alpha potentiates cortisol production by stimulating 11beta-hydroxysteroid dehydrogenase 1: a novel feedback loop that may contribute to human labor. J Clin Endocrinol Metab 2001, 86:5585-5592. 10.1210/jc.86.11.5585, 11701739.
39. Boomsma CM, Keay SD, Macklon NS. Peri-implantation glucocorticoid administration for assisted reproductive technology cycles. Cochrane Database Syst Rev 2007, CD005996.
40. Quenby S, Kalumbi C, Bates M, Farquharson R, Vince G. Prednisolone reduces preconceptual endometrial natural killer cells in women with recurrent miscarriage. Fertil Steril 2005, 84:980-984. 10.1016/j.fertnstert.2005.05.012, 16213853.
41. Spencer TE, Bazer FW. Biology of progesterone action during pregnancy recognition and maintenance of pregnancy. Front Biosci 2002, 7:d1879-d1898. 10.2741/spencer, 12161340.
42. Wimsatt WA. New histological observations on the placenta of the sheep. Am J Anat 1950, 87:391-436. 10.1002/aja.1000870304, 14789741.
43. Guillomot M. Cellular interactions during implantation in domestic ruminants. J Reprod Fertil 1995, 49:39-51.
44. Bazer FW, Spencer TE, Thatcher WW. Growth and development of the ovine conceptus. J Anim Sci 2012, 90:159-170. 10.2527/jas.2011-4180, 21841083.
45. Stewart DM, Johnson GA, Gray CA, Schuler LA, Burghardt RC, Joyce MM, Bazer FW, Spencer TE. Prolactin receptor and uterine milk protein expression in the ovine uterus during the estrous cycle and early pregnancy. Biol Reprod 2000, 62:1779-1789. 10.1095/biolreprod62.6.1779, 10819783.
46. Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. J Anim Sci 2004, 82(E-Suppl):E4-E13.
47. Johnson GA, Spencer TE, Burghardt RC, Bazer FW. Ovine osteopontin: I. Cloning and expression of mRNA in the uterus during the peri-implantation period. Biol Reprod 1999, 61:884-891. 10.1095/biolreprod61.4.884, 10491620.
48. Ing NH, Roberts RM. The major progesterone-modulated proteins secreted into the sheep uterus are members of the serpin superfamily of serine protease inhibitors. J Biol Chem 1989, 264:3372-3379.
49. Johnson GA, Burghardt RC, Joyce MM, Spencer TE, Bazer FW, Pfarrer C, Gray CA. Osteopontin expression in uterine stroma indicates a decidualization-like differentiation during ovine pregnancy. Biol Reprod 2003, 68:1951-1958.
50. Anthony RV, Limesand SW, Fanning MD, Liang R. Placental lactogen and growth hormone: regulation and action. The endocrinology of pregnancy 1998, 461-490. New Jersey: Humana Press, Bazer FW.
51. Gertler A, Djiane J. Mechanism of ruminant placental lactogen action: molecular and in vivo studies. Mol Genet Metab 2002, 75:189-201. 10.1006/mgme.2002.3303, 11914030.
52. Noel S, Herman A, Johnson GA, Gray CA, Stewart MD, Bazer FW, Gertler A, Spencer TE. Ovine placental lactogen specifically binds endometrial glands of the ovine uterus. Biol Reprod 2003, 68:772-780.
53. Lacroix MC, Devinoy E, Servely JL, Puissant C, Kann G. Expression of the growth hormone gene in ovine placenta: detection and cellular localization of the protein. Endocrinology 1996, 137:4886-4892. 10.1210/en.137.11.4886, 8895361.
54. Fischer HE, Bazer FW, Fields MJ. Steroid metabolism by endometrial and conceptus tissues during early pregnancy and pseudopregnancy in gilts. J Reprod Fert 1985, 75:69-78.
55. Joyce MM, Burghardt RC, Geisert RD, Burghardt JR, Hooper RN, Ross JW, Ashworth MD, Johnson GA. Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. Endocrinology 2007, 148:4420-4431. 10.1210/en.2007-0505, 17525118.
56. Ka H, Jaeger LA, Johnson GA, Spencer TE, Bazer FW. Keratinocyte growth factor expression is up-regulated by estrogen in porcine uterine endometrium and it functions in trophectodermal cell proliferation and differentiation. Endocrinology 2001, 142:2303-2310. 10.1210/en.142.6.2303, 11356676.
57. Ka H, Spencer TE, Johnson GA, Bazer FW. Keratinocyte growth factor: expression by endometrial epithelia in the porcine uterus. Biol Reprod 2000, 62:1772-1778. 10.1095/biolreprod62.6.1772, 10819782.
58. Ka H, Al-Ramadan S, Johnson GA, Burghardt RC, Spencer TE, Jaeger LA, Bazer FW. Regulation of fibroblast growth factor 7 expression in the pig uterine endometrium by progesterone and estradiol. Biol Reprod 2007, 77:172-180. 10.1095/biolreprod.106.056309, 17392499.
59. Ross JW, Malayer JR, Ritchey JW, Geisert RD. Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol Reprod 2003, 69:1251-1259. 10.1095/biolreprod.103.015842, 12801990.
60. Harney JP, Bazer FW. Effect of porcine conceptus secretory proteins on interoestrous interval and uterine secretion of prostaglandins. Biol Reprod 1989, 41:277-284. 10.1095/biolreprod41.2.277, 2804221.
61. Joyce MM, Burghardt JR, Burghardt RC, Hooper RN, Jaeger LA, Spencer TE, Bazer FW, Johnson GA. Pig conceptuses increase uterine interferon regulatory factor-1 (IRF-1), but restrict expression to stroma through estrogen-induced IRF-2 in luminal epithelium. Biol Reprod 2007, 77:292-302. 10.1095/biolreprod.107.060939, 17475929.
62. Joyce MM, Burghardt JR, Burghardt RC, Hooper RN, Bazer FW, Johnson GA. Uterine MHC class I molecules and beta 2-microglobulin are regulated by progesterone and conceptus interferons during pig pregnancy. J Immunol 2008, 181:2494-2505.
63. Wessels JM, Linton NF, Croy BA, Tayade C. A review of molecular contrasts between arresting and viable porcine attachment sites. Am J Reprod Immunol 2007, 58:470-480. 10.1111/j.1600-0897.2007.00534.x, 17997745.
64. Choi Y, Johnson GA, Burghardt RC, Berghman LR, Joyce MM, Taylor KM, Stewart MD, Bazer FW, Spencer TE. Interferon regulatory factor two restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus. Biol Reprod 2001, 65:1038-1049. 10.1095/biolreprod65.4.1038, 11566724.
65. Spencer TE, Ott TL, Bazer FW. Expression of interferon regulatory factors one and two in the ovine endometrium: Effects of pregnancy and ovine interferon tau. Biol Reprod 1998, 58:1154-1162. 10.1095/biolreprod58.5.1154, 9603248.
66. Young KH, Kraeling RR, Bazer FW. Effect of pregnancy and exogenous ovarian steroids on endometrial prolactin receptor ontogeny and uterine secretory response in pigs. Biol Reprod 1990, 43:592-599. 10.1095/biolreprod43.4.592, 2289013.
67. Michael AE, Papageorghiou AT. Potential significance of physiological and pharmacological glucocorticoids in early pregnancy. Hum Reprod Update 2008, 14:497-517. 10.1093/humupd/dmn021, 18552168.
68. Barnes N, Haywood P, Flint P, Knox WF, Bundred NJ. Survivin expression in in situ and invasive breast cancer relates to COX-2 expression and DCIS recurrence. Br J Cancer 2006, 94:253-258. 10.1038/sj.bjc.6602932, 2361101, 16421596.
69. Zhang Q, Collins V, Chakrabarty K, Wolf RF, Unno N, Howe D, Rose JC, Wu WX. Regulation of membrane-associated prostaglandin E2 synthase 1 in pregnant sheep intrauterine tissues by glucocorticoid and estradiol. Endocrinology 2006, 147:3719-3726. 10.1210/en.2006-0293, 16690805.
70. Patel FA, Funder JW, Challis JR. Mechanism of cortisol/progesterone antagonism in the regulation of 15-hydroxyprostaglandin dehydrogenase activity and messenger ribonucleic acid levels in human chorion and placental trophoblast cells at term. J Clin Endocrinol Metab 2003, 88:2922-2933. 10.1210/jc.2002-021710, 12788907.
71. Hardy DB, Dixon SJ, Narayanan N, Yang K. Calcium inhibits human placental 11beta-hydroxysteroid dehydrogenase type 2 activity. Biochem Biophys Res Commun 2001, 283:756-761. 10.1006/bbrc.2001.4851, 11350048.
72. Mandl M, Ghaffari-Tabrizi N, Haas J, Nöhammer G, Desoye G. Differential glucocorticoid effects on proliferation and invasion of human trophoblast cell lines. Reproduction 2006, 132:159-167. 10.1530/rep.1.00976, 16816341.
73. Librach CL, Feigenbaum SL, Bass KE, Cui TY, Verastas N, Sadovsky Y, Quigley JP, French DL, Fisher SJ. Interleukin-1 beta regulates human cytotrophoblast metalloproteinase activity and invasion in vitro. J Biol Chem 1994, 269:17125-17131.
74. Loskutoff DJ, Sawdey M, Keeton M, Schneiderman J. Regulation of PAI-1 gene expression in vivo. Thromb Haemost 1993, 70:135-137.
75. Hofmann GE, Glatstein I, Schatz F, Heller D, Deligdisch L. Immunohistochemical localization of urokinase-type plasminogen activator and the plasminogen activator inhibitors 1 and 2 in early human implantation sites. Am J Obstet Gynecol 1994, 170:671-676. 10.1016/S0002-9378(94)70246-2, 8116730.
76. Ma Y, Ryu JS, Dulay A, Segal M, Guller S. Regulation of plasminogen activator inhibitor (PAI)-1 expression in a human trophoblast cell line by glucocorticoid (GC) and transforming growth factor (TGF)-β. Placenta 2002, 23:727-734.
77. Grancha S, Estellés A, Gilabert J, Chirivella M, España F, Aznar J. Decreased expression of PAI-2 mRNA and protein in pregnancies complicated with intrauterine fetal growth retardation. Thromb Haemost 1996, 76:761-767.
78. Simmons RM, Satterfield MC, Welsh TH, Bazer FW, Spencer TE. HSD11B1, HSD11B2, PTGS2, and NR3C1 expression in the peri-implantation ovine uterus: effects of pregnancy, progesterone, and interferon tau. Biol Reprod 2009, 82:35-43.
79. Wu G, Bazer FW, Davis TA, Kim SW, Li P, Rhoads JM, Satterfield MC, Smith SM, Spencer TE, Yin YL. Arginine metabolism and nutrition in growth, health and disease. Amino Acids 2009, 37:153-168. 10.1007/s00726-008-0210-y, 2677116, 19030957.
80. Arosh JA, Banu SK, Chapdelaine P, Fortier MA. Temporal and tissue-specific expression of prostaglandin receptors EP2, EP3, EP4, FP, and cyclooxygenases 1 and 2 in uterus and fetal membranes during bovine pregnancy. Endocrinology 2004, 145:407-417.
81. Minamizaki T, Yoshiko Y, Kozai K, Aubin JE, Maeda N. EP2 and EP4 receptors differentially mediate MAPK pathways underlying anabolic actions of prostaglandin E2 on bone formation in rat calvaria cell cultures. Bone 2009, 44:1177-1185. 10.1016/j.bone.2009.02.010, 19233324.