DOI QR코드

DOI QR Code

Imprinted Gene mRNA Expression during Porcine Peri-implantation Development

  • Cha, Byung-Hyun ;
  • Kim, Bong-Ki ;
  • Hwang, Seongsoo ;
  • Yang, Byoung-Chul ;
  • Im, Gi-Sun ;
  • Park, Mi-Rung ;
  • Woo, Jae-Seok ;
  • Kim, Myung-Jick ;
  • Seong, Hwan-Hoo ;
  • Cho, Jae-Hyeon ;
  • Ko, Yeoung-Gyu
  • Received : 2008.07.29
  • Accepted : 2009.03.15
  • Published : 2010.06.01

Abstract

Imprinted genes are essential for fetal development, growth regulation, and postnatal behavior. However, little is known about imprinted genes in livestock. We hypothesized that certain putatively imprinted genes affected normal peri-implantation development such as embryo elongation, initial placental development, and preparation of implantation. The objective of the present study was to investigate the mRNA expression patterns of several putatively imprinted genes during the porcine peri-implantation stages from day 6 to day 21 of gestation. Imprinted genes were selected both maternally (Dlk1, IGF2, Ndn, and Sgce) and paternally (IGF2r, H19, Gnas and Xist). Here, we report that the maternally imprinted gene IGF2 was expressed from day 6 (Blastocyst stage), but Dlk1, Ndn, and Sgce were not expressed in this stage. These genes were first expressed between days 12 and day 14. All the maternally imprinted genes studied showed significantly high expression patterns from day 18 of embryo development. In contrast, paternally imprinted genes IGF2r, H19, Gnas, and Xist were first expressed from day 6 of embryo development (BL). Our data demonstrated that the expression of H19 and Gnas genes was significantly increased from day 14 of the embryo developmental stage, while IGF2r and Xist only showed high expression after day 21. This study is the first to show that the putatively imprinted genes were stage-specific during porcine embryonic development. These results demonstrate that the genes studied may exert important effects on embryo implantation and fetal development.

Keywords

Imprinted Genes;Peri-implantation;mRNA Expression;Early Development;Pig

References

  1. Cheng, H. C., F. W. Zhang, C. Y. Deng, C. D. Jiang, Y. Z. Xiong, F. E. Li and M. G. Lei. 2007. ASCL2 gene expression analysis and its association with carcass traits in pigs. Asian-Aust. J. Anim. Sci. 20:1485-1489
  2. Efstratiadis, A. 1998. Genetics of mouse growth. Int. J. Dev. Biol. 42:955-976
  3. Goshen, R., J. Rachmilewitz, T. Schneider, N. de-Groot, I. Ariel, Z. Palti and A. A. Hochberg. 1993. The expression of the H-19 and IGF-2 genes during human embryogenesis and placental development. Mol. Reprod. Dev. 34:374-379 https://doi.org/10.1002/mrd.1080340405
  4. Gries, L. K., R. D. Geisert, M. T. Zavy, J. E. Garrett and G. L. Morgan. 1989. Uterine secretory alterations coincident with embryonic mortality in the gilt after exogenous estrogen administration. J. Anim. Sci. 67:276-284
  5. Lee, H. K., S. S. Lee, T. H. Kim, G. J. Jeon, Y. S. Shin, J. H. Han, B. H. Choi and I. C. Cheong. 2003. Detection of imprinted QTL for growth traits in pigs. Asian-Aust. J. Anim. Sci. 16:1807-1092
  6. Reik, W., W. Dean and J. Walter. 2001. Epigenetic reprogramming in mammalian development. Science 293:1089-1093 https://doi.org/10.1126/science.1063443
  7. Tilghman, S. M. 1999. The sins of the fathers and mothers:genomic imprinting in mammalian development. Cell. 96:185-193 https://doi.org/10.1016/S0092-8674(00)80559-0
  8. Bennett, G. L. and K. A. Leymaster. 1989. Integration of ovulation rate, potential embryonic viability and uterine capacity into a model of litter size in swine. J. Anim. Sci. 67:1230-1241
  9. Surani, M. A., R. Kothary, N. D. Allen, P. B. Singh, R. Fundele, A. C. Ferguson-Smith and S. C. Barton. 1990. Genome imprinting and development in the mouse. Dev. Suppl. 89-98
  10. Young, L. E., A. E. Schnieke, K. J. McCreath, S. Wieckowski, G. Konfortova, K. Fernandes, G. Ptak, A. J. Kind, I. Wilmut, P. Loi and R. Feil. 2003. Conservation of IGF2-H19 and IGF2R imprinting in sheep: effects of somatic cell nuclear transfer. Mech. 120:1433-1442 https://doi.org/10.1016/j.mod.2003.09.006
  11. Pusateri, A. E., M. F. Rothschild, C. M. Warner and S. P. Ford. 1990. Changes in morphology, cell number, cell size and cellular estrogen content of individual littermate pig conceptuses on days 9 to 13 of gestation. J. Anim. Sci. 68:3727-3735
  12. Surani, M. A., S. C. Barton and M. L. Norris. 1984. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548-550 https://doi.org/10.1038/308548a0
  13. DeChiara, T. M., A. Efstratiadis and E. J. Robertson. 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345:78-80 https://doi.org/10.1038/345078a0
  14. Ross, J. W., M. D. Ashworth, A. G. Hurst, J. R. Malayer and R. D. Geisert. 2003. Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reprod. Biol. Endocrinol. 1:23-34 https://doi.org/10.1186/1477-7827-1-23
  15. Perry, J. S. 1981. The mammalian fetal membranes. J. Reprod. Fertil. 62:321-335 https://doi.org/10.1530/jrf.0.0620321
  16. Schmidt, J. V., P. G. Matteson, B. K. Jones, X. J. Guan and S. M. Tilghman. 2000. The Dlk1 and Gtl2 genes are linked and reciprocally imprinted. Genes Dev. 14:1997-2002
  17. Killian, J. K., C. M. Nolan, A. A. Wylie, T. Li, T. H. Vu, A. R. Hoffman and R. L. Jirtle. 2001. Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary. Hum. Mol. Genet. 10:1721-1728 https://doi.org/10.1093/hmg/10.17.1721
  18. Amarger, V., M. Nguyen, A. S. Van Laere, M. Braunschweig, C. Nezer, M. Georges and L. Andersson. 2002. Comparative sequence analysis of the INS-IGF2-H19 gene cluster in pigs. Mamm Genome. 13:388-398 https://doi.org/10.1007/s00335-001-3059-x
  19. Lee, M. Y., J. H. Lee and J. J. Kim. 2007. Evaluation of reciprocal cross design on detection and characterization of non-mendelian QTL in F2 outbred populations: I. parent-of-origin effect. Asian-Aust. J. Anim. Sci. 20:1805-1811
  20. University of Otago. 2006. The catalogue of imprinted genes and parent-of-origin effects in humans and animals. http://igc.otago.ac.nz/home.html/Acessed Dec. 1, 2006
  21. Constancia, M., M. Hemberger, J. Hughes, W. Dean, A. Ferguson-Smith, R. Fundele, F. Stewart, G. Kelsey, A. Fowden, C. Sibley and W. Reik. 2002. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945-948 https://doi.org/10.1038/nature00819
  22. Geisert, R. D. and J. V. Yelich. 1997. Regulation of conceptus development and attachment in pigs. J. Reprod. Fertil. Suppl. 52:133-149
  23. Ruddock, N. T., K. J. Wilson, M. A. Cooney, N. A. Korfiatis, R. T. Tecirlioglu and A. J. French. 2004. Analysis of imprinted messenger RNA expression during bovine preimplantation development. Biol. Reprod. 70:1131-1135 https://doi.org/10.1095/biolreprod.103.022236
  24. Livak, K. J. and T. D. Schmittgen. 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
  25. Geisert, R. D., J. W. Brookbank, R. M. Roberts and F. W. Bazer. 1982. Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biol. Reprod. 27:941-955 https://doi.org/10.1095/biolreprod27.4.941
  26. Latham, K. E. and R. M. Schultz. 2001. Embryonic genome activation. Front Biosci. 6:D748-759 https://doi.org/10.2741/Latham
  27. Brannan, C. I., E. C. Dees, R. S. Ingram and S. M. Tilghman. 1990. The product of the H19 gene may function as an RNA. Mol. Cell Biol. 10:28-36
  28. MacDonald, H. R. and R. Wevrick. 1997. The necdin gene is deleted in Prader-Willi syndrome and is imprinted in human and mouse. Hum. Mol. Genet. 6:1873-1878 https://doi.org/10.1093/hmg/6.11.1873
  29. Piras, G., A. El Kharroubi, S. Kozlov, D. Escalante-Alcalde, L. Hernandez, N. G. Copeland, D. J. Gilbert, N. A. Jenkins and C. L. Stewart. 2000. Zac1 (Lot1), a potential tumor suppressor gene, and the gene for epsilon-sarcoglycan are maternally imprinted genes: identification by a subtractive screen of novel uniparental fibroblast lines. Mol. Cell Biol. 20:3308-3315 https://doi.org/10.1128/MCB.20.9.3308-3315.2000
  30. Li, X. P., K. T. Do, J. J. Kim, J. Huang, S. H. Zhao, Y. Lee, M. F. Rothschild, C. K. Lee and K. S. Kim. 2008. Molecular characteristics of the porcine DLK1 and MEG3 genes. Anim Genet. 39:189-192 https://doi.org/10.1111/j.1365-2052.2007.01693.x