Starvation-induced transgenerational inheritance of small RNAs in C. elegans

Cell

Volumn 158, Issue 2, 2014, Pages 277-287

  Rechavi, Oded ^a,b   Houri Ze'Evi, Leah ^a   Anava, Sarit ^a   Goh, Wee Siong Sho ^c   Kerk, Sze Yen ^b   Hannon, Gregory J ^c   Hobert, Oliver ^b  

^a TEL AVIV UNIVERSITY   (Israel)

^b NewYork Presbyterian Hospital   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA; SMALL RNA; UNCLASSIFIED DRUG; VITELLOGENIN; MICRORNA; SMALL INTERFERING RNA;

ARTICLE; BASE PAIRING; BIOGENESIS; CAENORHABDITIS ELEGANS; DEVELOPMENTAL STAGE; ENVIRONMENTAL CHANGE; GENE SILENCING; GENE TARGETING; GENETIC CODE; HERMAPHRODITE; INHERITANCE; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROGENY; PROTEIN METABOLISM; STARVATION; UPREGULATION; ADULT; GENE EXPRESSION REGULATION; NUTRITION; RNA SEQUENCE; RNA TRANSPORT; TRANSGENERATIONAL INHERITANCE;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; EPIGENESIS, GENETIC; HUMANS; LONGEVITY; MODELS, ANIMAL; RNA INTERFERENCE; RNA, HELMINTH; RNA, SMALL UNTRANSLATED; STARVATION;

EID: 84904561365     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.06.020     Document Type: Article

References (60)

1. Billi,A.C.; Fischer, S.E.J.; and Kim, J.K. (2014). Endogenous RNAi pathways in C. elegans. WormBook, ed. The C. elegans Research Community, WormBook, http://dx.doi.org/10.1895/wormbook.1.170.1, http://www.wormbook.org.
2. A. Ashe, A. Sapetschnig, E.-M. Weick, J. Mitchell, M.P. Bagijn, A.C. Cording, A.-L. Doebley, L.D. Goldstein, N.J. Lehrbach, and J. Le Pen et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans Cell 150 2012 88 99
3. M.P. Bagijn, L.D. Goldstein, A. Sapetschnig, E.-M. Weick, S. Bouasker, N.J. Lehrbach, M.J. Simard, and E.A. Miska Function, targets, and evolution of Caenorhabditis elegans piRNAs Science 337 2012 574 578
4. L.R. Baugh To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest Genetics 194 2013 539 555
5. A.C. Billi, A.F. Alessi, V. Khivansara, T. Han, M. Freeberg, S. Mitani, and J.K. Kim The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs PLoS Genet. 8 2012 e1002617
6. 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
7. 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
8. L.O. Bygren, G. Kaati, and S. Edvinsson Longevity determined by paternal ancestors' nutrition during their slow growth period Acta Biotheor. 49 2001 53 59
9. 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, and R.F. Ketting et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation Cell 139 2009 123 134
10. C.C. Conine, J.J. Moresco, W. Gu, M. Shirayama, D. Conte Jr.; J.R. Yates 3rd, and C.C. Mello Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans Cell 155 2013 1532 1544
11. A.S. DePina, W.B. Iser, S.-S. Park, S. Maudsley, M.A. Wilson, and C.A. Wolkow Regulation of Caenorhabditis elegans vitellogenesis by DAF-2/IIS through separable transcriptional and posttranscriptional mechanisms BMC Physiol. 11 2011 11
12. 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
13. S.E.J. Fischer, T.A. Montgomery, C. Zhang, N. Fahlgren, P.C. Breen, A. Hwang, C.M. Sullivan, J.C. Carrington, and G. Ruvkun The ERI-6/7 helicase acts at the first stage of an siRNA amplification pathway that targets recent gene duplications PLoS Genet. 7 2011 e1002369
14. K. Gapp, A. Jawaid, P. Sarkies, J. Bohacek, P. Pelczar, J. Prados, L. Farinelli, E. Miska, and I.M. Mansuy Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice Nat. Neurosci. 17 2014 667 669
15. 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
16. 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
17. A. Grishok Biology and Mechanisms of Short RNAs in Caenorhabditis elegans Adv. Genet. 83 2013 1 69
18. W. Gu, M. Shirayama, D. Conte Jr.; J. Vasale, P.J. Batista, J.M. Claycomb, J.J. Moresco, E.M. Youngman, J. Keys, and M.J. Stoltz et al. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline Mol. Cell 36 2009 231 244
19. 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
20. S.E. Hall, G.-W. Chirn, N.C. Lau, and P. Sengupta RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans RNA 19 2013 306 319
21. T. Han, A.P. Manoharan, T.T. Harkins, P. Bouffard, C. Fitzpatrick, D.S. Chu, D. Thierry-Mieg, J. Thierry-Mieg, and J.K. Kim 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 106 2009 18674 18679
22. S.C. Harvey, and H.E. Orbidans All eggs are not equal: the maternal environment affects progeny reproduction and developmental fate in Caenorhabditis elegans PLoS ONE 6 2011 e25840
23. E. Heard, and R.A. Martienssen Transgenerational epigenetic inheritance: myths and mechanisms Cell 157 2014 95 109
24. S. Hellwig, and B.L. Bass A starvation-induced noncoding RNA modulates expression of Dicer-regulated genes Proc. Natl. Acad. Sci. USA 105 2008 12897 12902
25. E. Jablonka, and M.J. Lamb Soft inheritance: challenging the modern synthesis Genet. Mol. Biol. 31 2008 389 395
26. G. Kaati, L.O. Bygren, M. Pembrey, and M. Sjöström Transgenerational response to nutrition, early life circumstances and longevity Eur. J. Hum. Genet. 15 2007 784 790
27. L.M. Kamminga, J.C. van Wolfswinkel, M.J. Luteijn, L.J.T. Kaaij, M.P. Bagijn, A. Sapetschnig, E.A. Miska, E. Berezikov, and R.F. Ketting Differential impact of the HEN1 homolog HENN-1 on 21U and 26G RNAs in the germline of Caenorhabditis elegans PLoS Genet. 8 2012 e1002702
28. E.V. Koonin, and Y.I. Wolf Is evolution Darwinian or/and Lamarckian? Biol. Direct 4 2009 42
29. R.C. Lee, C.M. Hammell, and V. Ambros Interacting endogenous and exogenous RNAi pathways in Caenorhabditis elegans RNA 12 2006 589 597
30. H.-C. Lee, W. Gu, M. Shirayama, E. Youngman, D. Conte Jr.; and C.C. Mello C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts Cell 150 2012 78 87
31. A.R. Mansisidor, G. Cecere, S. Hoersch, M.B. Jensen, T. Kawli, L.M. Kennedy, V. Chavez, M.-W. Tan, J.D. Lieb, and A. Grishok A conserved PHD finger protein and endogenous RNAi modulate insulin signaling in Caenorhabditis elegans PLoS Genet. 7 2011 e1002299
32. C.S. Maxwell, I. Antoshechkin, N. Kurhanewicz, J.A. Belsky, and L.R. Baugh Nutritional control of mRNA isoform expression during developmental arrest and recovery in C. elegans Genome Res. 22 2012 1920 1929
33. S. Meloche, and P.P. Roux F-box proteins elongate translation during stress recovery Sci. Signal. 5 2012 pe25
34. T.A. Montgomery, Y.-S. Rim, C. Zhang, R.H. Dowen, C.M. Phillips, S.E.J. Fischer, and G. Ruvkun PIWI associated siRNAs and piRNAs specifically require the Caenorhabditis elegans HEN1 ortholog henn-1 PLoS Genet. 8 2012 e1002616
35. R.C. Painter, C. Osmond, P. Gluckman, M. Hanson, D.I.W. Phillips, and T.J. Roseboom Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life BJOG 115 2008 1243 1249
36. J. Pak, and A. Fire Distinct populations of primary and secondary effectors during RNAi in C. elegans Science 315 2007 241 244
37. O. Rechavi Guest list or black list: heritable small RNAs as immunogenic memories Trends Cell Biol. 24 2013 212 220
38. 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
39. V. Reinke, I.S. Gil, S. Ward, and K. Kazmer Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans Development 131 2004 311 323
40. J.-J. Remy Stable inheritance of an acquired behavior in Caenorhabditis elegans Curr. Biol. 20 2010 R877 R878
41. J.-J. Remy, and O. Hobert An interneuronal chemoreceptor required for olfactory imprinting in C. elegans Science 309 2005 787 790
42. 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
43. 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
44. T. Sijen, J. Fleenor, F. Simmer, K.L. Thijssen, S. Parrish, L. Timmons, R.H. Plasterk, and A. Fire On the role of RNA amplification in dsRNA-triggered gene silencing Cell 107 2001 465 476
45. V.J. Simpson, T.E. Johnson, and R.F. Hammen Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging Nucleic Acids Res. 14 1986 6711 6719
46. 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
47. S. Song, W. Wang, and P. Hu Famine, death, and madness: schizophrenia in early adulthood after prenatal exposure to the Chinese Great Leap Forward Famine Soc. Sci. Med. 68 2009 1315 1321
48. S.A. Stanner, K. Bulmer, C. Andrès, O.E. Lantseva, V. Borodina, V.V. Poteen, and J.S. Yudkin Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study BMJ 315 1997 1342 1348
49. M.G. Sterken, L.B. Snoek, K.J. Bosman, J. Daamen, J.A.G. Riksen, J. Bakker, G.P. Pijlman, and J.E. Kammenga A heritable antiviral RNAi response limits Orsay virus infection in Caenorhabditis elegans N2 PLoS ONE 9 2014 e89760
50. 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
51. 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
52. 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
53. 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
54. X. Zhang, R. Zabinsky, Y. Teng, M. Cui, and M. Han microRNAs play critical roles in the survival and recovery of Caenorhabditis elegans from starvation-induced L1 diapause Proc. Natl. Acad. Sci. USA 108 2011 17997 18002
55. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
56. S. Anders, P.T. Pyl, and W. Huber HTSeq A Python framework to work with high-throughput sequencing data 2014 Cold Spring Harbor Labs Journals Cold Spring Harbor
57. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359
58. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin 1000 Genome Project Data Processing Subgroup The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2009 2078 2079
59. M. Martin Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet.journal 17 2011 10
60. R. Suzuki, and H. Shimodaira Pvclust: an R package for assessing the uncertainty in hierarchical clustering Bioinformatics 22 2006 1540 1542