Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

PIWI proteins and PIWI-interacting RNAs in the soma

Nature volume 505, pages 353–359 (2014)Cite this article

Subjects

Abstract

The discovery of millions of PIWI-interacting RNAs revealed a fascinating and unanticipated dimension of biology. The PIWI–piRNA pathway has been commonly perceived as germline-specific, even though the somatic function of PIWI proteins was documented when they were first discovered. Recent studies have begun to re-explore this pathway in somatic cells in diverse organisms, particularly lower eukaryotes. These studies have illustrated the multifaceted somatic functions of the pathway not only in transposon silencing but also in genome rearrangement and epigenetic programming, with biological roles in stem-cell function, whole-body regeneration, memory and possibly cancer.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: piRNA biogenesis in the Drosophila ovarian soma.
Figure 2: Piwi–piRNA mediated epigenetic regulation.
Figure 3: Somatic genome rearrangement in ciliates.

Similar content being viewed by others

References

  1. Lin, H. & Spradling, A. C. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463–2476 (1997).

    PubMed  CAS  Google Scholar 

  2. 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). This paper reports the discovery of the argonaute/piwi gene family and is the first demonstration of the somatic function of a PIWI protein (for germline stem-cell maintenance).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Girard, A., Sachidanandam, R., Hannon, G. J. & Carmell, M. A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199–202 (2006).

    ADS  PubMed  Google Scholar 

  4. Aravin, A. et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203–207 (2006).

    ADS  CAS  PubMed  Google Scholar 

  5. Grivna, S. T., Beyret, E., Wang, Z. & Lin, H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20, 1709–1714 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Lau, N. C. et al. Characterization of the piRNA complex from rat testes. Science 313, 363–367 (2006).

    ADS  CAS  PubMed  Google Scholar 

  7. Saito, K. et al. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 20, 2214–2222 (2006). This work defines a somatic piRNA pathway in the Drosophila ovary.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Yin, H. & Lin, H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450, 304–308 (2007).

    ADS  CAS  PubMed  Google Scholar 

  9. Brennecke, J. et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128, 1089–1103 (2007).

    CAS  PubMed  Google Scholar 

  10. Aravin, A. A. et al. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337–350 (2003).

    CAS  PubMed  Google Scholar 

  11. Vagin, V. V. et al. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320–324 (2006).

    ADS  CAS  PubMed  Google Scholar 

  12. Deng, W. & Lin, H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2, 819–830 (2002).

    CAS  PubMed  Google Scholar 

  13. Kuramochi-Miyagawa, S. et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131, 839–849 (2004).

    CAS  PubMed  Google Scholar 

  14. Carmell, M. A. et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12, 503–514 (2007).

    CAS  PubMed  Google Scholar 

  15. Siomi, M. C., Sato, K., Pezic, D. & Aravin, A. A. PIWI-interacting small RNAs: the vanguard of genome defence. Nature Rev. Mol. Cell Biol. 12, 246–258 (2011).

    CAS  Google Scholar 

  16. Funayama, N., Nakatsukasa, M., Mohri, K., Masuda, Y. & Agata, K. Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol. Dev. 12, 275–287 (2010).

    CAS  PubMed  Google Scholar 

  17. Denker, E., Manuel, M., Leclere, L., Le Guyader, H. & Rabet, N. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev. Biol. 315, 99–113 (2008).

    CAS  PubMed  Google Scholar 

  18. Seipel, K., Yanze, N. & Schmid, V. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int. J. Dev. Biol. 48, 1–7 (2004).

    CAS  PubMed  Google Scholar 

  19. Alié, A. et al. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev. Biol. 350, 183–197 (2011).

    PubMed  Google Scholar 

  20. De Mulder, K. et al. Stem cells are differentially regulated during development, regeneration and homeostasis in flatworms. Dev. Biol. 334, 198–212 (2009).

    CAS  PubMed  Google Scholar 

  21. 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).

    ADS  CAS  PubMed  Google Scholar 

  22. Palakodeti, D., Smielewska, M., Lu, Y. C., Yeo, G. W. & Graveley, B. R. The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14, 1174–1186 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Rinkevich, Y. et al. Piwi positive cells that line the vasculature epithelium, underlie whole body regeneration in a basal chordate. Dev. Biol. 345, 94–104 (2010).

    CAS  PubMed  Google Scholar 

  24. Rinkevich, Y. et al. Repeated, long-term cycling of putative stem cells between niches in a basal chordate. Dev. Cell 24, 76–88 (2013).

    CAS  PubMed  Google Scholar 

  25. Cox, D. N., Chao, A. & Lin, H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127, 503–514 (2000).

    CAS  PubMed  Google Scholar 

  26. Brower-Toland, B. et al. Drosophila Piwi associates with chromatin and interacts directly with HP1a. Genes Dev. 21, 2300–2311 (2007). This paper shows the direct interaction between Piwi and HP1a, the binding of Piwi to chromosomes in Drosophila somatic cells and the epigenetic effect of such interaction and binding.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Perrat, P. N. et al. Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340, 91–95 (2013).

    ADS  CAS  PubMed  Google Scholar 

  28. Ghildiyal, M. et al. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320, 1077–1081 (2008).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mani, S. R., Megosh, H. & Lin, H. PIWI proteins are essential for early Drosophila embryogenesis. Dev. Biol. http://dx.doi.org/10.1016/j.ydbio.2013.10.017 (31 October 2013).

  30. Sharma, A. K. et al. Human CD34+ stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 97, 426–434 (2001).

    CAS  PubMed  Google Scholar 

  31. Nolde, M. J., Cheng, E. C., Guo, S. & Lin, H. Piwi genes are dispensable for normal hematopoiesis in mice. PLoS ONE 8, e71950 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  32. Qiao, D., Zeeman, A. M., Deng, W., Looijenga, L. H. & Lin, H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 21, 3988–3999 (2002).

    CAS  PubMed  Google Scholar 

  33. Lee, J. H. et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet. 15, 201–211 (2006).

    CAS  PubMed  Google Scholar 

  34. Zhao, Y. M. et al. HIWI is associated with prognosis in patients with hepatocellular carcinoma after curative resection. Cancer 118, 2708–2717 (2012).

    CAS  PubMed  Google Scholar 

  35. Taubert, H. et al. Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene 26, 1098–1100 (2007).

    CAS  PubMed  Google Scholar 

  36. Liu, X. et al. Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. Int. J. Cancer 118, 1922–1929 (2006).

    CAS  PubMed  Google Scholar 

  37. Yan, Z. et al. Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 39, 6596–6607 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Malone, C. D. et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137, 522–535 (2009). This work delineates distinct germline and somatic piRNA pathways in the Drosophila ovary.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Saito, K. et al. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461, 1296–1299 (2009).

    ADS  CAS  PubMed  Google Scholar 

  40. Ipsaro, J. J., Haase, A. D., Knott, S. R., Joshua-Tor, L. & Hannon, G. J. The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491, 279–283 (2012).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  41. Olivieri, D., Sykora, M. M., Sachidanandam, R., Mechtler, K. & Brennecke, J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 29, 3301–3317 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Saito, K. et al. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 24, 2493–2498 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Qi, H. et al. The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J. Biol. Chem. 286, 3789–3797 (2011).

    CAS  PubMed  Google Scholar 

  44. Szakmary, A., Reedy, M., Qi, H. & Lin, H. The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J. Cell Biol. 185, 613–627 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Handler, D. et al. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 30, 3977–3993 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Nishimasu, H. et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491, 284–287 (2012).

    ADS  CAS  PubMed  Google Scholar 

  47. Watanabe, T. et al. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 20, 364–375 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Zheng, K. et al. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc. Natl Acad. Sci. USA 107, 11841–11846 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  49. Frost, R. J. et al. MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc. Natl Acad. Sci. USA 107, 11847–11852 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  50. Xiol, J. et al. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol. Cell 47, 970–979 (2012).

    CAS  PubMed  Google Scholar 

  51. Crackower, M. A. et al. Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 300, 1291–1295 (2003).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  52. Pandey, R. R. et al. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc. Natl Acad. Sci. 110, 16492–16497 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  53. Darricarrère, N., Liu, N., Watanabe, T. & Lin, H. Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity. Proc. Natl Acad. Sci. USA 110, 1297–1302 (2013).

    ADS  PubMed  PubMed Central  Google Scholar 

  54. Olivieri, D., Senti, K. A., Subramanian, S., Sachidanandam, R. & Brennecke, J. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol. Cell 47, 954–969 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Kawaoka, S., Izumi, N., Katsuma, S. & Tomari, Y. 3′ end formation of PIWI-interacting RNAs in vitro. Mol. Cell 43, 1015–1022 (2011).

    CAS  PubMed  Google Scholar 

  56. Parker, J. S., Roe, S. M. & Barford, D. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J. 23, 4727–4737 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Boland, A., Huntzinger, E., Schmidt, S., Izaurralde, E. & Weichenrieder, O. Crystal structure of the MID-PIWI lobe of a eukaryotic Argonaute protein. Proc. Natl Acad. Sci. USA 108, 10466–10471 (2011).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  58. Nakanishi, K., Weinberg, D. E., Bartel, D. P. & Patel, D. J. Structure of yeast Argonaute with guide RNA. Nature 486, 368–374 (2012).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  59. Saito, K., Sakaguchi, Y., Suzuki, T., Siomi, H. & Siomi, M. C. Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 3′ ends. Genes Dev. 21, 1603–1608 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Pal-Bhadra, M., Bhadra, U. & Birchler, J. A. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9, 315–327 (2002). This is the first demonstration that Piwi is essential for transcriptional and post-transcriptional gene silencing.

    CAS  PubMed  Google Scholar 

  61. Grimaud, C. et al. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124, 957–971 (2006).

    CAS  PubMed  Google Scholar 

  62. Pal-Bhadra, M. et al. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303, 669–672 (2004).

    ADS  CAS  PubMed  Google Scholar 

  63. Sienski, G., Donertas, D. & Brennecke, J. Transcriptional silencing of transposons by Piwi and Maelstrom and its impact on chromatin state and gene expression. Cell 151, 964–980 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Huang, X. A. et al. A major epigenetic programming mechanism guided by piRNAs. Dev. Cell 24, 502–516 (2013). This work demonstrates that piRNAs are both necessary and sufficient to recruit Piwi and epigenetic factors to target sites and presents a whole-genome analysis of Piwi binding.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Le Thomas, A. et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27, 390–399 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Rozhkov, N. V., Hammell, M. & Hannon, G. J. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev. 27, 400–412 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Ge, D. T. & Zamore, P. D. Small RNA-directed silencing: the fly finds its inner fission yeast? Curr. Biol. 23, R318–R320 (2013).

    CAS  PubMed  Google Scholar 

  68. Muerdter, F. et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol. Cell 50, 736–748 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Ohtani, H. et al. DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev. 27, 1656–1661 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Dönertas, D., Sienski, G. & Brennecke, J. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev. 27, 1693–1705 (2013).

    PubMed  PubMed Central  Google Scholar 

  71. Akkouche, A. et al. Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells. EMBO Rep. 14, 458–464 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Gu, T. & Elgin, S. C. R. Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet. 9, e1003780 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Schoeberl, U. E. & Mochizuki, K. Keeping the soma free of transposons: programmed DNA elimination in ciliates. J. Biol. Chem. 286, 37045–37052 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Mochizuki, K. & Gorovsky, M. A. A dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev. 19, 77–89 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Okamura, K. & Lai, E. C. Endogenous small interfering RNAs in animals. Nature Rev. Mol. Cell Biol. 9, 673–678 (2008).

    CAS  Google Scholar 

  76. Mochizuki, K., Fine, N. A., Fujisawa, T. & Gorovsky, M. A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110, 689–699 (2002). This demonstrates that a PIWI protein is required for DNA elimination/rearrangement in Tetrahymena.

    CAS  PubMed  Google Scholar 

  77. Taverna, S. D., Coyne, R. S. & Allis, C. D. Methylation of histone h3 at lysine 9 targets programmed DNA elimination in tetrahymena. Cell 110, 701–711 (2002).

    CAS  PubMed  Google Scholar 

  78. Aronica, L. et al. Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev. 22, 2228–2241 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Fang, W., Wang, X., Bracht, J. R., Nowacki, M. & Landweber, L. F. Piwi-interacting RNAs protect DNA against loss during Oxytricha genome rearrangement. Cell 151, 1243–1255 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Rajasethupathy, P. et al. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 149, 693–707 (2012). This work reports an epigenetic function for the PIWI–piRNA pathway in the Aplysia neural system.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Waddington, C. H. Canalization of development and the inheritance of acquired characters. Nature 150, 563–565 (1942).

    ADS  Google Scholar 

  82. Queitsch, C., Sangster, T. A. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618–624 (2002).

    ADS  CAS  PubMed  Google Scholar 

  83. Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998).

    ADS  CAS  PubMed  Google Scholar 

  84. Gangaraju, V. K. et al. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nature Genet. 43, 153–158 (2011).

    CAS  PubMed  Google Scholar 

  85. Specchia, V. et al. Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463, 662–665 (2010).

    ADS  CAS  PubMed  Google Scholar 

  86. Sollars, V. et al. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nature Genet. 33, 70–74 (2003).

    CAS  PubMed  Google Scholar 

  87. Ashe, A. et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150, 88–99 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Grochola, L. F. et al. The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. Br. J. Cancer 99, 1083–1088 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Lee, J. H. et al. Pathways of proliferation and antiapoptosis driven in breast cancer stem cells by stem cell protein Piwil2. Cancer Res. 70, 4569–4579 (2010).

    CAS  PubMed  Google Scholar 

  90. Janic, A., Mendizabal, L., Llamazares, S., Rossell, D. & Gonzalez, C. Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 330, 1824–1827 (2010).

    ADS  CAS  PubMed  Google Scholar 

  91. Lee, E. et al. Landscape of somatic retrotransposition in human cancers. Science 337, 967–971 (2012).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  92. Harris, A. N. & Macdonald, P. M. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128, 2823–2832 (2001).

    PubMed  CAS  Google Scholar 

  93. Li, C. et al. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137, 509–521 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank S. Christensen, C. Juliano and S. Ramesh Mani for their critical reading of the manuscript. R.J.R. and M.M.W. are supported by an NIH Medical Scientist Training Program grant (T32-GM07205). The current work in the Lin lab on PIWIs and piRNA is supported by the NIH (DP1CA174418 and R01HD42012), the G. Harold & Leila Mathers Foundation, and an Ellison Medical Foundation Senior Scholar Award.

Author information

Author notes

  1. Robert J. Ross and Molly M. Weiner: These authors contributed equally to this work.

Authors and Affiliations

  1. Yale Stem Cell Center and Department of Cell Biology, Yale University School of Medicine, New Haven, 06509, Connecticut, USA

    Robert J. Ross, Molly M. Weiner & Haifan Lin

Authors
  1. Robert J. Ross
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Molly M. Weiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haifan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haifan Lin.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reprints and permissions information is available at www.nature.com/reprints.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ross, R., Weiner, M. & Lin, H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature 505, 353–359 (2014). https://doi.org/10.1038/nature12987

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature12987

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing