Expression of Placenta-Related Genes (Cdx2 and GATA6) in Cloned Porcine Development

  • Cha, Byung-Hyun (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Hwang, Seong-Soo (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Lee, Hwi-Cheul (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Park, Mi-Rung (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Im, Gi-Sun (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Woo, Jae-Seok (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Park, Soo-Bong (Division of Animal Biotechnology, National Institute of Animal Science, RDA) ;
  • Cho, Jae-Hyeon (Gyeongsang National University) ;
  • Ko, Yeoung-Gyu (Division of Animal Biotechnology, National Institute of Animal Science, RDA)
  • Published : 2009.12.31

Abstract

Abnormal development and fetal loss during the post-implantation period are key concerns in the production of cloned animals by somatic cell nuclear transfer (SCNT). We hypothesized that the problems in cloned porcine offspring derived from SCNT are related to interactions between the conceptus and the endometrial environment. In the present study, we investigated expression patterns in the formation of placenta-related genes (Cdx2 and GATA6) in whole in vivo normal porcine embryos (from single cell to blastocyst) and each tissue of a normal fetus at Days 25, 35 and 55 by quantitative mRNA expression analysis using real-time PCR. The expression of Cdx2 and GATA6 mRNA increased to around the blastocyst stage. These genes were gradually decreased from the peri-implantation to post-implantation stage. Moreover, we examined the expression patterns of Cdx2 and GATA6 in Day 35 normal and SCNT cloned fetuses by the same methods. And, the level of Cdx2 and GATA6 gene expression in the extraembryonic tissue of SCNT was significantly higher than that of control tissues. From the present results, it can be postulated that the aberrant expression of Cdx2 and GATA6 genes in the endometrial and extraembryonic tissues at pre- and peri-implantation stages may be closely related to the lower efficiency of animal cloning.

Keywords

References

  1. aguisi A, Behboodi E, Melican DT, Pollock JS, Destrempes MM, Cammuso C, Williams JL, Nims SD, Porter CA, Meade HM, Godke RA, Gavin WG, Overstrom EW, Echelard Y (1999): Production of goats by somatic cell nuclear transfer. Nat Biotechnol 17:456-461 https://doi.org/10.1038/8632
  2. Bedding RSP, Robertson EJ (1989): An assessment of the developmental potential of the embryonic stem cells in the midgestation mouse embryo. Development 105:733-737
  3. Boquest AC, Grupen CG, Harrison SJ, Mcllfatrick SM, Ashman RJ, d'Apice AJ, Nottle MB (2002): Production of cloned pigs from cultured fetal fibroblast cells. Biol Reprod 66:1283-1287 https://doi.org/10.1095/biolreprod66.5.1283
  4. Chavatte-Palmer P, Heyman Y, Renard JP (2000): Cloning and associated physiopathology of gestation. Gynecol Obstet Fertil 28:633-642
  5. Christenson RK, Leymaster LA (2000): Effects of selection for ovulation rate or uterine capacity on gravid uterine, farrowing and weaning traits in swine. J Anim Sci 78 (Suppl. 1):202(Abstr)
  6. Dean W, Santos F, Reik W (2003): Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Sem Cell Dev Biol 14:93-100 https://doi.org/10.1016/S1084-9521(02)00141-6
  7. De Sousa PA, King T, Harkness L, Young LE, Walker SK, Wilmut I (2001): Evaluation of gestational deficiencies in cloned sheep fetuses and placenta. Biol Reprod 65:23-30 https://doi.org/10.1095/biolreprod65.1.23
  8. Dyce KM, Sack WO, Wensing CJG (2002): Textbook of Veterinary Anatomy. NL, Elsevier Science
  9. Foxcroft, GR (1997): Mechanisms mediating nutritional effects on embryonic survival in pigs. J Reprod Fertil Suppl 52:47-61
  10. Gove C, Walmsley M, Nijjar S, Bertwistle, D, Guille M, Partington G, Bomford A, Patient R (1997): Over-expression of GATA-6 in xenopus embryos blocks differentiation of the heart precursors. EMBO J 16: 355-368 https://doi.org/10.1093/emboj/16.2.355
  11. Gries LKR, Giesert D, Zavy MT, Garrett JE, Morgan GL (1989): Uterine secretory alterations coincident with embryonic mortality in the gilt exogenous estrogen administration. J Anim Sci 67:276-284 https://doi.org/10.2527/jas1989.671276x
  12. Heiner Niemann, X Cindy Tian, W Allan King and Rita S F Lee (2008): Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135:151- 163 https://doi.org/10.1530/REP-07-0397
  13. Hill JR, Burghard RC, Jones K, Long CR, Looney CR, Shin T, Spencer TE, Thompson JA, Winger QA, Westhusin ME (2000): Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol Reprod 63:1787-17794 https://doi.org/10.1095/biolreprod63.6.1787
  14. Humpherys D, Eggan K, Akutsu H, Friedman A, Hochedlinger K, Yangimachi R, Lander ES, Golub TR, Jaenisch R (2002): Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc Natl Aced Sci USA 99: 12889-12894 https://doi.org/10.1073/pnas.192433399
  15. 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 73:55
  16. Inoue K, Kohda T, Lee J, Ogonuki N, Mochida K, Noguchi Y, Tanemura K, Kaneko-Ishino T, Ishino F, Ogura A (2002): Faithful expression of imprinted genes in cloned mice. Science 295:297 https://doi.org/10.1126/science.295.5553.297
  17. Kato Y, Tani T, Sotomaru Y, Kurokawa K, Kato J, Doguchi H, Yasue H, Tsunoda Y (1998): Eight calves cloned from somatic cells of a single adult. Science 282:2095-2098 https://doi.org/10.1126/science.282.5396.2095
  18. Klisch K, Boos A, Friedrich M, Herzog K, Feldmann M, Sousa N, Beckers J, Leiser R, Schuler G (2006): The glycosylation of pregnancy-associated glycoproteins and prolactin-related protein-I in bovine binucleate trophoblast giant cells changes before parturition. Reproduction 132:791-798 https://doi.org/10.1530/REP-06-0040
  19. Koutsourakis M, Langeveld A, Patient R, Beddington R & Grosveld F (1999): The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723-732
  20. Kues WA, Niemann H (2004): The contribution of farm animals to human health. Trends in Biotechnology 22:286-294 https://doi.org/10.1016/j.tibtech.2004.04.003
  21. Latham KE (2004): Cloning: questions answered and unsolved. Differentiation 72:11-22 https://doi.org/10.1111/j.1432-0436.2004.07201003.x
  22. Livak KJ, Schmittgen TD (2001): Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408 https://doi.org/10.1006/meth.2001.1262
  23. Ono Y, Shimozawa N, Ito M, Kono T (2001): Cloned mice from fetal fibroblast cells arrested at metaphase by a serial nuclear transfer. Biol Reprod 64: 44-50 https://doi.org/10.1095/biolreprod64.1.44
  24. Ogawa H, Ono Y, Shimozawa N, Sotomaru Y, Katsuzawa Y, Hiura H, Ito M, Kono T (2003): Disruption of imprinting in cloned mouse fetuses from embryonic stem cells. Reproduction 126:549-557 https://doi.org/10.1530/rep.0.1260549
  25. Ogura A, Inoue K, Ogonuki N, Lee J, Kohda T, Ishino F (2002): Phenotypic effects of somatic cell cloning in the mouse. Cloning Stem Cells 4:397-405 https://doi.org/10.1089/153623002321025078
  26. Polejaeva IA, Chen SH, Vaught TD, Page RL, Mullins J, Ball S, Dai Y, Boone J, Walker S, Ayares DL, Colman A, Campbell KH (2000): Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86-90 https://doi.org/10.1038/35024082
  27. Piedrahita JA, Mir B, Dindot S, Walker S (2004): Somatic cell cloning: The ultimate form of nuclear reprogramming? J Am Soc Nephrol 15:1140-1144 https://doi.org/10.1097/01.ASN.0000110183.87476.05
  28. Ralston A, Rossant J (2008): Cdx2 downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryos. Developmental Biology 313:614-629 https://doi.org/10.1016/j.ydbio.2007.10.054
  29. Sawai K, Kageyama S, Moriyasu S, Hirayama H, Minamihashi A, Onoe S(2005): Analysis of mRNA transcripts for insulin-like growth factor receptors and binding proteins in bovine embryos derived from somatic cell nuclear transfer. Cloning Stem Cells 7:189-198 https://doi.org/10.1089/clo.2005.7.189
  30. Stroband HW, Taverne N, Langenfeld K, Barends PM (1986): The ultrastructure of the uterine epithelium of the pig during the estrous cycle and early pregnancy. Cell Tissue Res 246:81-9
  31. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J (2005): Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093-2102 https://doi.org/10.1242/dev.01801
  32. Wilson ME, Biensen MJ, Ford SP (1999): Novel insight into the control of litter size in pigs, using placental efficiency as a selection tool. J Anim Sci 77:1654-1658 https://doi.org/10.2527/1999.7771654x
  33. Xie S, Nagel RJ, Green J, Beckers JF, Roberts RM. (1996): Trophoblast-specific processing and phosphorylation of pregnancy-associated glycoprotein-1 in day 15 to 25 sheep placenta. Biol Reprod 54:122-129 https://doi.org/10.1095/biolreprod54.1.122
  34. Yang L, Xue F, Tian XC, Du F, Kubota C, Taneja M, Dinnyes A, Dai Y, Levine H, Lii S, Kuo B, Buckley A, Buckley D, Chen C, Xu X, Coss D, Walker AM (2002): Maternal prolactin composition can permanently affect epidermal T cell function in the offspring. Dev Comp Immunol. 26:849-860 https://doi.org/10.1016/S0145-305X(02)00036-8
  35. Yamaguchi H, Ikeda Y, Moreno JI, Katsumura M, Miyazawa T, Takahashi E, Imakawa K, Sakai S, Christenson RK (1999): Identification of a functional transcription factor AP-1 site in the sheep interferon t gene that mediates a response to PMA in JEG3 cells. Biochem J 340:767-773 https://doi.org/10.1042/0264-6021:3400767
  36. Yamazaki Y, Mann MR, Lee SS, Marh J, McCarrey JR, Yanagimachi R, Bartolomei MS (2003): Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc Natl Acad Sci USA 100:12207-12212 https://doi.org/10.1073/pnas.2035119100