Skip to main content
Log in

Expression and imprinting analysis of AK044800, a transcript from the Dlk1-Dio3 imprinted gene cluster during mouse embryogenesis

  • Research Article
  • Published:
Molecules and Cells

Abstract

Recent advances of induced pluripotent stem cells (iPSCs) has demonstrated that full development potential is closely related with the expression state of noncoding RNAs (ncRNAs) of the Dlk1-Dio3 imprinted gene cluster. However, few of them, especially the long noncoding RNAs (lncRNAs), have been characterized in detail. AK044800 is a transcript from the Dlk1-Dio3 imprinted region with little known information. This study reports original data on the expression pattern of AK044800 during embryogenesis. Expression analysis showed that AK044800 was specifically expressed in the brain at mid-gestation, E9.5 and E11.5. And at E15.5, its expression was mainly concentrated in the forebrain. In the late-gestation stage (E18.5), AK044800 expression was weaker in the brain and began to emerge in some other tissues during this period. Notably, the expression of AK044800 was biallelic in the brain, unlike other noncoding transcripts from this imprinted region. In addition, its expression was dependent on inbred mouse strains. This may be the first lncRNA that has been identified with a different expression between inbred mouse strains. This study may provide useful clues for further investigations of expression regulation and functions of lncRNAs of the Dlk1-Dio3 imprinted region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Charalambous, M., da Rocha, S.T., and Ferguson-Smith, A.C. (2007). Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr. Opin. Endocrinol. Diabetes Obes. 14, 3–12.

    Article  PubMed  CAS  Google Scholar 

  • da Rocha, S.T., Edwards, C.A., Ito, M., Ogata, T., and Ferguson-Smith, A.C. (2008). Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet. 24, 306–316.

    Article  PubMed  Google Scholar 

  • Giardino, W.J., Cote, D.M., Li, J., and Ryabinin, A.E. (2012). Characterization of genetic differences within the centrally projecting edinger-westphal nucleus of C57BL/6J and DBA/2J mice by expression profiling. Front Neuroanat. 6, 5.

    PubMed  CAS  Google Scholar 

  • Gieryk, A., Ziolkowska, B., Solecki, W., Kubik, J., and Przewlocki, R. (2010). Forebrain PENK and PDYN gene expression levels in three inbred strains of mice and their relationship to genotype-dependent morphine reward sensitivity. Psychopharmacology (Berl) 208, 291–300.

    Article  CAS  Google Scholar 

  • Gu, T., He, H., Xing, Y., Liu, Q., Gu, N., Kenkichi, S., Jiang, H., and Wu, Q. (2011). Expression of non-coding RNA AB063319 derived from Rian gene during mouse development. J. Mol. Histol. 42, 105–112.

    Article  PubMed  CAS  Google Scholar 

  • Gu, T., He, H., Han, Z., Zeng, T., Huang, Z., Liu, Q., Gu, N., Chen, Y., Sugimoto, K., Jiang, H., et al. (2012). Expression of macro non-coding RNAs Meg8 and Irm in mouse embryonic development. Acta Histochem. 114, 392–399.

    Article  PubMed  CAS  Google Scholar 

  • Guttman, M., Amit, I., Garber, M., French, C., Lin, M.F., Feldser, D., Huarte, M., Zuk, O., Carey, B.W., Cassady, J.P., et al. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223–227.

    Article  PubMed  CAS  Google Scholar 

  • Hagan, J.P., O’Neill, B.L., Stewart, C.L., Kozlov, S.V., and Croce, C.M. (2009). At least ten genes define the imprinted Dlk1-Dio3 cluster on mouse chromosome 12qF1. PLoS One 4, e4352.

    Article  PubMed  Google Scholar 

  • Han, Z., He, H., Zhang, F., Huang, Z., Liu, Z., Jiang, H., and Wu, Q. (2012). Spatiotemporal expression pattern of Mirg, an imprinted non-coding gene, during mouse embryogenesis. J. Mol. Histol. 43, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Jamensky, N.T., and Gianoulakis, C. (1997). Content of dynorphins and kappa-opioid receptors in distinct brain regions of C57BL/6 and DBA/2 mice. Alcohol. Clin. Exp. Res. 21, 1455–1464.

    PubMed  CAS  Google Scholar 

  • Jamensky, N.T., and Gianoulakis, C. (1999). Comparison of the proopiomelanocortin and proenkephalin opioid peptide systems in brain regions of the alcohol-preferring C57BL/6 and alcoholavoiding DBA/2 mice. Alcohol 18, 177–187.

    Article  PubMed  CAS  Google Scholar 

  • Lin, S.P., Coan, P., da Rocha, S.T., Seitz, H., Cavaille, J., Teng, P.W., Takada, S., and Ferguson-Smith, A.C. (2007). Differential regulation of imprinting in the murine embryo and placenta by the Dlk1-Dio3 imprinting control region. Development 134, 417–426.

    Article  PubMed  CAS  Google Scholar 

  • Liu, L., Luo, G.Z., Yang, W., Zhao, X., Zheng, Q., Lv, Z., Li, W., Wu, H.J., Wang, L., Wang, X.J., et al. (2010). Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J. Biol. Chem. 285, 19483–19490.

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin, D., Vidaki, M., Renieri, E., and Karagogeos, D. (2006). Expression pattern of the maternally imprinted gene Gtl2 in the forebrain during embryonic development and adulthood. Gene Expr. Patterns 6, 394–399.

    Article  PubMed  CAS  Google Scholar 

  • Mercer, T.R., Dinger, M.E., Sunkin, S.M., Mehler, M.F., and Mattick, J.S. (2008). Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA 105, 716–721.

    Article  PubMed  CAS  Google Scholar 

  • Mercer, T.R., Qureshi, I.A., Gokhan, S., Dinger, M.E., Li, G., Mattick, J.S., and Mehler, M.F. (2010). Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci. 11, 14.

    Article  PubMed  Google Scholar 

  • Olivier, B., and Walter, W. (1998). A simplified in situ hybridization protocol using non-radioactivety labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1, 10–16.

    Google Scholar 

  • Parsons, M.J., Grimm, C.H., Paya-Cano, J.L., Sugden, K., Nietfeld, W., Lehrach, H., and Schalkwyk, L.C. (2008). Using hippocampal microRNA expression differences between mouse inbred strains to characterise miRNA function. Mamm. Genome 19, 552–560.

    Article  PubMed  CAS  Google Scholar 

  • Peirce, J.L., Derr, R., Shendure, J., Kolata, T., and Silver, L.M. (1998). A major influence of sex-specific loci on alcohol preference in C57Bl/6 and DBA/2 inbred mice. Mamm. Genome 9, 942–948.

    Article  PubMed  CAS  Google Scholar 

  • Ponjavic, J., Oliver, P.L., Lunter, G., and Ponting, C.P. (2009). Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet. 5, e1000617.

    Article  PubMed  Google Scholar 

  • Qureshi, I.A., and Mehler, M.F. (2012). Emerging roles of noncoding RNAs in brain evolution, development, plasticity and disease. Nat. Rev. Neurosci. 13, 528–541.

    Article  PubMed  CAS  Google Scholar 

  • Qureshi, I.A., Mattick, J.S., and Mehler, M.F. (2010). Long noncoding RNAs in nervous system function and disease. Brain Res. 1338, 20–35.

    Article  PubMed  CAS  Google Scholar 

  • Schuster-Gossler, K., Bilinski, P., Sado, T., Ferguson-Smith, A., and Gossler, A. (1998). The mouse Gtl2 gene is differentially expressed during embryonic development, encodes multiple alternatively spliced transcripts, and may act as an RNA. Dev. Dyn. 212, 214–228.

    Article  PubMed  CAS  Google Scholar 

  • Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., Natesan, S., Kono, T., Shioda, T., and Hochedlinger, K. (2010). Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465, 175–181.

    Article  PubMed  CAS  Google Scholar 

  • Tapocik, J.D., Luu, T.V., Mayo, C.L., Wang, B.D., Doyle, E., Lee, A.D., Lee, N.H., and Elmer, G.I. (2012). Neuroplasticity, axonal guidance and micro-RNA genes are associated with morphine self-administration behavior. Addict. Biol. [Epub ahead of print]

    Google Scholar 

  • Tevendale, M., Watkins, M., Rasberry, C., Cattanach, B., and Ferguson-Smith, A.C. (2006). Analysis of mouse conceptuses with uniparental duplication/deficiency for distal chromosome 12: comparison with chromosome 12 uniparental disomy and implications for genomic imprinting. Cytogenet. Genome Res. 113, 215–222.

    Article  PubMed  CAS  Google Scholar 

  • Tierling, S., Dalbert, S., Schoppenhorst, S., Tsai, C.E., Oliger, S., Ferguson-Smith, A.C., Paulsen, M., and Walter, J. (2006). Highresolution map and imprinting analysis of the Gtl2-Dnchc1 domain on mouse chromosome 12. Genomics 87, 225–235.

    Article  PubMed  CAS  Google Scholar 

  • Tsai, C.E., Lin, S.P., Ito, M., Takagi, N., Takada, S., and Ferguson-Smith, A.C. (2002). Genomic imprinting contributes to thyroid hormone metabolism in the mouse embryo. Curr. Biol. 12, 1221–1226.

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson, L.S., Davies, W., and Isles, A.R. (2007). Genomic imprinting effects on brain development and function. Nat. Rev. Neurosci. 8, 832–843.

    Article  PubMed  CAS  Google Scholar 

  • Yevtodiyenko, A., Carr, M.S., Patel, N., and Schmidt, J.V. (2002). Analysis of candidate imprinted genes linked to Dlk1-Gtl2 using a congenic mouse line. Mamm. Genome 13, 633–638.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiong Wu.

About this article

Cite this article

Han, Z., Liu, Q., Huang, Z. et al. Expression and imprinting analysis of AK044800, a transcript from the Dlk1-Dio3 imprinted gene cluster during mouse embryogenesis. Mol Cells 35, 285–290 (2013). https://doi.org/10.1007/s10059-013-2275-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10059-013-2275-z

Keywords

Navigation