Home LiteratureArticle Details
PMID: 22119442 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans.

Cell ·Vol. 147 ·No. 6 ·2011-12-09 ·Pages 1248-56

Rechavi O, Minevich G, Hobert O

Abstract

Induced expression of the Flock House virus in the soma of C. elegans results in the RNAi-dependent production of virus-derived, small-interfering RNAs (viRNAs), which in turn silence the viral genome. We show here that the viRNA-mediated viral silencing effect is transmitted in a non-Mendelian manner to many ensuing generations. We show that the viral silencing agents, viRNAs, are transgenerationally transmitted in a template-independent manner and work in trans to silence viral genomes present in animals that are deficient in producing their own viRNAs. These results provide evidence for the transgenerational inheritance of an acquired trait, induced by the exposure of animals to a specific, biologically relevant physiological challenge. The ability to inherit such extragenic information may provide adaptive benefits to an animal.

MeSH Terms
Animals Caenorhabditis elegans/cytology,genetics,immunology,virology Extrachromosomal Inheritance Genome, Viral Nodaviridae/genetics,metabolism RNA Interference RNA, Small Interfering/metabolism RNA, Viral/metabolism
Chemicals
RNA, Small Interfering RNA, Viral
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Rechavi Oded
Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University Medical Center, New York, NY 10032, USA. [email protected]
Minevich Gregory
Hobert Oliver
References (36)
36 references, click to expand
  1. Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans.
    Genetics. 2008 Nov;180(3):1275-88 PMID: 18757930
  2. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans.
    Nature. 2005 Aug 18;436(7053):1040-1043 PMID: 16107851
  3. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring.
    Nature. 2010 Oct 21;467(7318):963-6 PMID: 20962845
  4. Induction and suppression of RNA silencing by an animal virus.
    Science. 2002 May 17;296(5571):1319-21 PMID: 12016316
  5. Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants.
    Nature. 2005 Jul 28;436(7050):593-7 PMID: 16049496
  6. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi.
    Nature. 2003 Jan 16;421(6920):231-7 PMID: 12529635
  7. Epigenetic mechanisms and the transgenerational effects of maternal care.
    Front Neuroendocrinol. 2008 Jun;29(3):386-97 PMID: 18462782
  8. A Genome-Wide RNAi Screen for Factors Involved in Neuronal Specification in Caenorhabditis elegans.
    PLoS Genet. 2011 Jun;7(6):e1002109 PMID: 21698137
  9. In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans.
    EMBO J. 2007 Dec 12;26(24):5007-19 PMID: 18007599
  10. A greedy algorithm for aligning DNA sequences.
    J Comput Biol. 2000 Feb-Apr;7(1-2):203-14 PMID: 10890397
  11. An RIG-I-Like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditis elegans.
    PLoS Pathog. 2009 Feb;5(2):e1000286 PMID: 19197349
  12. Stable inheritance of an acquired behavior in Caenorhabditis elegans.
    Curr Biol. 2010 Oct 26;20(20):R877-8 PMID: 20971427
  13. An extensive class of small RNAs in Caenorhabditis elegans.
    Science. 2001 Oct 26;294(5543):862-4 PMID: 11679672
  14. Functional genomic analysis of RNA interference in C. elegans.
    Science. 2005 May 20;308(5725):1164-7 PMID: 15790806
  15. Meiotic silencing by unpaired DNA.
    Cell. 2001 Dec 28;107(7):905-16 PMID: 11779466
  16. Genetic requirements for inheritance of RNAi in C. elegans.
    Science. 2000 Mar 31;287(5462):2494-7 PMID: 10741970
  17. Nodavirus RNA replication: mechanism and harnessing to vaccinia virus recombinants.
    Arch Virol Suppl. 1994;9:407-16 PMID: 7518273
  18. RNA interference is an antiviral defence mechanism in Caenorhabditis elegans.
    Nature. 2005 Aug 18;436(7053):1044-7 PMID: 16107852
  19. Quasispecies theory and the behavior of RNA viruses.
    PLoS Pathog. 2010 Jul 22;6(7):e1001005 PMID: 20661479
  20. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals.
    Cell. 2000 Mar 31;101(1):25-33 PMID: 10778853
  21. Distinct roles for RDE-1 and RDE-4 during RNA interference in Caenorhabditis elegans.
    RNA. 2001 Oct;7(10):1397-402 PMID: 11680844
  22. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class.
    Science. 2007 Jan 12;315(5809):244-7 PMID: 17158288
  23. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.
    Nature. 1998 Feb 19;391(6669):806-11 PMID: 9486653
  24. An antiviral role for the RNA interference machinery in Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18420-4 PMID: 16339901
  25. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi.
    Cell. 2006 Nov 17;127(4):747-57 PMID: 17110334
  26. Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans soma.
    Mol Cell. 2010 Mar 12;37(5):679-89 PMID: 20116306
  27. RDE-1 slicer activity is required only for passenger-strand cleavage during RNAi in Caenorhabditis elegans.
    Nat Struct Mol Biol. 2009 Feb;16(2):207-11 PMID: 19151723
  28. Gene expression: long-term gene silencing by RNAi.
    Nature. 2006 Aug 24;442(7105):882 PMID: 16929289
  29. Replication of flock house virus RNAs from primary transcripts made in cells by RNA polymerase II.
    J Virol. 1997 Apr;71(4):3323-7 PMID: 9060703
  30. On the nature of in vivo requirements for rde-4 in RNAi and developmental pathways in C. elegans.
    RNA Biol. 2011 May-Jun;8(3):458-67 PMID: 21519199
  31. Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene.
    Genetics. 1997 May;146(1):227-38 PMID: 9136012
  32. Quality control and preprocessing of metagenomic datasets.
    Bioinformatics. 2011 Mar 15;27(6):863-4 PMID: 21278185
  33. Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs.
    Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1606-11 PMID: 20080648
  34. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems.
    PLoS Pathog. 2010 Feb 12;6(2):e1000764 PMID: 20169186
  35. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses.
    PLoS Biol. 2011 Jan 25;9(1):e1000586 PMID: 21283608
  36. The RNA silencing pathway: the bits and pieces that matter.
    PLoS Comput Biol. 2005 Jul;1(2):155-65 PMID: 16110335
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2011.10.042
Email
[email protected]
Published
2011-12-09
Epub
2011-00-23
Pages
1248-56
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3250924
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NICHD NIH HHS · T32HD055165 · United States
Databases
GEO
GSE33334
External Links
PubMed source DOI: 10.1016/j.cell.2011.10.042 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2