LTR-Retrotransposon Control by tRNA-Derived Small RNAs

Cell

Volumn 170, Issue 1, 2017, Pages 61-71.e11

  Schorn, Andrea J ^a   Gutbrod, Michael J ^a   LeBlanc, Chantal ^a,b,c   Martienssen, Rob ^a,b  

^a Simons Center for Quantitative Biology   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

epigenetic reprogramming; LTR retrotransposon mobility; mouse endogenous retroviruses; small RNA; transposon control; tRNA fragments

Indexed keywords

HISTONE H3; LYSINE; TRANSFER RNA; SMALL UNTRANSLATED RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDOGENOUS RETROVIRUS; EPIGENETICS; GENE EXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROPOSON; REVERSE TRANSCRIPTION; RNAI THERAPEUTICS; TRANSCRIPTION INITIATION; TRANSPOSON; ANIMAL; GENE SILENCING; GENETICS; METABOLISM; RETROVIRIDAE; STEM CELL; VIROLOGY;

ANIMALS; GENE SILENCING; HELA CELLS; HUMANS; MICE; RETROVIRIDAE; RNA, SMALL UNTRANSLATED; RNA, TRANSFER; STEM CELLS; TERMINAL REPEAT SEQUENCES;

EID: 85021391363     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.06.013     Document Type: Article

References (68)

1. Aravin, A.A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K.F., Bestor, T., Hannon, G.J., A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31 (2008), 785–799.
2. Barnett, D.W., Garrison, E.K., Quinlan, A.R., Strömberg, M.P., Marth, G.T., BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27 (2011), 1691–1692.
3. Chuong, E.B., Rumi, M.A., Soares, M.J., Baker, J.C., Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45 (2013), 325–329.
4. Cole, C., Sobala, A., Lu, C., Thatcher, S.R., Bowman, A., Brown, J.W., Green, P.J., Barton, G.J., Hutvagner, G., Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 15 (2009), 2147–2160.
5. Couvillion, M.T., Sachidanandam, R., Collins, K., A growth-essential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev. 24 (2010), 2742–2747.
6. Dewannieux, M., Dupressoir, A., Harper, F., Pierron, G., Heidmann, T., Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat. Genet. 36 (2004), 534–539.
7. Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P., Heidmann, T., Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. USA 106 (2009), 12127–12132.
8. Ecco, G., Cassano, M., Kauzlaric, A., Duc, J., Coluccio, A., Offner, S., Imbeault, M., Rowe, H.M., Turelli, P., Trono, D., Transposable elements and their KRAB-ZFP controllers regulate gene expression in adult tissues. Dev. Cell 36 (2016), 611–623.
9. Elsässer, S.J., Noh, K.M., Diaz, N., Allis, C.D., Banaszynski, L.A., Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 522 (2015), 240–244.
10. Esnault, C., Maestre, J., Heidmann, T., Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24 (2000), 363–367.
11. Fadloun, A., Le Gras, S., Jost, B., Ziegler-Birling, C., Takahashi, H., Gorab, E., Carninci, P., Torres-Padilla, M.E., Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat. Struct. Mol. Biol. 20 (2013), 332–338.
12. Faulkner, G.J., Kimura, Y., Daub, C.O., Wani, S., Plessy, C., Irvine, K.M., Schroder, K., Cloonan, N., Steptoe, A.L., Lassmann, T., et al. The regulated retrotransposon transcriptome of mammalian cells. Nat. Genet. 41 (2009), 563–571.
13. Feschotte, C., Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9 (2008), 397–405.
14. Fort, A., Hashimoto, K., Yamada, D., Salimullah, M., Keya, C.A., Saxena, A., Bonetti, A., Voineagu, I., Bertin, N., Kratz, A., et al., FANTOM Consortium. Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat. Genet. 46 (2014), 558–566.
15. Haussecker, D., Huang, Y., Lau, A., Parameswaran, P., Fire, A.Z., Kay, M.A., Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16 (2010), 673–695.
16. Heidmann, O., Heidmann, T., Retrotransposition of a mouse IAP sequence tagged with an indicator gene. Cell 64 (1991), 159–170.
17. Hemberger, M., Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics 5 (2010), 24–29.
18. Ito, M., Sferruzzi-Perri, A.N., Edwards, C.A., Adalsteinsson, B.T., Allen, S.E., Loo, T.H., Kitazawa, M., Kaneko-Ishino, T., Ishino, F., Stewart, C.L., Ferguson-Smith, A.C., A trans-homologue interaction between reciprocally imprinted miR-127 and Rtl1 regulates placenta development. Development 142 (2015), 2425–2430.
19. Juliano, C., Wang, J., Lin, H., Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu. Rev. Genet. 45 (2011), 447–469.
20. Karimi, M.M., Goyal, P., Maksakova, I.A., Bilenky, M., Leung, D., Tang, J.X., Shinkai, Y., Mager, D.L., Jones, S., Hirst, M., Lorincz, M.C., DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8 (2011), 676–687.
21. Kawaji, H., Nakamura, M., Takahashi, Y., Sandelin, A., Katayama, S., Fukuda, S., Daub, C.O., Kai, C., Kawai, J., Yasuda, J., et al. Hidden layers of human small RNAs. BMC Genomics, 9, 2008, 157.
22. Keam, S.P., Hutvagner, G., tRNA-derived fragments (tRFs): emerging new roles for an ancient RNA in the regulation of gene expression. Life (Basel) 5 (2015), 1638–1651.
23. Keam, S.P., Young, P.E., McCorkindale, A.L., Dang, T.H., Clancy, J.L., Humphreys, D.T., Preiss, T., Hutvagner, G., Martin, D.I., Cropley, J.E., Suter, C.M., The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells. Nucleic Acids Res. 42 (2014), 8984–8995.
24. Keeney, J.B., Chapman, K.B., Lauermann, V., Voytas, D.F., Aström, S.U., von Pawel-Rammingen, U., Byström, A., Boeke, J.D., Multiple molecular determinants for retrotransposition in a primer tRNA. Mol. Cell. Biol. 15 (1995), 217–226.
25. Kraushaar, D.C., Jin, W., Maunakea, A., Abraham, B., Ha, M., Zhao, K., Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol., 14, 2013, R121.
26. Kumar, P., Anaya, J., Mudunuri, S.B., Dutta, A., Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol., 12, 2014, 78.
27. Kumar, P., Kuscu, C., Dutta, A., Biogenesis and function of transfer RNA-related fragments (tRFs). Trends Biochem. Sci. 41 (2016), 679–689.
28. Kunarso, G., Chia, N.Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y.S., Ng, H.H., Bourque, G., Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42 (2010), 631–634.
29. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
30. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, 2009, R25.
31. Le Grice, S.F., “In the beginning”: initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42 (2003), 14349–14355.
32. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The sequence alignment/map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
33. Li, Z., Ender, C., Meister, G., Moore, P.S., Chang, Y., John, B., Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res. 40 (2012), 6787–6799.
34. Macfarlan, T.S., Gifford, W.D., Driscoll, S., Lettieri, K., Rowe, H.M., Bonanomi, D., Firth, A., Singer, O., Trono, D., Pfaff, S.L., Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487 (2012), 57–63.
35. Maksakova, I.A., Zhang, Y., Mager, D.L., Preferential epigenetic suppression of the autonomous MusD over the nonautonomous ETn mouse retrotransposons. Mol. Cell. Biol. 29 (2009), 2456–2468.
36. Martin, M., Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. 17 (2011), 10–22.
37. Martinez, G., Choudury, S.G., Slotkin, R.K., tRNA-derived small RNAs target transposable element transcripts. Nucleic Acids Res. 45 (2017), 5142–5152.
38. Matsui, T., Leung, D., Miyashita, H., Maksakova, I.A., Miyachi, H., Kimura, H., Tachibana, M., Lorincz, M.C., Shinkai, Y., Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464 (2010), 927–931.
39. Maute, R.L., Schneider, C., Sumazin, P., Holmes, A., Califano, A., Basso, K., Dalla-Favera, R., tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc. Natl. Acad. Sci. USA 110 (2013), 1404–1409.
40. Molla-Herman, A., Vallés, A.M., Ganem-Elbaz, C., Antoniewski, C., Huynh, J.R., tRNA processing defects induce replication stress and Chk2-dependent disruption of piRNA transcription. EMBO J. 34 (2015), 3009–3027.
41. Morgan, H.D., Sutherland, H.G., Martin, D.I., Whitelaw, E., Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23 (1999), 314–318.
42. Nellåker, C., Keane, T.M., Yalcin, B., Wong, K., Agam, A., Belgard, T.G., Flint, J., Adams, D.J., Frankel, W.N., Ponting, C.P., The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol., 13, 2012, R45.
43. Ohnishi, Y., Totoki, Y., Toyoda, A., Watanabe, T., Yamamoto, Y., Tokunaga, K., Sakaki, Y., Sasaki, H., Hohjoh, H., Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development. Nucleic Acids Res. 38 (2010), 5141–5151.
44. Panganiban, A.T., Fiore, D., Ordered interstrand and intrastrand DNA transfer during reverse transcription. Science 241 (1988), 1064–1069.
45. Peaston, A.E., Evsikov, A.V., Graber, J.H., de Vries, W.N., Holbrook, A.E., Solter, D., Knowles, B.B., Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7 (2004), 597–606.
46. Quinlan, A.R., Hall, I.M., BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 (2010), 841–842.
47. Raina, M., Ibba, M., tRNAs as regulators of biological processes. Front. Genet., 5, 2014, 171.
48. Rebollo, R., Karimi, M.M., Bilenky, M., Gagnier, L., Miceli-Royer, K., Zhang, Y., Goyal, P., Keane, T.M., Jones, S., Hirst, M., et al. Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet., 7, 2011, e1002301.
49. Ribet, D., Dewannieux, M., Heidmann, T., An active murine transposon family pair: retrotransposition of “master” MusD copies and ETn trans-mobilization. Genome Res. 14 (2004), 2261–2267.
50. Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat Biotechnol. 29 (2011), 24–26.
51. Rowe, H.M., Jakobsson, J., Mesnard, D., Rougemont, J., Reynard, S., Aktas, T., Maillard, P.V., Layard-Liesching, H., Verp, S., Marquis, J., et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463 (2010), 237–240.
52. Rugg-Gunn, P.J., Cox, B.J., Ralston, A., Rossant, J., Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc. Natl. Acad. Sci. USA 107 (2010), 10783–10790.
53. Ruggero, K., Guffanti, A., Corradin, A., Sharma, V.K., De Bellis, G., Corti, G., Grassi, A., Zanovello, P., Bronte, V., Ciminale, V., D'Agostino, D.M., Small noncoding RNAs in cells transformed by human T-cell leukemia virus type 1: a role for a tRNA fragment as a primer for reverse transcriptase. J. Virol. 88 (2014), 3612–3622.
54. Schorn, A., and Martienssen, R.A. (2011). F1000Prime Recommendation of [Couvillion MT et al., Genes Dev. 2010, 24(24):2742–7]. https://f1000.com/prime/8668956.
55. Sharma, U., Conine, C.C., Shea, J.M., Boskovic, A., Derr, A.G., Bing, X.Y., Belleannee, C., Kucukural, A., Serra, R.W., Sun, F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351 (2016), 391–396.
56. Sienski, G., Dönertas, D., Brennecke, J., Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151 (2012), 964–980.
57. Slotkin, R.K., Martienssen, R., Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8 (2007), 272–285.
58. Tam, O.H., Aravin, A.A., Stein, P., Girard, A., Murchison, E.P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R.M., Hannon, G.J., Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453 (2008), 534–538.
59. Tan, X., Xu, X., Elkenani, M., Smorag, L., Zechner, U., Nolte, J., Engel, W., Pantakani, D.V., Zfp819, a novel KRAB-zinc finger protein, interacts with KAP1 and functions in genomic integrity maintenance of mouse embryonic stem cells. Stem Cell Res. (Amst.) 11 (2013), 1045–1059.
60. Tanaka, S., Kunath, T., Hadjantonakis, A.K., Nagy, A., Rossant, J., Promotion of trophoblast stem cell proliferation by FGF4. Science 282 (1998), 2072–2075.
61. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., Martienssen, R.A., Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297 (2002), 1833–1837.
62. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T., et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453 (2008), 539–543.
63. Watanabe, T., Tomizawa, S., Mitsuya, K., Totoki, Y., Yamamoto, Y., Kuramochi-Miyagawa, S., Iida, N., Hoki, Y., Murphy, P.J., Toyoda, A., et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332 (2011), 848–852.
64. Wei, W., Gilbert, N., Ooi, S.L., Lawler, J.F., Ostertag, E.M., Kazazian, H.H., Boeke, J.D., Moran, J.V., Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 21 (2001), 1429–1439.
65. Wolf, D., Hug, K., Goff, S.P., TRIM28 mediates primer binding site-targeted silencing of Lys1,2 tRNA-utilizing retroviruses in embryonic cells. Proc. Natl. Acad. Sci. USA 105 (2008), 12521–12526.
66. Wolf, G., Yang, P., Füchtbauer, A.C., Füchtbauer, E.M., Silva, A.M., Park, C., Wu, W., Nielsen, A.L., Pedersen, F.S., Macfarlan, T.S., The KRAB zinc finger protein ZFP809 is required to initiate epigenetic silencing of endogenous retroviruses. Genes Dev. 29 (2015), 538–554.
67. Yeung, M.L., Bennasser, Y., Watashi, K., Le, S.Y., Houzet, L., Jeang, K.T., Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res. 37 (2009), 6575–6586.
68. Yuan, P., Han, J., Guo, G., Orlov, Y.L., Huss, M., Loh, Y.H., Yaw, L.P., Robson, P., Lim, B., Ng, H.H., Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23 (2009), 2507–2520.