Concise review: The Piwi-piRNA Axis: Pivotal beyond transposon silencing

Stem Cells

Volumn 30, Issue 12, 2012, Pages 2603-2611

  Bamezai, Shiva ^a   Rawat, Vijay P S ^a   Buske, Christian ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Cancer; Piwi; Piwi interacting RNA; Stem cell

Indexed keywords

PIWI INTERACTING RNA; PIWI PROTEIN;

ADENOCARCINOMA; CELL RENEWAL; CHROMATIN; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; GLIOMA; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SARCOMA; SOMATIC CELL; STEM CELL; TRANSPOSON;

ANIMALS; ARGONAUTE PROTEINS; DNA TRANSPOSABLE ELEMENTS; GENE SILENCING; HUMANS; RNA, SMALL INTERFERING; STEM CELLS;

MAMMALIA;

EID: 84870325420     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1237     Document Type: Review

References (93)

1. Hedges DJ, Deininger PL. Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res 2007;616:46-59.
2. Zhang Y, Romanish MT, Mager DL. Distributions of transposable elements reveal hazardous zones in mammalian introns. PLoS Comput Biol 2011;7:e1002046.
3. Brennecke J, Aravin AA, Stark A et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007;128:1089-1103.
4. Brennecke J, Malone CD, Aravin AA et al. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 2008;322:1387-1392.
5. Aravin AA, Sachidanandam R, Bourc'his D, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 2008;31:785-799.
6. Aravin AA, Bourc'his D. Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev 2008;22:970-975.
7. Aravin AA, Sachidanandam R, Girard A et al. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007;316:744-747.
8. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007;318:761-764.
9. King FJ, Szakmary A, Cox DN et al. Yb modulates the divisions of both germline and somatic stem cells through piwi- and hh-mediated mechanisms in the Drosophila ovary. Mol Cell 2001;7:497-508.
10. Sharma AK, Nelson MC, Brandt JE et al. Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 2001;97:426-434.
11. Janic A, Mendizabal L, Llamazares S et al. Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 2010;330:1824-1827.
12. Siddiqi S, Terry M, Matushansky I. Hiwi mediated tumorigenesis is associated with DNA hypermethylation. PLoS One 2012;7:e33711.
13. O'Brien CA, Kreso A, Dick JE. Cancer stem cells in solid tumors: An overview. Semin Radiat Oncol 2009;19:71-77.
14. Dick JE. Breast cancer stem cells revealed. Proc Natl Acad Sci USA 2003;100:3547-3549.
15. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-An evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010;11:220-228.
16. Kohno T, Ichikawa H, Totoki Y et al. KIF5B-RET fusions in lung adenocarcinoma. Nat Med 2012;18:375-377.
17. Lipson D, Capelletti M, Yelensky R et al. Identification of new ALK and RET gene fusions from colorectal and lung cancer biopsies. Nat Med 2012;18:382-384.
18. Grochola LF, Greither T, Taubert H et al. The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: Expression and risk of tumour-related death. Br J Cancer 2008;99:1083-1088.
19. Lee JH, Schutte D, Wulf G et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet 2006;15:201-211.
20. Liu JJ, Shen R, Chen L et al. Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker. Int J Clin Exp Pathol 2010;3:328-337.
21. Liu XY, Sun Y, Guo JP et al. Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. Int J Cancer 2006;118:1922-1929.
22. Lu Y, Zhang K, Li C et al. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS One 2012;7:e30999.
23. Zeng Y, Qu LK, Meng L et al. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J (Engl) 2011;124:2144-2149.
24. Cox DN, Chao A, Baker J et al. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 1998;12:3715-3727.
25. Cox DN, Chao A, Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 2000;127:503-514.
26. Qiao D, Zeeman AM, Deng W et al. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 2002;21:3988-3999.
27. Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002;2:819-830.
28. Cerutti L, Mian N, Bateman A. Domains in gene silencing and cell differentiation proteins: The novel PAZ domain and redefinition of the Piwi domain. Trends Biochem Sci 2000;25:481-482.
29. Tahbaz N, Kolb FA, Zhang H et al. Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO Rep 2004;5:189-194.
30. Parker JS, Roe SM, Barford D. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J 2004;23:4727-4737.
31. Hutvagner G, Simard MJ. Argonaute proteins: Key players in RNA silencing. Nat Rev Mol Cell Biol 2008;9:22-32.
32. Yang LJ, Chen Y, Ma Q et al. Effect of betulinic acid on the regulation of Hiwi and cyclin B1 in human gastric adenocarcinoma AGS cells. Acta Pharmacol Sin 2010;31:66-72.
33. Lingel A, Simon B, Izaurralde E et al. Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 2003;426:465-469.
34. Schwalbe H. Double take on Piwi protein/piRNA complex structure. Structure 2011;19:141-142.
35. Tolia NH, Joshua-Tor L. Slicer and the argonautes. Nat Chem Biol 2007;3:36-43.
36. Parker JS, Roe SM, Barford D. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 2005;434:663-666.
37. Kiriakidou M, Tan GS, Lamprinaki S et al. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 2007;129:1141-1151.
38. Parker JS, Parizotto EA, Wang M et al. Enhancement of the seed-target recognition step in RNA silencing by a PIWI/MID domain protein. Mol Cell 2009;33:204-214.
39. Grivna ST, Pyhtila B, Lin H. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 2006;103:13415-13420.
40. Kirino Y, Kim N, de Planell-Saguer M et al. Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 2009;11:652-658.
41. Huang HY, Houwing S, Kaaij LJ et al. Tdrd1 acts as a molecular scaffold for Piwi proteins and piRNA targets in zebrafish. EMBO J 2011;30:3298-3308.
42. Siomi MC, Mannen T, Siomi H. How does the royal family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 2010;24:636-646.
43. Aravin A, Gaidatzis D, Pfeffer S et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006;442:203-207.
44. Girard A, Sachidanandam R, Hannon GJ et al. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006;442:199-202.
45. Kim VN. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev 2006;20:1993-1997.
46. Cichocki F, Lenvik T, Sharma N et al. Cutting edge: KIR antisense transcripts are processed into a 28-base PIWI-like RNA in human NK cells. J Immunol 2010;185:2009-2012.
47. Shoji M, Tanaka T, Hosokawa M et al. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 2009;17:775-787.
48. Aravin AA, van der Heijden GW, Castaneda J et al. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet 2009;5:e1000764.
49. Ishizu H, Nagao A, Siomi H. Gatekeepers for Piwi-piRNA complexes to enter the nucleus. Curr Opin Genet Dev 2011;21:484-490.
50. Li MA, Alls JD, Avancini RM et al. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol 2003;5:994-1000.
51. Rouget C, Papin C, Boureux A et al. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010;467:1128-1132.
52. Qi H, Watanabe T, Ku HY et al. The Yb body, a major site for Piwiassociated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J Biol Chem 2011;286:3789-3797.
53. Saito K, Inagaki S, Mituyama T et al. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009;461:1296-1299.
54. Moussian B, Schoof H, Haecker A et al. Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 1998;17:1799-1809.
55. Reddien PW, Oviedo NJ, Jennings JR et al. SMEDWI-2 is a PIWIlike protein that regulates planarian stem cells. Science 2005;310:1327-1330.
56. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: Progress and prospect. Annu Rev Cell Dev Biol 2009;25:355-376.
57. Carmell MA, Girard A, van de Kant HJ et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 2007;12:503-514.
58. Kuramochi-Miyagawa S, Kimura T, Ijiri TW et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004;131:839-849.
59. Unhavaithaya Y, Hao Y, Beyret E et al. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem 2009;284:6507-6519.
60. Reuter M, Berninger P, Chuma S et al. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 2011;480:264-267.
61. Webster KE, O'Bryan MK, Fletcher S et al. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci USA 2005;102:4068-4073.
62. Alie A, Leclere L, Jager M et al. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: Ancient association of "germline genes" with stemness. Dev Biol 2011;350:183-197.
63. Giani VC, Jr., Yamaguchi E, Boyle MJ et al. Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta. Evodevo 2011;2:10.
64. Funayama N, Nakatsukasa M, Mohri K et al. Piwi expression in archeocytes and choanocytes in demosponges: Insights into the stem cell system in demosponges. Evol Dev 2010;12:275-287.
65. Brown FD, Keeling EL, Le AD et al. Whole body regeneration in a colonial ascidian, Botrylloides violaceus. J Exp Zool B Mol Dev Evol 2009;312:885-900.
66. Rinkevich Y, Rosner A, Rabinowitz C et al. Piwi positive cells that line the vasculature epithelium, underlie whole body regeneration in a basal chordate. Dev Biol 2010;345:94-104.
67. Pal-Bhadra M, Leibovitch BA, Gandhi SG et al. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 2004;303:669-672.
68. Brower-Toland B, Findley SD, Jiang L et al. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 2007;21:2300-2311.
69. Klattenhoff C, Xi H, Li C et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dualstrand clusters. Cell 2009;138:1137-1149.
70. Yin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007;450:304-308.
71. Jiang J, Zhang H, Tang Q et al. Expression of HIWI in human hepatocellular carcinoma. Cell Biochem Biophys 2011;61:53-58.
72. Sun G, Wang Y, Sun L et al. Clinical significance of Hiwi gene expression in gliomas. Brain Res 2011;1373:183-188.
73. Lee JH, Engel W, Nayernia K. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol Reprod Dev 2006;73:173-179.
74. Oyamada M, Oyamada Y, Kaneko T et al. Regulation of gap junction protein (connexin) genes and function in differentiating ES cells. Methods Mol Biol 2002;185:63-69.
75. Cariati M, Naderi A, Brown JP et al. Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. Int J Cancer 2008;122:298-304.
76. Wang C, Chelly MR, Chai N et al. Transcriptomic fingerprinting of bone marrow-derived hepatic beta2m-/Thy-1+ stem cells. Biochem Biophys Res Commun 2005;327:252-260.
77. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 2004;70:70-75.
78. Bowles J, Knight D, Smith C et al. Retinoid signaling determines germ cell fate in mice. Science 2006;312:596-600.
79. Silva C, Wood JR, Salvador L et al. Expression profile of male germ cell-associated genes in mouse embryonic stem cell cultures treated with all-trans retinoic acid and testosterone. Mol Reprod Dev 2009;76:11-21.
80. Wu Q, Ma Q, Shehadeh LA et al. Expression of the Argonaute protein PiwiL2 and piRNAs in adult mouse mesenchymal stem cells. Biochem Biophys Res Commun 2010;396:915-920.
81. Lu Y, Li C, Zhang K et al. Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep 2010;43:635-641.
82. Cheng J, Deng H, Xiao B et al. piR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett 2012;315:12-17.
83. Cheng J, Guo JM, Xiao BX et al. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin Chim Acta 2011;412:1621-1625.
84. Chi SW, Zang JB, Mele A et al. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 2009;460:479-486.
85. Volpe TA, Kidner C, Hall IM et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 2002;297:1833-1837.
86. Motamedi MR, Verdel A, Colmenares SU et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 2004;119:789-802.
87. Noma K, Sugiyama T, Cam H et al. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 2004;36:1174-1180.
88. Yang L, Chen D, Duan R et al. Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development 2007;134:4265-4272.
89. Klenov MS, Sokolova OA, Yakushev EY et al. Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc Natl Acad Sci USA 2011;108:18760-18765.
90. Wang SH, Elgin SC. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci USA 2011;108:21164-21169.
91. Bannister AJ, Zegerman P, Partridge JF et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001;410:120-124.
92. Morris KV, Santoso S, Turner AM et al. Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet 2008;4:e1000258.
93. Ezoe S, Matsumura I, Satoh Y et al. Cell cycle regulation in hematopoietic stem/progenitor cells. Cell Cycle 2004;3:314-318.