A Tunable Mechanism Determines the Duration of the Transgenerational Small RNA Inheritance in C. elegans

Cell

Volumn 165, Issue 1, 2016, Pages 88-99

  Houri Ze'evi, Leah ^a   Korem, Yael ^b   Sheftel, Hila ^b   Faigenbloom, Lior ^a   Toker, Itai Antoine ^a   Dagan, Yael ^a   Awad, Lama ^a   Degani, Luba ^a   Alon, Uri ^b   Rechavi, Oded ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; DOUBLE STRANDED RNA; HELMINTH RNA; SMALL UNTRANSLATED RNA;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; FEEDBACK SYSTEM; GENE SILENCING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; RNA INTERFERENCE; RNA SEQUENCE; ANIMAL; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANIMALS; CAENORHABDITIS ELEGANS; EPIGENESIS, GENETIC; FEEDBACK; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, HELMINTH; RNA, SMALL INTERFERING; RNA, SMALL UNTRANSLATED;

EID: 84961778139     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.02.057     Document Type: Article

References (56)

1. R.M. Alcazar, R. Lin, and A.Z. Fire Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans Genetics 180 2008 1275 1288
2. S. Anava, R. Posner, and O. Rechavi The soft genome Worm 3 2015 e989798
3. S. Anders, P.T. Pyl, and W. Huber HTSeq A Python framework to work with high-throughput sequencing data Bioinformatics 31 2015 166 169
4. K. Aoki, H. Moriguchi, T. Yoshioka, K. Okawa, and H. Tabara In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans EMBO J. 26 2007 5007 5019
5. A. Ashe, A. Sapetschnig, E.-M. Weick, J. Mitchell, M.P. Bagijn, A.C. Cording, A.-L. Doebley, L.D. Goldstein, N.J. Lehrbach, J. Le Pen, and et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans Cell 150 2012 88 99
6. M.J. Axtell Butter: High-precision genomic alignment of small RNA-seq data bioRxiv. 2014 10.1101/007427
7. A.C. Billi, S.E.J. Fischer, and J.K. Kim Endogenous RNAi pathways in C. elegans WormBook May 7 2014 1 49 10.1895/wormbook.1.170.1
8. B.A. Buckley, K.B. Burkhart, S.G. Gu, G. Spracklin, A. Kershner, H. Fritz, J. Kimble, A. Fire, and S. Kennedy A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality Nature 489 2012 447 451
9. N.O. Burton, K.B. Burkhart, and S. Kennedy Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 108 2011 19683 19688
10. G. Cecere, S. Hoersch, S. O'Keeffe, R. Sachidanandam, and A. Grishok Global effects of the CSR-1 RNA interference pathway on the transcriptional landscape Nat. Struct. Mol. Biol. 21 2014 358 365
11. J.M. Claycomb, P.J. Batista, K.M. Pang, W. Gu, J.J. Vasale, J.C. van Wolfswinkel, D.A. Chaves, M. Shirayama, S. Mitani, R.F. Ketting, and et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation Cell 139 2009 123 134
12. D. Crews, R. Gillette, I. Miller-Crews, A.C. Gore, and M.K. Skinner Nature, nurture and epigenetics Mol. Cell. Endocrinol. 398 2014 42 52
13. B.F.M. de Albuquerque, M. Placentino, and R.F. Ketting Maternal piRNAs are essential for germline development following de novo establishment of Endo-siRNAs in Caenorhabditis elegans Dev. Cell 34 2015 448 456
14. T.F. Duchaine, J.A. Wohlschlegel, S. Kennedy, Y. Bei, D. Conte Jr., K. Pang, D.R. Brownell, S. Harding, S. Mitani, G. Ruvkun, and et al. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways Cell 124 2006 343 354
15. A. Fire, S. Xu, M.K. Montgomery, S.A. Kostas, S.E. Driver, and C.C. Mello Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 391 1998 806 811
16. L.J. Gaydos, W. Wang, and S. Strome H3K27me and PRC2 transmit a memory of repression across generations and during development Science 345 2014 1515 1518
17. J.I. Gent, A.T. Lamm, D.M. Pavelec, J.M. Maniar, P. Parameswaran, L. Tao, S. Kennedy, and A.Z. Fire Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans soma Mol. Cell 37 2010 679 689
18. E.L. Greer, T.J. Maures, D. Ucar, A.G. Hauswirth, E. Mancini, J.P. Lim, B.A. Benayoun, Y. Shi, and A. Brunet Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans Nature 479 2011 365 371
19. E.L. Greer, M.A. Blanco, L. Gu, E. Sendinc, J. Liu, D. Aristizábal-Corrales, C.-H. Hsu, L. Aravind, C. He, and Y. Shi DNA Methylation on N6-Adenine in C. elegans Cell 161 2015 868 878
20. A. Grishok, H. Tabara, and C.C. Mello Genetic requirements for inheritance of RNAi in C. elegans Science 287 2000 2494 2497
21. S.G. Gu, J. Pak, S. Guang, J.M. Maniar, S. Kennedy, and A. Fire Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint Nat. Genet. 44 2012 157 164
22. S. Guang, A.F. Bochner, D.M. Pavelec, K.B. Burkhart, S. Harding, J. Lachowiec, and S. Kennedy An Argonaute transports siRNAs from the cytoplasm to the nucleus Science 321 2008 537 541
23. E. Heard, and R.A. Martienssen Transgenerational epigenetic inheritance: Myths and mechanisms Cell 157 2014 95 109
24. E. Jablonka Epigenetic inheritance and plasticity: The responsive germline Prog. Biophys. Mol. Biol. 111 2013 99 107
25. E. Jablonka, and M.J. Lamb Soft inheritance: Challenging the modern synthesis Genet. Mol. Biol. 31 2008 389 395
26. R.S. Kamath, M. Martinez-Campos, P. Zipperlen, A.G. Fraser, and J. Ahringer Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans Genome Biol. 2 2001 RESEARCH0002
27. W.G. Kelly Transgenerational epigenetics in the germline cycle of Caenorhabditis elegans Epigenetics Chromatin 7 2014 6
28. E.V. Koonin Calorie restriction à Lamarck Cell 158 2014 237 238
29. M.I. Love, W. Huber, and S. Anders Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol. 15 2014 550
30. R. Lu, M. Maduro, F. Li, H.W. Li, G. Broitman-Maduro, W.X. Li, and S.W. Ding Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans Nature 436 2005 1040 1043
31. M.J. Luteijn, P. van Bergeijk, L.J.T. Kaaij, M.V. Almeida, E.F. Roovers, E. Berezikov, and R.F. Ketting Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans EMBO J. 31 2012 3422 3430
32. J.M. Maniar, and A.Z. Fire EGO-1, a C. elegans RdRP, modulates gene expression via production of mRNA-templated short antisense RNAs Curr. Biol. 21 2011 449 459
33. M. Martin Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet J. 17 2011 10
34. J.A. Melo, and G. Ruvkun Inactivation of conserved C. elegans genes engages pathogen- A nd xenobiotic-associated defenses Cell 149 2012 452 466
35. O. Rechavi, G. Minevich, and O. Hobert Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans Cell 147 2011 1248 1256
36. O. Rechavi, L. Houri-Ze'evi, S. Anava, W.S.S. Goh, S.Y. Kerk, G.J. Hannon, and O. Hobert Starvation-induced transgenerational inheritance of small RNAs in C. elegans Cell 158 2014 277 287
37. A. Sapetschnig, P. Sarkies, N.J. Lehrbach, and E.A. Miska Tertiary siRNAs mediate paramutation in C. elegans PLoS Genet. 11 2015 e1005078
38. P. Sarkies, A. Ashe, J. Le Pen, M.A. McKie, and E.A. Miska Competition between virus-derived and endogenous small RNAs regulates gene expression in Caenorhabditis elegans Genome Res. 23 2013 1258 1270
39. D. Schott, I. Yanai, and C.P. Hunter Natural RNA interference directs a heritable response to the environment Sci. Rep. 4 2014 7387
40. M. Seth, M. Shirayama, W. Gu, T. Ishidate, D. Conte Jr., and C.C. Mello The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression Dev. Cell 27 2013 656 663
41. M. Shirayama, M. Seth, H.-C. Lee, W. Gu, T. Ishidate, D. Conte Jr., and C.C. Mello piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline Cell 150 2012 65 77
42. A. Smardon, J.M. Spoerke, S.C. Stacey, M.E. Klein, N. Mackin, and E.M. Maine EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans Curr. Biol. 10 2000 169 178
43. C.A. Spike, J. Bader, V. Reinke, and S. Strome DEPS-1 promotes P-granule assembly and RNA interference in C. elegans germ cells Development 135 2008 983 993
44. F.A. Steiner, K.L. Okihara, S.W. Hoogstrate, T. Sijen, and R.F. Ketting RDE-1 slicer activity is required only for passenger-strand cleavage during RNAi in Caenorhabditis elegans Nat. Struct. Mol. Biol. 16 2009 207 211
45. M. Tijsterman, K.L. Okihara, K. Thijssen, and R.H.A. Plasterk PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans Curr. Biol. 12 2002 1535 1540
46. S. Tu, M.Z. Wu, J. Wang, A.D. Cutter, Z. Weng, and J.M. Claycomb Comparative functional characterization of the CSR-1 22G-RNA pathway in Caenorhabditis nematodes Nucleic Acids Res. 43 2015 208 224
47. J.C. van Wolfswinkel, J.M. Claycomb, P.J. Batista, C.C. Mello, E. Berezikov, and R.F. Ketting CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs Cell 139 2009 135 148
48. J.J. Vasale, W. Gu, C. Thivierge, P.J. Batista, J.M. Claycomb, E.M. Youngman, T.F. Duchaine, C.C. Mello, and D. Conte Jr. Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway Proc. Natl. Acad. Sci. USA 107 2010 3582 3587
49. N.L. Vastenhouw, K. Brunschwig, K.L. Okihara, F. Müller, M. Tijsterman, and R.H.A. Plasterk Gene expression: Long-term gene silencing by RNAi Nature 442 2006 882
50. L. Wang, D. Smith, S. Bot, L. Dellamary, A. Bloom, and A. Bot Noncoding RNA danger motifs bridge innate and adaptive immunity and are potent adjuvants for vaccination J. Clin. Invest. 110 2002 1175 1184
51. C.J. Wedeles, M.Z. Wu, and J.M. Claycomb Protection of germline gene expression by the C. elegans Argonaute CSR-1 Dev. Cell 27 2013 664 671
52. D. Weigel, and V. Colot Epialleles in plant evolution Genome Biol. 13 2012 249
53. W.F.R. Weldon Mendel's laws of alternative inheritance in peas Biometrika 1 1902 228 254
54. D. Wu, A.T. Lamm, and A.Z. Fire Competition between ADAR and RNAi pathways for an extensive class of RNA targets Nat. Struct. Mol. Biol. 18 2011 1094 1101
55. E. Yigit, P.J. Batista, Y. Bei, K.M. Pang, C.-C.G. Chen, N.H. Tolia, L. Joshua-Tor, S. Mitani, M.J. Simard, and C.C. Mello Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi Cell 127 2006 747 757
56. J.J. Zhuang, and C.P. Hunter The influence of competition among C. elegans small RNA pathways on development Genes (Basel) October 19 2012 3