Biological roles of interferon tau (IFNT) and type I IFN receptors in elongation of the ovine conceptus

Biology of Reproduction

Volumn 92, Issue 2, 2015, Pages

  Brooks, Kelsey ^a   Spencer, Thomas E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Developmental biology; Embryo; Trophectoderm; Uterus

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; ALPHA BETA INTERFERON RECEPTOR 1; ALPHA BETA INTERFERON RECEPTOR 2; ANTISENSE OLIGONUCLEOTIDE; MORPHOLINO OLIGONUCLEOTIDE; TAU INTERFERON; UNCLASSIFIED DRUG; INTERFERON; PLACENTA PROTEIN; TROPHOBLAST PROTEIN 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; BLASTOCYST; CONCEPTION; CONTROLLED STUDY; ENDOMETRIUM; ENZYME INHIBITION; EWE; FEMALE; GERM LAYER; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; RNA TRANSLATION; SHEEP; TROPHECTODERM; TUNEL ASSAY; UTERUS CAVITY; ANIMAL; BREEDING; FETUS DEVELOPMENT; METABOLISM; PHYSIOLOGY; PREGNANCY; UTERUS;

GYMNOMYZA; OVIS;

ANIMALS; ENDOMETRIUM; FEMALE; FETAL DEVELOPMENT; INTERFERON TYPE I; PREGNANCY; PREGNANCY PROTEINS; PREGNANCY, ANIMAL; RECEPTOR, INTERFERON ALPHA-BETA; SHEEP; UTERUS;

EID: 84929577937     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.124156     Document Type: Article

References (79)

1. Guillomot M. Cellular interactions during implantation in domestic ruminants. J Reprod Fertil Suppl 1995; 49:39-51.
2. Lewis GS. Prostaglandin secretion by the blastocyst. J Reprod Fertil Suppl 1989; 37:261-267.
3. Farin CE, Imakawa K, Hansen TR, McDonnell JJ, Murphy CN, Farin PW, Roberts RM. Expression of trophoblastic interferon genes in sheep and cattle. Biol Reprod 1990; 43:210-218.
4. Anthony RV, Helmer SD, Sharif SF, Roberts RM, Hansen PJ, Thatcher WW, Bazer FW. Synthesis and processing of ovine trophoblast protein-1 and bovine trophoblast protein-1, conceptus secretory proteins involved in the maternal recognition of pregnancy. Endocrinology 1988; 123:1274-1280.
5. Marcus GJ. Prostaglandin formation by the sheep embryo and endometrium as an indication of maternal recognition of pregnancy. Biol Reprod 1981; 25:56-64.
6. Roberts RM, Cross JC, Leaman DW. Interferons as hormones of pregnancy. Endocrinol Rev 1992; 13:432-452.
7. Roberts RM, Xie S, Mathialagan N. Maternal recognition of pregnancy. Biol Reprod 1996; 54:294-302.
8. Spencer TE, Johnson GA, Bazer FW, Burghardt RC. Fetal-maternal interactions during the establishment of pregnancy in ruminants. Soc Reprod Fertil Suppl 2007; 64:379-396.
9. Thatcher WW, Hansen PJ, Gross TS, Helmer SD, Plante C, Bazer FW. Antiluteolytic effects of bovine trophoblast protein-1. J Reprod Fertil Suppl 1989; 37:91-99.
10. Spencer TE, Johnson GA, Bazer FW, Burghardt RC. Implantation mechanisms: insights from the sheep. Reproduction 2004; 128:657-668.
11. Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 2008; 135:165-179.
12. Bazer FW, Spencer TE, Johnson GA. Interferons and uterine receptivity. Semin Reprod Med 2009; 27:90-102.
13. Bauersachs S, Mitko K, Ulbrich SE, Blum H, Wolf E. Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Exp Clin Endocrinol Diabetes 2008; 116:371-384.
14. Hansen TR, Henkes LK, Ashley RL, Bott RC, Antoniazzi AQ, Han H. Endocrine actions of interferon-tau in ruminants. Soc Reprod Fertil Suppl 2010; 67:325-340.
15. Spencer TE, Johnson GA, Bazer FW, Burghardt RC, Palmarini M. Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod Fertil Dev 2007; 19:65-78.
16. 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.
17. Hansen TR, Austin KJ, Perry DJ, Pru JK, Teixeira MG, Johnson GA. Mechanism of action of interferon-tau in the uterus during early pregnancy. J Reprod Fertil 1999; 54:329-339.
18. Dorniak P, Bazer FW, Spencer TE. Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol Reprod 2011; 84:1119-1127.
19. Dorniak P, Welsh TH Jr, Bazer FW, Spencer TE. Cortisol and interferon tau regulation of endometrial function and conceptus development in female sheep. Endocrinology 2013; 154:931-941.
20. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998; 67:227-264.
21. Bazan JF. Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci U S A 1990; 87:6934-6938.
22. Stewart MD, Johnson GA, Bazer FW, Spencer TE. Interferon-tau (IFNtau) regulation of IFN-stimulated gene expression in cell lines lacking specific IFN-signaling components. Endocrinology 2001; 142:1786-1794.
23. Stewart MD, Johnson GA, Vyhlidal CA, Burghardt RC, Safe SH, Yu-Lee LY, Bazer FW, Spencer TE. Interferon-tau activates multiple signal transducer and activator of transcription proteins and has complex effects on interferon-responsive gene transcription in ovine endometrial epithelial cells. Endocrinology 2001; 142:98-107.
24. 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.
25. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005; 5:375-386.
26. Lee J, Banu SK, Nithy TK, Stanley JA, Arosh JA. Early pregnancy induced expression of prostaglandin E2 receptors EP2 and EP4 in the ovine endometrium and regulated by interferon tau through multiple cell signaling pathways. Mol Cell Endocrinol 2012; 348:211-223.
27. Banu SK, Lee J, Stephen SD, Nithy TK, Arosh JA. Interferon tau regulates PGF2alpha release from the ovine endometrial epithelial cells via activation of novel JAK/EGFR/ERK/EGR-1 pathways. Mol Endocrinol 2010; 24:2315-2330.
28. Han CS, Mathialagan N, Klemann SW, Roberts RM. Molecular cloning of ovine and bovine type I interferon receptor subunits from uteri, and endometrial expression of messenger ribonucleic acid for ovine receptors during the estrous cycle and pregnancy. Endocrinology 1997; 138:4757-4767.
29. Imakawa K, Tamura K, Lee RS, Ji Y, Kogo H, Sakai S, Christenson RK. Temporal expression of type I interferon receptor in the peri-implantation ovine extra-embryonic membranes: demonstration that human IFNalpha can bind to this receptor. Endocrinol J 2002; 49:195-205.
30. Wang XL, Wang K, Han GC, Zeng SM. A potential autocrine role for interferon tau in ovine trophectoderm. Reprod Domest Anim 2013; 48:819-825.
31. Satterfield MC, Bazer FW, Spencer TE. Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol Reprod 2006; 75:289-296.
32. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci U S A 2006; 103:14390-14395.
33. Bazer FW, Roberts RM, Basha SM, Zavy MT, Caton D, Barron DH. Method for obtaining ovine uterine secretions from unilaterally pregnant ewes. J Anim Sci 1979; 49:1522-1527.
34. Summerton J, Weller D. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev 1997; 7:187-195.
35. Summerton J, Stein D, Huang SB, Matthews P, Weller D, Partridge M. Morpholino and phosphorothioate antisense oligomers compared in cellfree and in-cell systems. Antisense Nucleic Acid Drug Dev 1997; 7:63-70.
36. Wang X, Frank JW, Little DR, Dunlap KA, Carey Satterfield M, Burghardt RC, Hansen TR, Wu G, Bazer FW. Functional role of arginine during the peri-implantation period of pregnancy. I. Consequences of loss of function of arginine transporter SLC7A1 mRNA in ovine conceptus trophectoderm. FASEB J 2014; 28:2852-2863.
37. Wales RG, Cuneo CL. Morphology and chemical analysis of the sheep conceptus from the 13th to the 19th day of pregnancy. Reprod Fertil Dev 1989; 1:31-39.
38. Gerdes J, Schwab U, Lemke H, Stein H. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 1983; 31:13-20.
39. Li X, Traganos F, Melamed MR, Darzynkiewicz Z. Single-step procedure for labeling DNA strand breaks with fluorescein- or BODIPY-conjugated deoxynucleotides: detection of apoptosis and bromodeoxyuridine incorporation. Cytometry 1995; 20:172-180.
40. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119:493-501.
41. Wang X, Ying W, Dunlap KA, Lin G, Satterfield MC, Burghardt RC, Wu G, Bazer FW. Arginine decarboxylase and agmatinase: an alternative pathway for de novo biosynthesis of polyamines for development of mammalian conceptuses. Biol Reprod 2014; 90:84.
42. Satterfield MC, Gao H, Li X, Wu G, Johnson GA, Spencer TE, Bazer FW. Select nutrients and their associated transporters are increased in the ovine uterus following early progesterone administration. Biol Reprod 2010; 82:224-231.
43. Gao H, Wu G, Spencer TE, Johnson GA, Li X, Bazer FW. Select nutrients in the ovine uterine lumen. I. Amino acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes. Biol Reprod 2009; 80:86-93.
44. Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod 2008; 14:667-672.
45. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod 1998; 3:155-163.
46. Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 2002; 61:234-248.
47. Reik W, Romer I, Barton SC, Surani MA, Howlett SK, Klose J. Adult phenotype in the mouse can be affected by epigenetic events in the early embryo. Development 1993; 119:933-942.
48. Schwartzman RA, Cidlowski JA. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocrinol Rev 1993; 14:133-151.
49. Bortner CD, Oldenburg NB, Cidlowski JA. The role of DNA fragmentation in apoptosis. Trends Cell Biol 1995; 5:21-26.
50. Hernandez-Ledezma JJ, Sikes JD, Murphy CN, Watson AJ, Schultz GA, Roberts RM. Expression of bovine trophoblast interferon in conceptuses derived by in vitro techniques. Biol Reprod 1992; 47:374-380.
51. Hernandez-Ledezma JJ, Mathialagan N, Villanueva C, Sikes JD, Roberts RM. Expression of bovine trophoblast interferons by in vitro-derived blastocysts is correlated with their morphological quality and stage of development. Mol Reprod Dev 1993; 36:1-6.
52. Bartol FF, Roberts RM, Bazer FW, Lewis GS, Godkin JD, Thatcher WW. Characterization of proteins produced in vitro by periattachment bovine conceptuses. Biol Reprod 1985; 32:681-693.
53. Kubisch HM, Larson MA, Roberts RM. Relationship between age of blastocyst formation and interferon-tau secretion by in vitro-derived bovine embryos. Mol Reprod Dev 1998; 49:254-260.
54. Kubisch HM, Sirisathien S, Bosch P, Hernandez-Fonseca HJ, Clements G, Liukkonen JR, Brackett BG. Effects of developmental stage, embryonic interferon-tau secretion and recipient synchrony on pregnancy rate after transfer of in vitro produced bovine blastocysts. Reprod Domest Anim 2004; 39:120-124.
55. Spencer TE, Bazer FW. Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol Reprod 1995; 53:1527-1543.
56. Bauersachs S, Ulbrich SE, Reichenbach HD, Reichenbach M, Buttner M, Meyer HH, Spencer TE, Minten M, Sax G, Winter G, Wolf E. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biol Reprod 2012; 86:46.
57. 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.
58. Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, Reichenbach HD, Blum H, Spencer TE, Wolf E. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci U S A 2009; 106:5681-5686.
59. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A 2009; 106:5687-5692.
60. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O'Gaora P, Roche JF, et al. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod 2011; 85:144-156.
61. Ott TL, Gifford CA. Effects of early conceptus signals on circulating immune cells: lessons from domestic ruminants. Am J Reprod Immunol 2010; 64:245-254.
62. Johnson GA, Spencer TE, Hansen TR, Austin KJ, Burghardt RC, Bazer FW. Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biol Reprod 1999; 61:312-318.
63. Johnson GA, Spencer TE, Burghardt RC, Joyce MM, Bazer FW. Interferon-tau and progesterone regulate ubiquitin cross-reactive protein expression in the ovine uterus. Biol Reprod 2000; 62:622-627.
64. Spencer TE, Forde N, Dorniak P, Hansen TR, Romero JJ, Lonergan P. Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction 2013; 146:377-387.
65. Hansen TR, Austin KJ, Perry DJ, Pru JK, Teixeira MG, Johnson GA. Mechanism of action of interferon-tau in the uterus during early pregnancy. J Reprod Fertil Suppl 1999; 54:329-339.
66. Bauersachs S, Wolf E. Immune aspects of embryo-maternal cross-talk in the bovine uterus. J Reprod Immunol 2013; 97:20-26.
67. Hansen TR, Pru JK. ISGylation: a conserved pathway in mammalian pregnancy. Adv Exp Med Biol 2014; 759:13-31.
68. Imakawa K, Imai M, Sakai A, Suzuki M, Nagaoka K, Sakai S, Lee SR, Chang KT, Echternkamp SE, Christenson RK. Regulation of conceptus adhesion by endometrial CXC chemokines during the implantation period in sheep. Mol Reprod Dev 2006; 73:850-858.
69. Johnson GA, Austin KJ, Collins AM, Murdoch WJ, Hansen TR. Endometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows. Endocrine 1999; 10:243-252.
70. Uze G, Lutfalla G, Mogensen KE. Alpha and beta interferons and their receptor and their friends and relations. J Interferon Cytokine Res 1995; 15:3-26.
71. Lamken P, Gavutis M, Peters I, Van der Heyden J, Uze G, Piehler J. Functional cartography of the ectodomain of the type I interferon receptor subunit ifnar1. J Mol Biol 2005; 350:476-488.
72. de Weerd NA, Vivian JP, Nguyen TK, Mangan NE, Gould JA, Braniff SJ, Zaker-Tabrizi L, Fung KY, Forster SC, Beddoe T, Reid HH, Rossjohn J, et al. Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1. Nat Immunol 2013; 14:901-907.
73. Kim S, Choi Y, Bazer FW, Spencer TE. Identification of genes in the ovine endometrium regulated by interferon tau independent of signal transducer and activator of transcription 1. Endocrinology 2003; 144:5203-5214.
74. Choi Y, Johnson GA, Spencer TE, Bazer FW. Pregnancy and interferon tau regulate MHC class I and beta-2-microglobulin expression in the ovine uterus. Biol Reprod 2003; 68:1703-1710.
75. Lee J, Stanley JA, McCracken JA, Banu SK, Arosh JA. Intrauterine coadministration of ERK1/2 inhibitor U0126 inhibits interferon tau action in the endometrium and restores luteolytic PGF2alpha pulses in sheep. Biol Reprod 2014; 91:46.
76. Johnson GA, Burghardt RC, Newton GR, Bazer FW, Spencer TE. Development and characterization of immortalized ovine endometrial cell lines. Biol Reprod 1999; 61:1324-1330.
77. Johnson GA, Stewart MD, Gray CA, Choi Y, Burghardt RC, Yu-Lee LY, Bazer FW, Spencer TE. Effects of the estrous cycle, pregnancy, and interferon tau on 2',5'-oligoadenylate synthetase expression in the ovine uterus. Biol Reprod 2001; 64:1392-1399.
78. Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J Virol 2010; 84:4415-4425.
79. Joyce MM, White FJ, Burghardt RC, Muniz JJ, Spencer TE, Bazer FW, Johnson GA. Interferon stimulated gene 15 conjugates to endometrial cytosolic proteins and is expressed at the uterine-placental interface throughout pregnancy in sheep. Endocrinology 2005; 146:675-684.