Conservation of cis-Regulatory Element Controlling Timely Translation in the 3'-UTR of Selected Mammalian Maternal Transcripts

  • Lee, Hyun-Joo (Department of Bioengineering, Hankyong National University) ;
  • Lim, Yoon-Ki (Department of Bioengineering, Hankyong National University) ;
  • Chang, Sang-Ho (Department of Bioengineering, Hankyong National University) ;
  • Min, Kwan-Sik (Graduate School of Biotechnology, Environmental and Information Technology, Hankyong National University) ;
  • Han, Ching-Tack (Department of Life Science, Sogang University) ;
  • Hwang, Sue-Yun (Graduate School of Biotechnology, Environmental and Information Technology, Hankyong National University)
  • Published : 2007.12.31

Abstract

The earliest stages of mammalian embryogenesis are governed by the activity of maternally inherited transcripts and proteins. Cytoplasmic polyadenylation of selected maternal mRNA has been reported to be a major control mechanism of delayed translation during preimplantation embryogenesis in mice. The presence of cis-elements required for cytoplasmic polyadenylation (e.g., CPE) can serve as a useful tag in the screening of maternal genes partaking in key functions in the transcriptionally dormant egg and early embryo. However, due to its relative simplicity, UA-rich sequences satisfying the canonical rule of known CPE consensus sequences are often found in the 3'-UTR of maternal transcripts that do not actually undergo cytoplasmic polyadenylation. In this study, we developed a method to confirm the validity of candidate CPE sequences in a given gene by a multiplex comparison of 3'-UTR sequences between mammalian homologs. We found that genes undergoing cytoplasmic polyadenylation tend to create a conserved block around the CPE, while CPE-like sequences in the 3'-UTR of genes lacking cytoplasmic polyadenylation do not exhibit such conservation between species. Through this cross-species comparison, we also identified an alternative CPE in the 3'-UTR of tissue-type plasminogen activator (tPA), which is more likely to serve as a functional element. We suggest that verification of CPEs based on sequence conservation can provide a convenient tool for mass screening of factors governing the earliest processes of mammalian embryogenesis.

Keywords

References

  1. Choi, H.S., Kim, D.W., and Ryu, W. (2006). A pattern summary system using BLAST for sequence analysis. Genomics & Informatics 4. 173-181
  2. Davidson, E.H. (1986). Gene activity in early development. Academic Press. New York
  3. de Moore, C. and Richter, J. (1999). Cytoplasmic polyadenylation elements mediate kasking and unmasking of cyclin B1 mRNA. EMBO J. 18. 2294-2303 https://doi.org/10.1093/emboj/18.8.2294
  4. de Moore, C. and Richter, J. (2001). Translational control in vertebrate development. Int Rev Cytol. 203. 567-608 https://doi.org/10.1016/S0074-7696(01)03017-0
  5. Gebauer, F., Xu, W., Cooper, J., and Richter, J. (1994). Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 13. 5712-5720
  6. Gebauer, F., and Richter, J. (1996). Mouse cytoplasmic polyadenylation element binding protein: An evolutionary conserved protein that interact with the cytoplasmic polyadenylation elements of c-mos mRNA. Proc Natil Acad Sci USA. 93. 14602-14607
  7. Huarte, J., Belin, A., Vassali, S., and Strickland, S. (1987). Meiotic maturation of mouse oocyte triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA. Genes Develop. 1. 1201-1211 https://doi.org/10.1101/gad.1.10.1201
  8. Hwang, S.Y., Oh, B., Solter, D., Knowles, B., and Lee, J.S. (2001). Expression of genes involved in the mammalian meiosis during the transition from the egg to embryo. Mol Rep Devel. 59. 144-158 https://doi.org/10.1002/mrd.1017
  9. Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5. 150-163 https://doi.org/10.1093/bib/5.2.150
  10. Lee, J.S., Choi, K.D., Lee, S.Y., Min, K.S., and Hwang, S.Y. (2006). Maternal contribution of cell death regulatory genes in early mouse and chick embryogenesis: an in silico analysis using EST database and homology search. Korean J Genetics. 28 107-117
  11. Liberfarb, M., Chu, T., Wreden, C., Theurkauf, W., Gergen, P., and Strickland, S. (1996). Mutations that perturb poly(A)-dependent maternal mRNA activation block the initiation of development. Development. 122 579-588
  12. Mendez, R., and Richter, J. (2001). Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol. 2. 521-529 https://doi.org/10.1038/35080081
  13. Oh, B., Hwang, S.Y., Solter, D., and Knowles, B. (1997). Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo. Development. 124. 493-500
  14. Oh, B., Hwang, S.Y., McLaughlin, K., Solter, D., and Knowles, B. (2000). Timely translation during the mouse ooctye to embryo transition. Development. 127. 3795-3803
  15. Ohsugi, M., Hwang, S.Y., Butz, S., Knowles, B., Solter, D., and Kemler, R. (1996). Expression and cell membrane localization of catenins during mouse preimplantation development. Dev Dynamic. 206. 391-402 https://doi.org/10.1002/(SICI)1097-0177(199608)206:4<391::AID-AJA5>3.0.CO;2-D
  16. Paschoud, S., Dogar, A., Kruntz, C., Grisoni-Neupert, B., Richman, L., and Kuehn, L. (2006). Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol Cell Biol. 2006. 8228-8241
  17. Read, R., and Norbury, C. (2002). Roles for cytoplasmic polyadenylation in cell cycle regulation. J Cell Biochem. 87 258-265 https://doi.org/10.1002/jcb.10300
  18. Richards, W., Carroll, P., Kinlock, R., Wassarman, P., and Strickland, S. (1993). Creating maternal effect mutations in transgenic mice: antisense inhibition of an oocyte gene product. Dev Biol. 160. 543-553 https://doi.org/10.1006/dbio.1993.1328
  19. Richter, J. (1999). Cytoplasmic polyadenylation in development and beyond. Microbiol Mol Biol Rev. 63. 446-456
  20. Seko, Y., Cole, S., Kasprzak, W., Shapiro, B., and Ragheb, J. (2006). The role of cytokine mRNA stability in the pathogenesis of autoimmune diseases. Autoimmun Rev. 5. 299-305 https://doi.org/10.1016/j.autrev.2005.10.013
  21. Stebbins-Boaz, B., and Richter, J. (1997). Translational control during early development. Crit Rev Eukayot Gene Expr. 7. 73-94 https://doi.org/10.1615/CritRevEukarGeneExpr.v7.i1-2.50