Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
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Temporal Regulation of Ovine Interferon-tau Gene by the Transcription Factor Eomesodermin in the Peri-Implantation Period

  • Kim, Min-Su (Dairy Science Division, National Institute of Animal Science, RDA) ;
  • Lim, Hyun-Joo (Dairy Science Division, National Institute of Animal Science, RDA) ;
  • Lee, Ji Hwan (Dairy Science Division, National Institute of Animal Science, RDA) ;
  • Hur, Tae Young (Dairy Science Division, National Institute of Animal Science, RDA) ;
  • Son, Jun Kyu (Dairy Science Division, National Institute of Animal Science, RDA)
  • Received : 2019.10.31
  • Accepted : 2019.12.10
  • Published : 2019.12.31
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Abstract

Interferon tau (IFNT) regulation, an anti-luteolytic factor produced by conceptuses of the ruminant ungulates, is essential for the maintenance of early pregnancy, but a definitive mechanism for its temporal transcription has not been elucidated. We and others have observed the T-box protein eomesodermin (EOMES) exhibited high mRNA expression in the ovine embryonic trophectoderm; thus, both caudal-relatedhomeobox-2 (CDX2) and EOMES coexist during the early stages of conceptus development. Objective of this study was to examine the effect of EOMES on ovine IFNT gene transcription when evaluated with CDX2, ETS2 and AP1 transcription factors implicated in the control of cell differentiation in the trophectoderm. In this study, quantitatively via reverse transcription-polymerase chain reaction (RT-PCR) analysis between ovine trophoblast cells was initially performed, finding that transcription factors CDX2 and 'EOMES transcription factor mRNAs' were specific to trophectoderm cells. These mRNAs were also found in days 15, 17, and 21 ovine conceptuses. Furthermore, human choriocarcinoma JEG3 cells (trophoblast cell line) were cotransfected with an ovine IFNT (-654bp)-luciferase reporter (-654-oIFNT-Luc) construct and several transcription factor expression plasmids. Cotransfection of the reporter construct with CDX2, ETS2 and AP1 increased transcription of -654-oIFNT-Luc by about 11-fold compared with transfection of the construct alone. When cells were initially transfected with EOMES followed by transfection with CDX2, ETS2 and/or AP1, the expression of -654-oIFNT-Luc was decreased. Also, EOMES factor inhibited the stimulatory activity of CDX2 alone. These results suggest that when conceptuses attach to the uterine epithelium, ovine IFNT gene transcription is down-regulated by an increase of EOMES factor expression in the attached ovine trophoblast cells.

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References

  1. Ashworth CJ, Bazer FW. 1989. Changes in ovine conceptus and endometrial function following asynchronous embryo transfer or administration of progesterone. Biol Reprod 40:425-433. https://doi.org/10.1095/biolreprod40.2.425
  2. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I. 2005. Molecular evidence for critical period in mural trophoblast development in bovine blastocysts. Dev Biol 288:448-460. https://doi.org/10.1016/j.ydbio.2005.09.043
  3. Ezashi T, Das P, Gupta R, Walker A, Roberts RM. 2008. The role of homeobox protein distal-less 3 and its interaction with ETS2 in regulating bovine interferon-tau gene expressionsynergistic transcriptional activation with ETS2. Biol Reprod 79:115-124. https://doi.org/10.1095/biolreprod.107.066647
  4. Ezashi T, Ealy AD, Ostrowski MC, Roberts RM. 1998. Control of interferon-${\tau}$ gene expression by Ets-2. Proc Natl Acad Sci USA 95:7882-7887. https://doi.org/10.1073/pnas.95.14.7882
  5. Farin CE, Imakawa K, Roberts RM. 1989. In situ localization of mRNA for the interferon, ovine trophoblast protein-1, during early embryonic development of the sheep. Mol Endocrinol 3:1099-1107. https://doi.org/10.1210/mend-3-7-1099
  6. Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. 1982. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13-21. J Reprod Fertil 65:141-150. https://doi.org/10.1530/jrf.0.0650141
  7. Guillomot M, Michel C, Gaye P, Charlier N, Trojan J, Martal J. 1990. Cellular localization of an embryonic interferon, ovine trophoblastin and its mRNA in sheep embryos during early pregnancy. Biol Cell 68:205-211. https://doi.org/10.1016/0248-4900(90)90309-Q
  8. Hancock SN, Agulnik SI, Silver LM, Papaioannou VE. 1999. Mapping and expression analysis of the mouse ortholog of Xenopus Eomesodermin. Mech Dev 81:205-208. https://doi.org/10.1016/S0925-4773(98)00244-5
  9. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM. 1987. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature 330:377-379. https://doi.org/10.1038/330377a0
  10. Imakawa K, Chang K-T, Christenson RK. 2004. Pre-implantation conceptus and maternal uterine communications: Molecular events leading to successful implantation. J Reprod Dev 50:155-169. https://doi.org/10.1262/jrd.50.155
  11. Imakawa K, Kim M-S, Matsuda-Minehata F, Ishida S, Iizuka M, Suzuki M, Chang K-T, Echternkamp SE, Christenson RK. 2006. Regulation of the ovine interferon-tau gene by a trophoblastspecific transcription factor, Cdx2. Mol Reprod Dev 73:559-567. https://doi.org/10.1002/mrd.20457
  12. Kim MS, Sakurai T, Bai H, Bai R, Sato D, Nagaoka K, Chang KT, Godkin JD, Min KS, Imakawa K. 2013. Presence of Transcription Factor OCT4 Limits Interferon-tau Expression during the Pre-attachment Period in Sheep. Asian-Aust. J. Anim. Sci 5:638-645.
  13. Kurosaka S, Eckardt S, McLaughlin KJ. 2004. Pluriopotent lineage definition in bovine embryos by Oct4 transcript localization. Biol Reprod 71:1578-1582. https://doi.org/10.1095/biolreprod.104.029322
  14. Matsuda F, Xu N, Kijima S, Tachi C, Christenson RK, Sakai S, Imakawa K. 2004. Analysis of transcriptional control elements in the 5'-upstream region of ovine interferon--${\tau}$ gene using feeder-independent caprine trophoblast cell line, HTS-1. Placenta 25:166-175. https://doi.org/10.1016/j.placenta.2003.08.016
  15. Nephew KP, Whaley AE, Christenson RK, Imakawa K. 1993. Differential expression of distinct mRNAs for ovine trophoblast protein-1 and related sheep type I interferons. Biol Reprod 48:768-778. https://doi.org/10.1095/biolreprod48.4.768
  16. Roberts RM, Cross JC, Leaman DW. 1992. Interferons as hormones of pregnancy. Endocr Rev 13:432-452. https://doi.org/10.1210/edrv-13-3-432
  17. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95-99. https://doi.org/10.1038/35003601
  18. Sakurai T, Bai H, Bai R, Sato D, Arai M. 2013. Down-regulation of interferon tau gene transcription with a transcription factor, EOMES. Mol Reprod Dev 80:371-383. https://doi.org/10.1002/mrd.22171
  19. Sakurai T, Bai H, Konno T, Ideta A, Aoyagi Y, Godkin JD, Imakawa K. 2010. Function of a transcription factor CDX2 beyond its trophectoderm lineage specification. Endocrinology 151:5873-5881. https://doi.org/10.1210/en.2010-0458
  20. Sakurai T, Sakamoto A, Muroi Y, Bai H, Nagaoka K, Tamura K, Takahashi T, Hashizume K, Sakatani M, Takahashi M, Godkin JD, Imakawa K. 2009. Induction of endogenous interferon tau gene transcription by CDX2 and high acetylation in bovine nontrophoblast cells. Biol Reprod 80:1223-1231. https://doi.org/10.1095/biolreprod.108.073916
  21. Short RV. 1969. Implantation and the maternal recognition of pregnancy. In: GEW,Wolstenhome M, O'Connor editors. Foetal anatomy, Ciba Foundation Symposium. London: J&A Churchill. pp 2-26.
  22. Spencer TE, Bazer FW. 1996. Ovine interferon-t suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology 137:1144-1147. https://doi.org/10.1210/en.137.3.1144
  23. Vallet JL, Bazer FW, Fliss MF, Thatcher WW. 1988. Effect of ovine secretory proteins and purified ovine trophoblast protein-1 on interoestrous interval and plasma concentrations of prostaglandin F-2a and E and of 13, 14-dihydro-15-keto prostaglandin F-2a in cyclic ewes. J Reprod Fertil 84:493-504. https://doi.org/10.1530/jrf.0.0840493
  24. Xu N, Takahashi Y, Matsuda F, Sakai S, Christenson RK, Imakawa K. 2003. Coactivator CBP in the regulation of conceptus $IFN{\tau}$ gene transcription. Mol Reprod Dev 65:23-29. https://doi.org/10.1002/mrd.10293
  25. Yamaguchi H, Ikeda Y, Moreno JI, Katsumura M, Miyazawa T, Takahashi E, Imakawa K, Sakai S, Christenson RK. 1999. Identification of a functional transcriptional factor AP1 site in the sheep interferon-${\tau}$ gene that mediates a response to PMA in JEG3 cells. Biochem J 340:767-773. https://doi.org/10.1042/bj3400767
  26. Yamaguchi H, Katsumura M, Imakawa K, Sakai S, Christenson RK. 2000. Analysis of possible silencer elements of ovine interferon-tau gene. Endocr J 47:137-42. https://doi.org/10.1507/endocrj.47.137
  27. Yamaguchi H, Nagaoka K, Imakawa K, Sakai S, Christenson RK. 2001. Enhancer regions of ovine interferon-${\tau}$ gene that confer PMA response or cell type specific transcription. Mol Cell Endocrinol 173:147-155. https://doi.org/10.1016/S0303-7207(00)00408-1