Expression of Ids in Preimplantation Mouse Embryos

착상 전 생쥐배아에서 Id 유전자의 발현

  • Hong, Seok-Ho (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Nah, Hee-Young (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Lee, Young-Jin (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Lee, Ji-Won (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Son, Young-Soo (Cheong-Ju St. Marys' Hospital) ;
  • Chae, Hee-Dong (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Kim, Sung-Hoon (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Kang, Byung-Moon (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center) ;
  • Kim, Chung-Hoon (Dept of OBGY, College of Medicine, Ulsan University, Asan Medical Center)
  • 홍석호 (울산대학교 서울아산병원 산부인과) ;
  • 나희영 (울산대학교 서울아산병원 산부인과) ;
  • 이영진 (울산대학교 서울아산병원 산부인과) ;
  • 이지원 (울산대학교 서울아산병원 산부인과) ;
  • 손영수 (청주성모병원) ;
  • 채희동 (울산대학교 서울아산병원 산부인과) ;
  • 김성훈 (울산대학교 서울아산병원 산부인과) ;
  • 강병문 (울산대학교 서울아산병원 산부인과) ;
  • 김정훈 (울산대학교 서울아산병원 산부인과)
  • Published : 2004.12.30

Abstract

Objective: The Id family of helix-loop-helix proteins are thought to affect the balance between cell growth and differentiation by negatively regulating the function of basic-helix-loop-helix (bHLH) transcriptional factors. The aim of this study was to investigate the expression pattern of Ids (Id-1, -2, -3, and -4) in preimplantation mouse embryos at mRNA and protein levels. Methods: Oocytes and preimplantation embryos were collected from reproductive organs of female ICR mice following superovulation. RT-PCR was performed to investigate the mRNA expression patterns of Id genes and their protein were localized by immunofluorescence analysis. Results: Id-1 and Id-3 mRNAs were strongly expressed at the germinal vesicle (GV) oocyte and the blastocyst stages. Id-2 mRNA was expressed throughout preimplantation embryo development, but Id-4 was not expressed. Immunofluorescence showed that Id-1 and Id-2 were predominantly localized in cytoplasmic region, but the immunofluorescence signal of Id-3 was weak throughout preimplantation embryo development. Conclusion: These data show for the first time that Ids are expressed in preimplantation mouse embryos and suggest that Ids may play an important role in early preimplantation embryo development and uterine physiological changes.

Keywords

References

  1. Kadesch T. Helix-loop-helix proteins in the regula-tion of immunoglobulin gene transcription. Immunol Today 1992; 13: 31-6 https://doi.org/10.1016/0167-5699(92)90201-H
  2. Benezra R, Davis RL, Lockshon D, Turner DL, Wei-ntraub H. The protein Id: A negative regulator of helix-loop-helix DNA binding proteins. Cell 1990; 61: 49-59 https://doi.org/10.1016/0092-8674(90)90214-Y
  3. Jen Y, Weintraub H, Benezra R. Overexpression of Id protein inhibits the muscle differentiation pro-gram: In vivo association of Id with E2A proteins. Genes Dev 1992; 6: 1466-79 https://doi.org/10.1101/gad.6.8.1466
  4. Norton JD, Deed RW, Craggs G, Sablitzky F. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol 1998; 8: 58-65 https://doi.org/10.1016/S0962-8924(97)01183-5
  5. Sun XH, Copeland NG, Jenkins NA, Baltimore D. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 1991; 11: 5603-11 https://doi.org/10.1128/MCB.11.11.5603
  6. Christy BA, Sanders LK, Lau LF, Copeland NG, Je-nkins NA, Nathans D. An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. Proc Natl Acad Sci 1991; 88: 1815-9 https://doi.org/10.1073/pnas.88.5.1815
  7. Riechmann V, Van Cruchten I, Sablizky F. The expr-ession pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res 1994; 22: 749-55 https://doi.org/10.1093/nar/22.5.749
  8. Kurobayashi M, Dutta S, Kedes L. Serum inducible factors binding to an activating transcription factors motif regulate transcription of the Id2A promoter during myogenic differentiation. J Biol Chem 1994; 269: 31162-70
  9. Kreider B, Benezra R, Roverea G, Kadesch T. Inhi-bition of myeloid differentiation by the helix-loop-helix protein Id. Science 1992; 255: 1700-2 https://doi.org/10.1126/science.1372755
  10. Wilson RB, Kiledjian M, Shen CP, Benezra R, Zwo-llo P, Dymecki SM, Desiderio SV, Kadesch T. Repr-ession of immunoglobulin enhancers by the helix-loop-helix protein Id: Implication by B lymphoid development. Mol Cell Biol 1991; 11: 6185-91 https://doi.org/10.1128/MCB.11.12.6185
  11. Ogata T, Wozney JM, Benezra R, Noda M. Bone mo-rphogenetic protein 2 enhances expression of a gene Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cell. Proc Natl Acad Sci 1993; 90: 9219-22 https://doi.org/10.1073/pnas.90.19.9219
  12. Simonsen MS, Roosney A, Herman WH. Expression and differential regulation of Id1, a dominant nega-tive regulator of basic helix-loop-helix transcription factors, in glomerular mesangial cells. Nucleic Acid Res 1993; 21: 5767-74 https://doi.org/10.1093/nar/21.24.5767
  13. Mori S, Nishikawa SI, Yokota Y. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J 2000; 19: 5772-81 https://doi.org/10.1093/emboj/19.21.5772
  14. Sablitzky F, Moore A, Bromley M, Deed RW, Ne-wton JS, Norton JD. Stage- and subcellular-specific expression of Id proteins in male germ and Sertoli cells implicates distinctive regulatory roles for Id proteins during meiosis, spermatogenesis, and Sertoli cell function. Cell Growth Differ 1998; 9: 1015-24
  15. Nah HY, Hong SH, Lee JY, Chae HD, Kang BM, Kim CH. Id-1 expression in the mouse uterus. Kor J Fertil Steril 2003; 30: 171-8
  16. Hong SH, Nah HY, Lee JY, Kim CH, Gye MC, Kim MK. Analysis of estrogen-regulated genes in mouse uterus using cDNA microarray and laser capture mi-crodissection. J Endocrinol 2004; 181: 157-67 https://doi.org/10.1677/joe.0.1810157
  17. Reese J, Das SK, Paria BC, Lim H, Song H, Ma-tsumoto H, Knudtson KL, DuBois RN, Dey SK. Global gene expression analysis to identify mole-cular markers of uterine receptivity and embryo im-plantation. J Biol Chem 2001; 276: 44137-45 https://doi.org/10.1074/jbc.M107563200
  18. Watanabe H, Suzuki A, Mizutani T, Khono S, Lu-bahn DB, Handa H, Iguchi T. Genome-wide ana-lysis of changes in early gene expression induced by oestrogen. Genes Cells 2002; 7: 497-507 https://doi.org/10.1046/j.1365-2443.2002.00535.x
  19. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Man-ova K, Benezra R. Id1 and Id3 are required for ne-urogenesis, angiogenesis and vascularization of tu-mour xenografts. Nature 1999; 401: 670-7 https://doi.org/10.1038/44334
  20. Brooks PC, Montgomery AM, Rosenfeld M, Rei-sfeld RA, Hu T, Klier G, Cheresh DA. Localization of matrix metalloproteinase MMP2 to the surface of invasive cells by interaction with integrin alpha beta v 3. Cell 1994; 79: 1157-64 https://doi.org/10.1016/0092-8674(94)90007-8
  21. Jen Y, Manova K, Benezra R. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. 1997; Dev Dyn 208: 92-106
  22. Chaudhary J, Johnson J, Kim G, Skinner MK. Hor-monal regulation and differential actions of the helix-loop-helix transcriptional inhibitors of differentiation (Id1, Id2, Id3 and Id4) in Sertoli cells. Endocrino-logy 2001; 142: 1727-36 https://doi.org/10.1210/en.142.5.1727