A novel class of small RNAs bind to MILI protein in mouse testes (original) (raw)

References

  1. Meister, G. & Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343–349 (2004)
    Article ADS CAS Google Scholar
  2. Mello, C. C. & Conte, D. Jr. Revealing the world of RNA interference. Nature 431, 338–342 (2004)
    Article ADS CAS Google Scholar
  3. Matzke, M. A. & Birchler, J. A. RNAi-mediated pathways in the nucleus. Nature Rev. Genet. 6, 24–35 (2005)
    Article CAS Google Scholar
  4. Zamore, P. D. & Haley, B. Ribo-gnome: the big world of small RNAs. Science 309, 1519–1524 (2005)
    Article ADS CAS Google Scholar
  5. Carmell, M. A., Xuan, Z., Zhang, M. Q. & Hannon, G. J. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733–2742 (2002)
    Article CAS Google Scholar
  6. Cox, D. N. et al. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715–3727 (1998)
    Article CAS Google Scholar
  7. Reddien, P. W., Oviedo, N. J., Jennings, J. R., Jenkin, J. C. & Sanchez Alvarado, A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310, 1327–1330 (2005)
    Article ADS CAS Google Scholar
  8. Kuramochi-Miyagawa, S. et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131, 839–849 (2004)
    Article CAS Google Scholar
  9. Deng, W. & Lin, H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2, 819–830 (2002)
    Article CAS Google Scholar
  10. Aravin, A. A. et al. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337–350 (2003)
    Article CAS Google Scholar
  11. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004)
    Article CAS Google Scholar
  12. Chen, P. Y. et al. The developmental miRNA profiles of zebrafish as determined by small RNA cloning. Genes Dev. 19, 1288–1293 (2005)
    Article CAS Google Scholar
  13. Bellve, A. R. et al. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74, 68–85 (1977)
    Article CAS Google Scholar
  14. Siepel, A. et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034–1050 (2005)
    Article CAS Google Scholar
  15. Mochizuki, K. & Gorovsky, M. A. Small RNAs in genome rearrangement in Tetrahymena. Curr. Opin. Genet. Dev. 14, 181–187 (2004)
    Article CAS Google Scholar
  16. Grewal, S. I. & Rice, J. C. Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol. 16, 230–238 (2004)
    Article CAS Google Scholar
  17. Jenab, S. & Morris, P. L. Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells. Endocrinology 139, 1883–1890 (1998)
    Article CAS Google Scholar
  18. Pfeffer, S. et al. Identification of microRNAs of the herpesvirus family. Nature Methods 2, 269–276 (2005)
    Article CAS Google Scholar
  19. Pfeffer, S., Lagos-Quintana, M. & Tuschl, T. in Current Protocols in Molecular Biology (eds Ausubel, F. M. et al.) 26.4.1–26.4.18 (John Wiley and Sons, New York, 2003)
    Google Scholar
  20. Lagos-Quintana, M. et al. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735–739 (2002)
    Article CAS Google Scholar
  21. Pfeffer, S. et al. Identification of virus-encoded microRNAs. Science 304, 734–736 (2004)
    Article ADS CAS Google Scholar
  22. Lim, L. P., Glasner, M. E., Yekta, S., Burge, C. B. & Bartel, D. P. Vertebrate microRNA genes. Science 299, 1540 (2003)
    Article CAS Google Scholar
  23. Berezikov, E. et al. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 120, 21–24 (2005)
    Article CAS Google Scholar
  24. Legendre, M., Lambert, A. & Gautheret, D. Profile-based detection of microRNA precursors in animal genomes. Bioinformatics 21, 841–845 (2005)
    Article CAS Google Scholar
  25. Pruitt, K. D., Tatusova, T. & Maglott, D. R. NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 33, D501–D504 (2005)
    Article CAS Google Scholar

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Acknowledgements

We thank J. Brennecke, M. Landthaler, Y. Pei, K. Fejes Toth and A. Sewer for discussion and help with the manuscript. We also thank L. Mitchell and K. Hwang for expert assistance in germ-cell purification, M. Poy and M. Stoffel for providing mouse tissues, and D. Weir and R. Choksi for assistance with sequencing. This work was supported by a FRAXA Research Foundation postdoctoral fellowship to A.A., an NIH grant to P.M., NIH grants to T.T., and an SNF grant to M.Z. Author Contributions A.A., S.P. and M.L.-Q. prepared the mouse, and P.L. and N.I. the human, testes small RNA libraries. A.A. recognized the presence of piRNAs, performed the MILI IPs, prepared the MILI-interacting small RNA library, and performed, together with N.I., the northern blotting analysis. S.K.-M. and T.N. produced, characterized and purified the MILI antibody. T.T. developed the concept of cloning from Ago/Piwi IPs. P.M. isolated germline cells. M.C., J.J.R. and J.J. performed the large-scale sequencing. The bioinformatic analyses of piRNAs were designed and carried out by D.G. and M.Z. with input from A.A. and T.T. The database of RNAs with known function was compiled by M.Z., R.S., P.L. and S.P., the software used for small RNA annotation was developed by M.Z., R.S. and C.S., and the manuscript was written by A.A., M.Z. and T.T.

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Author notes

  1. Alexei Aravin
    Present address: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York, 11724, USA
  2. Sébastien Pfeffer
    Present address: CNRS-UPR 2357, IBMP, 12 rue du Général Zimmer, 67084, Strasbourg Cedex, France
  3. Alexei Aravin and Dimos Gaidatzis: *These authors contributed equally to this work

Authors and Affiliations

  1. Howard Hughes Medical Institute, Laboratory of RNA Molecular Biology, The Rockefeller University, New York, 1230 York Avenue, Box 186, New York, 10021, USA
    Alexei Aravin, Sébastien Pfeffer, Mariana Lagos-Quintana, Pablo Landgraf, Nicola Iovino & Thomas Tuschl
  2. Biozentrum, Universität Basel, Basel, Klingelbergstr 50-70, CH-4056, Switzerland
    Dimos Gaidatzis & Mihaela Zavolan
  3. Population Council, The Rockefeller University, New York, 1230 York Avenue, New York, 10021, USA
    Patricia Morris
  4. J. Craig Venter Institute, Functional Genomics, Rockville, 9704 Medical Center Drive, Maryland, 20850, USA
    Michael J. Brownstein
  5. Department of Pathology, Medical School, Graduate School of Frontier Biosciences, Osaka University, Osaka, Yamada-oka 2-2 Suita, 565-0871, Japan
    Satomi Kuramochi-Miyagawa & Toru Nakano
  6. Columbia Genome Center, Russ Berrie Pavilion, New York, 1150 St. Nicholas Avenue, New York, 10032, USA
    Minchen Chien, James J. Russo & Jingyue Ju
  7. Department of Chemical Engineering, Columbia University, New York, 500 West 120 Street, New York, 10027, USA
    Jingyue Ju
  8. Computational Biology Center, Memorial Sloan-Kettering Cancer Center, New York, New York, 10021, USA
    Robert Sheridan & Chris Sander
  9. Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York, 11724, USA
    Sébastien Pfeffer
  10. CNRS-UPR 2357, IBMP, 12 rue du Général Zimmer, 67084, Strasbourg Cedex, France
    Alexei Aravin

Authors

  1. Alexei Aravin
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  2. Dimos Gaidatzis
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  3. Sébastien Pfeffer
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  4. Mariana Lagos-Quintana
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  5. Pablo Landgraf
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  6. Nicola Iovino
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  7. Patricia Morris
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  8. Michael J. Brownstein
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  9. Satomi Kuramochi-Miyagawa
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  10. Toru Nakano
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  11. Minchen Chien
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  12. James J. Russo
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  13. Jingyue Ju
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  14. Robert Sheridan
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  15. Chris Sander
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  16. Mihaela Zavolan
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  17. Thomas Tuschl
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Corresponding authors

Correspondence toMihaela Zavolan or Thomas Tuschl.

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Competing interests

Sequences of the piRNAs determined in this paper are given in Supplementary Tables 4 and 9. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Aravin, A., Gaidatzis, D., Pfeffer, S. et al. A novel class of small RNAs bind to MILI protein in mouse testes.Nature 442, 203–207 (2006). https://doi.org/10.1038/nature04916

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