A SnoRNA-derived piRNA interacts with human interleukin-4 pre-mRNA and induces its decay in nuclear exosomes

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10474-10491

  Zhong, Fudi ^a   Zhou, Nan ^a   Wu, Kang ^a   Guo, Yubiao ^b   Tan, Weiping ^b   Zhang, Hong ^a   Zhang, Xue ^a   Geng, Guannan ^a   Pan, Ting ^a   Luo, Haihua ^a   Zhang, Yijun ^a   Xu, Zhibin ^a   Liu, Jun ^a   Liu, Bingfeng ^a   Gao, Wenchao ^a   Liu, Chao ^a   Ren, Liangliang ^a   Li, Jun ^a   Zhou, Jie ^a   Zhang, Hui ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 4 PROTEIN; ARGONAUTE PROTEIN; IMMUNOGLOBULIN E; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 7; MESSENGER RNA PRECURSOR; PIWI INTERACTING RNA; PIWI LIKE PROTEIN 4; PIWI PROTEIN; SMALL NUCLEOLAR RNA; TRAMP COMPLEX; UNCLASSIFIED DRUG; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; IL4 PROTEIN, HUMAN; MESSENGER RNA; RNA PRECURSOR; SMALL INTERFERING RNA;

ARTICLE; ASTHMA; CD4+ T LYMPHOCYTE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; EXOSOME; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INTRON; LYMPHOCYTE DIFFERENTIATION; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; TH2 CELL; CELL CULTURE; CHEMISTRY; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; RNA STABILITY;

ASTHMA; CD4-POSITIVE T-LYMPHOCYTES; CELL NUCLEUS; CELLS, CULTURED; DOWN-REGULATION; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTERLEUKIN-4; INTRONS; RNA PRECURSORS; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA, SMALL NUCLEOLAR; TH2 CELLS;

EID: 84983751493     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv954     Document Type: Article

References (79)

1. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M.J., Kuramochi-Miyagawa, S., Nakano, T. et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 442, 203-207
2. Girard, A., Sachidanandam, R., Hannon, G.J. and Carmell, M.A (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature, 442, 199-202
3. Grivna, S.T., Beyret, E., Wang, Z. and Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev., 20, 1709-1714
4. Lau, N.C., Seto, A.G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D.P. and Kingston, R.E. (2006) Characterization of the piRNA complex from rat testes. Science, 313, 363-367
5. Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N. and Imai, H. (2006) Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev., 20, 1732-1743
6. Cichocki, F., Lenvik, T., Sharma, N., Yun, G., Anderson, S.K. and Miller, J.S. (2010) Cutting edge: KIR antisense transcripts are processed into a 28-base PIWI-like RNA in human NK cells. J Immunol., 185, 2009-2012
7. Lee, E.J., Banerjee, S., Zhou, H., Jammalamadaka, A., Arcila, M., Manjunath, B.S. and Kosik, K.S. (2011) Identification of piRNAs in the central nervous system. RNA, 17, 1090-1099
8. Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T. and Kandel, E.R. (2012) A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell, 149, 693-707
9. Li, C.J., Vagin, V.V., Lee, S.H., Xu, J., Ma, S.M., Xi, H.L., Seitz, H., Horwich, M.D., Syrzycka, M., Honda, B.M. et al. (2009) Collapse of germline piRNAs in the absence of argonaute3 reveals somatic piRNAs in flies. Cell, 137, 509-521
10. Malone, C.D., Brennecke, J., Dus, M., Stark, A., McCombie, W.R., Sachidanandam, R. and Hannon, G.J. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary Cell, 137, 522-535
11. Yan, Z., Hu, H.Y., Jiang, X., Maierhofer, V., Neb, E., He, L., Hu, Y., Hu, H., Li, N., Chen, W. et al. (2011) Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res., 39, 6596-6607
12. Lu, Y., Li, C., Zhang, K., Sun, H., Tao, D., Liu, Y., Zhang, S. and Ma, Y (2010) Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep., 43, 635-641
13. Cheng, J., Deng, H.X., Xiao, B.X., Zhou, H., Zhou, F., Shen, Z.S. and Guo, J.M. (2012) piR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett., 315, 12-17
14. Cheng, J., Guo, J.M., Xiao, B.X., Miao, Y., Jiang, Z., Zhou, H. and Li, Q.N. (2011) piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin. Chim. Acta, 412, 1621-1625
15. Huang, G., Hu, H., Xue, X., Shen, S., Gao, E., Guo, G., Shen, X. and Zhang, X. (2013) Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin. Transl. Oncol., 15, 563-568
16. He, X., Chen, X., Zhang, X., Duan, X., Pan, T., Hu, Q., Zhang, Y., Zhong, F., Liu, J., Zhang, H. et al. (2015) An Lnc RNA (GAS5)/SnoRNA-derived piRNA induces activation of TRAIL gene by site-specifically recruiting MLL/COMPASS-like complexes Nucleic Acids Res., 43, 3712-3725
17. Brennecke, J., Aravin, A.A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R. and Hannon, G.J. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell, 128, 1089-1103
18. Gunawardane, L.S., Saito, K., Nishida, K.M., Miyoshi, K., Kawamura, Y., Nagami, T., Siomi, H. and Siomi, M.C. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science, 315, 1587-1590
19. Saito, K., Inagaki, S., Mituyama, T., Kawamura, Y., Ono, Y., Sakota, E., Kotani, H., Asai, K., Siomi, H. and Siomi, M.C. (2009) A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila Nature, 461, 1296-1299
20. Kirino, Y. and Mourelatos, Z. (2007) Mouse Piwi-interacting RNAs are 2′-O-methylated at their 3′ termini. Nat. Struct. Mol. Biol., 14, 347-348
21. Ohara, T., Sakaguchi, Y., Suzuki, T., Ueda, H. and Miyauchi, K. (2007) The 3′ termini of mouse Piwi-interacting RNAs are 2′-O-methylated Nat. Struct. Mol. Biol., 14, 349-350
22. Cox, D.N., Chao, A., Baker, J., Chang, L., Qiao, D. and Lin, H. (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev., 12, 3715-3727
23. Lin, H. and Spradling, A.C. (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development, 124, 2463-2476
24. Thomson, T. and Lin, H. (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev Biol., 25, 355-376
25. Siomi, M.C., Sato, K., Pezic, D. and Aravin, A.A. (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev. Mol. Cell Biol., 12, 246-258
26. Qiao, D., Zeeman, A.M., Deng, W., Looijenga, L.H. and Lin, H. (2002) Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas Oncogene, 21, 3988-3999
27. Ross, R.J., Weiner, M.M. and Lin, H. (2014) PIWI proteins and PIWI-interacting RNAs in the soma. Nature, 505, 353-359
28. Aravin, A.A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J. and Tuschl, T. (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell, 5, 337-350
29. Nishida, K.M., Saito, K., Mori, T., Kawamura, Y., Nagami-Okada, T., Inagaki, S., Siomi, H. and Siomi, M.C. (2007) Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA, 13, 1911-1922
30. Ghildiyal, M. and Zamore, P.D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet., 10, 94-108
31. Saito, K., Ishizu, H., Komai, M., Kotani, H., Kawamura, Y., Nishida, K.M., Siomi, H. and Siomi, M.C. (2010) Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev., 24, 2493-2498
32. Senti, K.A. and Brennecke, J. (2010) The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet., 26, 499-509
33. Siomi, M.C., Miyoshi, T. and Siomi, H. (2010) piRNA-mediated silencing in Drosophila germlines. Semin. Cell Dev. Biol., 21, 754-759
34. Siddiqi, S. and Matushansky, I. (2012) Piwis and piwi-interacting RNAs in the epigenetics of cancer. J. Cell Biochem., 113, 373-380
35. Meister, G., Landthaler, M., Dorsett, Y. and Tuschl, T. (2004) Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA, 10, 544-550
36. Chen, K. and Rajewsky, N. (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet., 8, 93-103
37. Pillai, R.S., Bhattacharyya, S.N. and Filipowicz, W. (2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol., 17, 118-126
38. Brower-Toland, B., Findley, S.D., Jiang, L., Liu, L., Yin, H., Dus, M., Zhou, P., Elgin, S.C. and Lin, H. (2007) Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev., 21, 2300-2311
39. Huang, X.A., Yin, H., Sweeney, S., Raha, D., Snyder, M. and Lin, H (2013) A major epigenetic programming mechanism guided by piRNAs. Dev. Cell, 24, 502-516
40. Le Thomas, A., Rogers, A.K., Webster, A., Marinov, G.K., Liao, S.E., Perkins, E.M., Hur, J.K., Aravin, A.A. and Toth, K.F. (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev., 27, 390-399
41. Sienski, G., Donertas, D. and Brennecke, J. (2012) Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell, 151, 964-980
42. Akkouche, A., Grentzinger, T., Fablet, M., Armenise, C., Burlet, N., Braman, V., Chambeyron, S. and Vieira, C. (2013) Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells. EMBO Rep., 14, 458-464
43. Watanabe, T., Tomizawa, S., Mitsuya, K., Totoki, Y., Yamamoto, Y., Kuramochi-Miyagawa, S., Iida, N., Hoki, Y., Murphy, P.J., Toyoda, A et al. (2011) Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science, 332, 848-852
44. Yin, H. and Lin, H. (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature, 450, 304-308
45. Kiuchi, T., Koga, H., Kawamoto, M., Shoji, K., Sakai, H., Arai, Y., Ishihara, G., Kawaoka, S., Sugano, S., Shimada, T. et al. (2014) A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature, 509, 633-636
46. Rouget, C., Papin, C., Boureux, A., Meunier, A.C., Franco, B., Robine, N., Lai, E.C., Pelisson, A. and Simonelig, M. (2010) Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature, 467, 1128-1132
47. Ono, M., Yamada, K., Avolio, F., Scott, M.S., van Koningsbruggen, S., Barton, G.J. and Lamond, A.I. (2010) Analysis of human small nucleolar RNAs (snoRNA) and the development of snoRNA modulator of gene expression vectors. Mol. Biol. Cell, 21, 1569-1584
48. Marnef, A., Richard, P., Pinzon, N. and Kiss, T. (2014) Targeting vertebrate intron-encoded box C/D 2′-O-methylation guide RNAs into the Cajal body. Nucleic Acids Res., 42, 6616-6629
49. Dong, Z.W., Shao, P., Diao, L.T., Zhou, H., Yu, C.H. and Qu, L.H (2012) RTL-P: a sensitive approach for detecting sites of 2′-O-methylation in RNA molecules. Nucleic Acids Res., 40, e157
50. Ro, S., Park, C., Jin, J., Sanders, K.M. and Yan, W.(2006) A PCR-based method for detection and quantification of small RNAs. Biochem Biopphys Res Commun, 351, 756-763
51. Varallyay, E., Burgyan, J. and Havelda, Z. (2008) MicroRNA detection by northern blotting using locked nucleic acid probes. Nat. Protoc., 3, 190-196
52. Liu, C., Zhang, X., Huang, F., Yang, B., Li, J., Liu, B., Luo, H., Zhang, P and Zhang, H. (2012) APOBEC3G inhibits microRNA-mediated repression of translation by interfering with the interaction between Argonaute-2 and MOV10. J. Biol. Chem., 287, 29373-29383
53. Falaleeva, M. and Stamm, S. (2013) Processing of snoRNAs as a new source of regulatory non-coding RNAs: snoRNA fragments form a new class of functional RNAs. Bioessays, 35, 46-54
54. Speckmann, W.A., Terns, R.M. and Terns, M.P. (2000) The box C/D motif directs snoRNA 5′-cap hypermethylation. Nucleic Acids Res., 28, 4467-4473
55. Scott, M.S., Ono, M., Yamada, K., Endo, A., Barton, G.J. and Lamond, A.I. (2012) Human box C/D snoRNA processing conservation across multiple cell types. Nucleic Acids Res., 40, 3676-3688
56. Baumjohann, D. and Ansel, K.M. (2013) MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat. Rev Immunol., 13, 666-678
57. Rossi, R.L., Rossetti, G., Wenandy, L., Curti, S., Ripamonti, A., Bonnal, R.J., Birolo, R.S., Moro, M., Crosti, M.C., Gruarin, P. et al (2011) Distinct microRNA signatures in human lymphocyte subsets and enforcement of the naive state in CD4+ T cells by the microRNA miR-125b. Nat. Immunol., 12, 796-803
58. Ma, F., Xu, S., Liu, X., Zhang, Q., Xu, X., Liu, M., Hua, M., Li, N., Yao, H. and Cao, X. (2011) The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat. Immunol., 12, 861-869
59. Li, Q.J., Chau, J., Ebert, P.J., Sylvester, G., Min, H., Liu, G., Braich, R., Manoharan, M., Soutschek, J., Skare, P. et al. (2007) miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell, 129, 147-161
60. Ender, C., Krek, A., Friedlander, M.R., Beitzinger, M., Weinmann, L., Chen, W., Pfeffer, S., Rajewsky, N. and Meister, G. (2008) A human snoRNA with microRNA-like functions. Mol. Cell, 32, 519-528
61. Lemieux, C., Marguerat, S., Lafontaine, J., Barbezier, N., Bahler, J. and Bachand, F. (2011) A pre-mRNA degradation pathway that selectively targets intron-containing genes requires the nuclear poly(A)-binding protein. Mol. Cell, 44, 108-119
62. Kong, K.Y., Tang, H.M., Pan, K., Huang, Z., Lee, T.H., Hinnebusch, A.G., Jin, D.Y. and Wong, C.M. (2014) Cotranscriptional recruitment of yeast TRAMP complex to intronic sequences promotes optimal pre-mRNA splicing. Nucleic Acids Res., 42, 643-660
63. Sugimoto, K., Kage, H., Aki, N., Sano, A., Kitagawa, H., Nagase, T., Yatomi, Y., Ohishi, N. and Takai, D. (2007) The induction of H3K9 methylation by PIWIL4 at the p16Ink4a locus. Biochem. Biophys Res. Commun., 359, 497-502
64. Modzelewski, A.J., Holmes, R.J., Hilz, S., Grimson, A. and Cohen, P.E (2012) AGO4 regulates entry into meiosis and influences silencing of sex chromosomes in the male mouse germline. Dev. Cell, 23, 251-264
65. Aravin, A.A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K.F., Bestor, T. and Hannon, G.J. (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell, 31, 785-799
66. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R., Parker, R. and Hannon, G.J. (2005) A role for the P-body component GW182 in microRNA function. Nat. Cell Biol., 7, 1261-1266
67. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A. and Tollervey, D. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell, 121, 713-724
68. Nag, A. and Steitz, J.A. (2012) Tri-snRNP-associated proteins interact with subunits of the TRAMP and nuclear exosome complexes, linking RNA decay and pre-mRNA splicing. RNA Biol., 9, 334-342
69. Ashe, A., Sapetschnig, A., Weick, E.M., Mitchell, J., Bagijn, M.P., Cording, A.C., Doebley, A.L., Goldstein, L.D., Lehrbach, N.J., Le Pen, J. et al. (2012) piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell, 150, 88-99
70. Brennecke, J., Malone, C.D., Aravin, A.A., Sachidanandam, R., Stark, A. and Hannon, G.J. (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science, 322, 1387-1392
71. Nolde, M.J., Cheng, E.C., Guo, S. and Lin, H. (2013) Piwi genes are dispensable for normal hematopoiesis in mice. PLoS One, 8, e71950
72. Kishore, S. and Stamm, S. (2006) The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science, 311, 230-232
73. Kishore, S., Khanna, A., Zhang, Z.Y., Hui, J.Y., Balwierz, P.J., Stefan, M., Beach, C., Nicholls, R.D., Zavolan, M. and Stamm, S (2010) The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum. Mol. Genet., 19, 1153-1164
74. Haussecker, D., Huang, Y., Lau, A., Parameswaran, P., Fire, A.Z. and Kay, M.A. (2010) Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA, 16, 673-695
75. Kawaji, H., Nakamura, M., Takahashi, Y., Sandelin, A., Katayama, S., Fukuda, S., Daub, C.O., Kai, C., Kawai, J., Yasuda, J. et al. (2008) Hidden layers of human small RNAs. BMC Genomics, 9, 157
76. Taft, R.J., Glazov, E.A., Lassmann, T., Hayashizaki, Y., Carninci, P. and Mattick, J.S. (2009) Small RNAs derived from snoRNAs. RNA, 15, 1233-1240
77. Filipowicz, W. and Pogacic, V. (2002) Biogenesis of small nucleolar ribonucleoproteins. Curr. Opin. Cell Biol., 14, 319-327
78. Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell, 136, 763-776
79. Houseley, J., LaCava, J. and Tollervey, D. (2006) RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol., 7, 529-539.