Skip to main content

Advertisement

SpringerLink
Log in

MicroRNA Expression Profile in Murine Central Nervous System Development

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) regulate gene expression in a post-transcriptional sequence-specific manner. In order to better understand the possible roles of miRNAs in central nervous system (CNS) development, we examined the expression profile of 104 miRNAs during murine brain development. We obtained brain samples from animals at embryonic days (E) E15, E17, and postnatal days (P) P1 and P7. Total RNA was isolated from tissue and used to obtain mature miRNAs by reverse transcription. Our results indicate that there is a group of 12 miRNAs that show a distinct expression profile, with the highest expression during embryonic stages and decreasing significantly during development. This profile suggests key roles in processes occurring during early CNS development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Ambros, V. (2004). The functions of animal microRNAs. Nature, 431, 350–355.

    Article  PubMed  CAS  Google Scholar 

  • Ayres, M., Ayres, M., Jr., Ayres, D. L., & Dos Santos, A. S. (2003). BioEstat 3.0: Aplicações estatísticas nas áreas das Ciências Biológicas e Médicas. Belém: Sociedade civil Mamiruá, Brasília.

    Google Scholar 

  • Bartel, D. P. (2004). MicroRNAs: Genomics, biogenesis, mechanism and functions. Cell, 23, 281–297.

    Article  Google Scholar 

  • Bellefroid, E. J., Bourguignon, C., Hollemann, T., Ma, Q., Anderson, D. J., Kintner, C., et al. (1996). X-MyT1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell, 87(7), 1191–1202.

    Article  PubMed  CAS  Google Scholar 

  • Chen, C., Ridzon, D. A., Broomer, A. J., Zhou, Z., Lee, D. H., Nguyen, J. T., et al. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research, 33(20), e179.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, S. M., & Brennecke, J. (2006). Developmental biology. Mixed messages in early development. Science, 312(5770), 65–66.

    Article  PubMed  CAS  Google Scholar 

  • Conaco, C., Otto, S., Han, J. J., & Mandel, G. (2006). Reciprocal actions of REST and a microRNA promote neuronal identity. Proceedings of the National Academy of Sciences of the United States of America, 103(7), 2422–2427.

    Article  PubMed  CAS  Google Scholar 

  • Emsley, J. G., & Hagg, T. (2003). Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice. Experimental Neurology, 183(2), 298–310.

    Article  PubMed  CAS  Google Scholar 

  • Franklin, A., Kao, A., Tapscott, S., & Unis, A. (2001). NeuroD homologue expression during cortical development in the human brain. Journal of Child Neurology, 16(11), 849–853.

    Article  PubMed  CAS  Google Scholar 

  • Gazit, R., Krizhanovsky, V., & Ben-Arie, N. (2004). Math1 controls cerebellar granule cell differentiation by regulating multiple components of the Notch signaling pathway. Development, 131(4), 903–913.

    Article  PubMed  CAS  Google Scholar 

  • Herrero, J., & Dopazo, J. (2002). Combining hierarchical clustering and self-organizing maps for exploratory analysis of gene expression pattern. Journal of Proteome Research, 1, 467–470.

    Article  PubMed  CAS  Google Scholar 

  • Ketting, R. F., Fischer, S. E., Bernstein, E., Sijen, T., Hannon, G. J., & Plasterk, R. H. (2001). Dicer functions in RNA interference and in synthesis of small RNA involved in development timing in C. elegans. Genes & Development, 15(20), 2654–2659.

    Article  CAS  Google Scholar 

  • Kim, V. N. (2005). MicroRNA biogenesis: Coordinated cropping and dicing. Nature Reviews. Molecular Cell Biology, 6(5), 376–385.

    Article  PubMed  CAS  Google Scholar 

  • Kloosterman, W. P., & Plasterk, R. H. (2006). The diverse functions of microRNAs in animal development and disease. Developmental Cell, 11(4), 441–450.

    Article  PubMed  CAS  Google Scholar 

  • Koh, J. T., Lee, Z. H., Ahn, K. Y., Kim, J. K., Bae, C. S., Kim, H. H., et al. (2001). Characterization of mouse brain-specific angiogenesis inhibitor 1 (BAI1) and phytanoyl-CoA alpha-hydroxylase-associated protein 1, a novel BAI1-binding protein. Molecular Brain Research, 87(2), 223–237.

    Article  PubMed  CAS  Google Scholar 

  • Kohonen, T. (1997). Self-organizing maps. New York, NY: Springer.

    Google Scholar 

  • Kosik, K. S. (2006). The neuronal microRNA system. Nature Reviews. Neuroscience, 7(12), 911–920.

    Article  PubMed  CAS  Google Scholar 

  • Kosik, K. S., & Krichevsky, A. M. (2005). The elegance of microRNAs: a neuronal perspective. Neuron, 47(6), 779–782.

    Article  PubMed  CAS  Google Scholar 

  • Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K., & Kosik, K. S. (2003). A microRNA array reveals extensive regulation of microRNAs during brain development. RNA, 9(10), 1274–1281.

    Article  PubMed  CAS  Google Scholar 

  • Krichevsky, A. M., Sonntag, K. C., Isacson, O., & Kosik, K. S. (2006). Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells, 24(4), 857–864.

    Article  PubMed  CAS  Google Scholar 

  • Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., Sontheimer, E. J., & Carthew, R. W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell, 117(1), 69–81.

    Article  PubMed  CAS  Google Scholar 

  • Li, H., Wu, D. K., & Sullivan, S. L. (1999). Characterization and expression of sema4g, a novel member of the semaphorin gene family. Mechanisms of Development, 87(1–2), 169–173.

    Article  PubMed  CAS  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the \(2_{\text{T}}^{\Delta \Delta {\text{C}}} \) method. Methods, 25(4), 402–408.

    Article  PubMed  CAS  Google Scholar 

  • Maniatis, T., & Tasic, B. (2002). Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature, 418(6894), 236–243.

    Article  PubMed  CAS  Google Scholar 

  • Mansfield, J. H., Harfe, B. D., Nissen, R., Obenauer, J., Srineel, J., Chaudhuri, A., et al. (2004). MicroRNA-responsive ‘sensor’ transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nature Genetics, 36(10), 1079–1083.

    Article  PubMed  CAS  Google Scholar 

  • Margolis, F. L., Verhaagen, J., Biffo, S., Huang, F. L., & Grillo, M. (1991). Regulation of gene expression in the olfactory neuroepithelium: A neurogenetic matrix. Progress in Brain Research, 89, 97–122.

    Article  PubMed  CAS  Google Scholar 

  • Miska, E. A., Alvarez-Saavedra, E., Townsend, M., Yoshii, A., Sestan, N., Rakic, P., et al. (2004). Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biology, 5(9), R68.

    Article  PubMed  Google Scholar 

  • Musunuru, K., & Darnell, R. B. (2001). Paraneoplastic neurologic disease antigens: RNA-binding proteins and signaling proteins in neuronal degeneration. Annual Review of Neuroscience, 24, 239–262.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, P. T., Hatzigeorgiou, A. G., & Mourelatos, Z. (2004). miRNP: mRNA association in polyribosome in a human neuronal cell line. RNA, 10(3), 387–394.

    Article  PubMed  CAS  Google Scholar 

  • Peters, L., & Meister, G. (2007). Argonaute proteins: Mediators of RNA silencing. Molecular Cell, 26(5), 611–623.

    Article  PubMed  CAS  Google Scholar 

  • Przyborski, S. A., Morton, I. E., Wood, A., & Andrews, P. W. (2000). Developmental regulation of neurogenesis in the pluripotent human embryonal carcinoma cell line NTERA-2. European Journal of Neuroscience, 12(10), 3521–3528.

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2007). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org.ent).

  • Sethupathy, P., Megraw, M., & Hatzigeorgiou, A. G. (2006). A guide through present computational approaches for the identification of mammalian microRNA targets. Nature Methods, 3, 881–886.

    Article  PubMed  CAS  Google Scholar 

  • Shanley, D. K., & Sullivan, A. M. (2007). Expression of the cell surface markers mAb 2F7 and PSA-NCAM in the embryonic rat brain. Neuroscience Letters, 424(3), 165–169.

    Article  PubMed  CAS  Google Scholar 

  • Smirnova, L., Grafe, A., Seiler, A., Schumacher, S., Nitsch, R., & Wulczyn, F. G. (2005). Regulation of miRNA expression during neural cell specification. European Journal of Neuroscience, 21(6), 1469–1477.

    PubMed  Google Scholar 

  • Steward, O., & Schuman, E. M. (2003). Compartmentalized synthesis and degradation of proteins in neurons. Neuron, 40(2), 347–359.

    Article  PubMed  CAS  Google Scholar 

  • Strauss, W. M., Chen, C., Lee, C. T., & Ridzon, D. (2006). Nonrestrictive developmental regulation of microRNA gene expression. Mammalian Genome, 17(8), 833–840.

    Article  PubMed  CAS  Google Scholar 

  • Strom, A.-L., Jonasson, J., Hart, P., Brannstrom, T., Forsgren, L., & Holmberg, M. (2002). Cloning and expression analysis of the murine homolog of the spinocerebellar ataxia type 7 (SCA7) gene. Gene, 285, 91–99.

    Article  PubMed  CAS  Google Scholar 

  • Tiedge, H., Bloom, F. E., & Richter, D. (1999). RNA, whither goest thou? Science, 283(5399), 186–187.

    Article  PubMed  CAS  Google Scholar 

  • Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., et al. (2005). A cAMP-response element binding protein-indiced microRNA regulates neuronal morphogenesis. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16426–16431.

    Article  PubMed  CAS  Google Scholar 

  • Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., et al. (2005). MicroRNA expression in zebrafish embryonic development. Science, 309(5732), 310–311.

    Article  PubMed  CAS  Google Scholar 

  • Wienholds, E., & Plasterk, R. H. (2005). MicroRNA function in animal development. FEBS, 597(26), 5911–5922.

    Article  CAS  Google Scholar 

  • Wulczyn, F. G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., et al. (2007). Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB Journal, 21(2), 415–426.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, B., Pan, X., & Anderson, T. A. (2006). MicroRNA: A new player in stem cells. Journal of Cellular Physiology, 209(2), 266–269.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, N., Hashida, H., Takahashi, N., & Sakaki, Y. (1994). Cloning and sequence analysis of the human SNAP25 cDNA. Gene, 145(2), 313–314.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical Genetics, Faculty of Medical Sciences, University of Campinas—UNICAMP, Tessália Vieira de Camargo, 126, Campinas, 13084-971, Sao Paulo, Brazil

    Danyella B. Dogini, Patrícia A. O. Ribeiro, Cristiane Rocha, Tiago C. Pereira & Iscia Lopes-Cendes

Authors
  1. Danyella B. Dogini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrícia A. O. Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristiane Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tiago C. Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Iscia Lopes-Cendes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iscia Lopes-Cendes.

Additional information

This paper was supported by the National Council for Scientific and Technological Development (CNPq) and the State of Sao Paulo Research Foundation (FAPESP).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dogini, D.B., Ribeiro, P.A.O., Rocha, C. et al. MicroRNA Expression Profile in Murine Central Nervous System Development. J Mol Neurosci 35, 331–337 (2008). https://doi.org/10.1007/s12031-008-9068-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-008-9068-4

Keywords

Search

Navigation