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Science 313 (5785): 363-367

Copyright © 2006 by the American Association for the Advancement of Science

Characterization of the piRNA Complex from Rat Testes

Nelson C. Lau,1* Anita G. Seto,1* Jinkuk Kim,2,3 Satomi Kuramochi-Miyagawa,4 Toru Nakano,4 David P. Bartel,3,5 Robert E. Kingston1{dagger}

Abstract: Small noncoding RNAs regulate processes essential for cell growth and development, including mRNA degradation, translational repression, and transcriptional gene silencing (TGS). During a search for candidate mammalian factors for TGS, we purified a complex that contains small RNAs and Riwi, the rat homolog to human Piwi. The RNAs, frequently 29 to 30 nucleotides in length, are called Piwi-interacting RNAs (piRNAs), 94% of which map to 100 defined (≤101 kb) genomic regions. Within these regions, the piRNAs generally distribute across only one genomic strand or distribute on two strands but in a divergent, nonoverlapping manner. Preparations of piRNA complex (piRC) contain rRecQ1, which is homologous to qde-3 from Neurospora, a gene implicated in silencing pathways. Piwi has been genetically linked to TGS in flies, and slicer activity cofractionates with the purified complex. These results are consistent with a gene-silencing role for piRC in mammals.

1 Department of Molecular Biology, Massachusetts General Hospital, 185 Cambridge Street, Boston, MA 02114, USA.
2 Harvard-MIT Division of Health Sciences and Technology, E18-435, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
3 Howard Hughes Medical Institute and Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, MA 02142, USA.
4 Department of Molecular Cell Biology, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamada-oka, Suita-shi, Osaka 565-0871, Japan.
5 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: kingston{at}molbio.mgh.harvard.edu


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Abstract »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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E. P. Murchison, P. Kheradpour, R. Sachidanandam, C. Smith, E. Hodges, Z. Xuan, M. Kellis, F. Grutzner, A. Stark, and G. J. Hannon (2008)
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   Abstract »    Full Text »    PDF »
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S. Kuramochi-Miyagawa, T. Watanabe, K. Gotoh, Y. Totoki, A. Toyoda, M. Ikawa, N. Asada, K. Kojima, Y. Yamaguchi, T. W. Ijiri, et al. (2008)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members.
T. A. Farazi, S. A. Juranek, and T. Tuschl (2008)
Development 135, 1201-1214
   Abstract »    Full Text »    PDF »
Long, abundantly expressed non-coding transcripts are altered in cancer.
D. S. Perez, T. R. Hoage, J. R. Pritchett, A. L. Ducharme-Smith, M. L. Halling, S. C. Ganapathiraju, P. S. Streng, and D. I. Smith (2008)
Hum. Mol. Genet. 17, 642-655
   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
SnoReport: computational identification of snoRNAs with unknown targets.
J. Hertel, I. L. Hofacker, and P. F. Stadler (2008)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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S. Ro, R. Song, C. Park, H. Zheng, K. M. Sanders, and W. Yan (2007)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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S. Ro, C. Park, R. Song, D. Nguyen, J. Jin, K. M. Sanders, J. R. McCarrey, and W. Yan (2007)
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   Abstract »    Full Text »    PDF »
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