Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline.

doi:10.1016/J.MOLCEL.2009.09.020

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Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline.

Journal Article•DOI•

Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline.

Weifeng Gu¹, Masaki Shirayama¹, Darryl Conte¹, Jessica J. Vasale¹, Pedro J. Batista¹, Julie M. Claycomb¹, James J. Moresco², Elaine M. Youngman¹, Jennifer Keys¹, Matthew J. Stoltz¹, Chun-Cheih G. Chen¹, Daniel A. Chaves³, Daniel A. Chaves¹, Shenghua E. Duan¹, Krisitin D. Kasschau⁴, Noah Fahlgren⁴, John R. Yates², Shohei Mitani, James C. Carrington⁴, Craig C. Mello⁵, Craig C. Mello¹ - Show less +17 more•Institutions (5)

University of Massachusetts Medical School¹, Scripps Research Institute², Instituto de Medicina Molecular³, Oregon State University⁴, Howard Hughes Medical Institute⁵

23 Oct 2009-Molecular Cell (Cell Press)-Vol. 36, Iss: 2, pp 231-244

TL;DR: Deep-sequencing and genetic approaches are combined to explore the biogenesis and function of endo-siRNAs in C. elegans and show that, in the germline, one system is dependent on worm-specific AGOs, including WAGO-1, which localizes to germline nuage structures called P granules.

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About: This article is published in Molecular Cell.The article was published on 2009-10-23 and is currently open access. It has received 468 citations till now. The article focuses on the topics: RasiRNA & Argonaute.

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Journal Article•DOI•

Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals

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Upasna Sharma¹, Colin C. Conine¹, Jeremy M. Shea¹, Ana Bošković¹, Alan G. Derr¹, Xin Y. Bing¹, Clémence Belleannée², Alper Kucukural¹, Ryan W. Serra¹, Fengyun Sun¹, Lina Song¹, Benjamin R. Carone¹, Emiliano P. Ricci¹, Xin Zhiguo Li¹, Lucas Fauquier¹, Melissa J. Moore¹, Robert Sullivan², Craig C. Mello¹, Manuel Garber¹, Oliver J. Rando¹ - Show less +16 more•Institutions (2)

University of Massachusetts Medical School¹, Laval University²

22 Jan 2016-Science

TL;DR: The results shed light on sRNA biogenesis and its dietary regulation during posttesticular sperm maturation, and they also link tRNA fragments to regulation of endogenous retroelements active in the preimplantation embryo.

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Abstract: Several recent studies link parental environments to phenotypes in subsequent generations. In this work, we investigate the mechanism by which paternal diet affects offspring metabolism. Protein restriction in mice affects small RNA (sRNA) levels in mature sperm, with decreased let-7 levels and increased amounts of 5′ fragments of glycine transfer RNAs (tRNAs). In testicular sperm, tRNA fragments are scarce but increase in abundance as sperm mature in the epididymis. Epididymosomes (vesicles that fuse with sperm during epididymal transit) carry RNA payloads matching those of mature sperm and can deliver RNAs to immature sperm in vitro. Functionally, tRNA-glycine-GCC fragments repress genes associated with the endogenous retroelement MERVL, in both embryonic stem cells and embryos. Our results shed light on sRNA biogenesis and its dietary regulation during posttesticular sperm maturation, and they also link tRNA fragments to regulation of endogenous retroelements active in the preimplantation embryo.

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928 citations

Journal Article•DOI•

piRNAs Can Trigger a Multigenerational Epigenetic Memory in the Germline of C. elegans

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Alyson Ashe¹, Alexandra Sapetschnig², Alexandra Sapetschnig¹, Eva-Maria Weick², Eva-Maria Weick¹, Jacinth Mitchell³, Marloes P. Bagijn², Marloes P. Bagijn¹, Amy C. Cording¹, Amy C. Cording², Anna-Lisa Doebley³, Leonard D. Goldstein², Leonard D. Goldstein¹, Nicolas J. Lehrbach², Nicolas J. Lehrbach¹, Jérémie Le Pen¹, Jérémie Le Pen², Greta Pintacuda¹, Aisa Sakaguchi³, Peter Sarkies¹, Peter Sarkies², Shawn Ahmed³, Eric A. Miska¹, Eric A. Miska² - Show less +20 more•Institutions (3)

Wellcome Trust/Cancer Research UK Gurdon Institute¹, University of Cambridge², University of North Carolina at Chapel Hill³

06 Jul 2012-Cell

TL;DR: It is demonstrated that a germline nuclear small RNA/chromatin pathway can maintain stable inheritance for many generations when triggered by a piRNA-dependent foreign RNA response in C. elegans.

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689 citations

Cites background from "Distinct argonaute-mediated 22G-RNA..."

...RNAi effects are generally systemic (soma and germline) and are observed in the F1 generation, but the latter requires the generation of secondary siRNAs (Grishok et al., 2000; Pak and Fire, 2007; Sijen et al., 2007; Gu et al., 2009)....
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Journal Article•DOI•

piRNAs Initiate an Epigenetic Memory of Nonself RNA in the C. elegans Germline

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Masaki Shirayama¹, Meetu Seth¹, Heng-Chi Lee¹, Weifeng Gu¹, Takao Ishidate¹, Darryl Conte¹, Craig C. Mello¹ - Show less +3 more•Institutions (1)

University of Massachusetts Medical School¹

06 Jul 2012-Cell

TL;DR: It is shown that the Piwi Argonaute PRG-1 and its genomically encoded piRNA cofactors initiate permanent silencing, and maintenance depends on chromatin factors and the WAGOArgonaute pathway.

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569 citations

Journal Article•DOI•

A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality

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Bethany A. Buckley¹, Kirk B. Burkhart¹, Sam Guoping Gu², George Spracklin¹, Aaron M. Kershner¹, Heidi Fritz¹, Judith Kimble¹, Andrew Fire², Scott Kennedy¹ - Show less +5 more•Institutions (2)

University of Wisconsin-Madison¹, Stanford University²

20 Sep 2012-Nature

TL;DR: It is proposed that Caenorhabditis elegans use the RNAi inheritance machinery to transmit epigenetic information, accrued by past generations, into future generations to regulate important biological processes.

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Abstract: Double-stranded RNA interference (RNAi) in Caenorhabditis elegans is heritable; here a genetic screen for factors required for RNAi inheritance identifies the nuclear-localized Argonaute gene hrde-1, which acts in the germ cells of progeny to promote multigenerational inheritance of silencing and, also, germline immortality. Gene silencing due to RNA-mediated interference (RNAi) in the nematode Caenorhabditis elegans can be inherited for more than five generations. Here, Scott Kennedy and colleagues have performed a genetic screen for defects in the transmission of RNAi-silencing signals to future generations, and identify a nuclear-localized Argonaute protein termed HRDE-1. It associates with small-interfering RNAs and acts in the germ cells of the progeny of animals exposed to double-stranded RNA to promote multigenerational inheritance of silencing. The authors propose that one biological function of the RNAi-inheritance machinery is to transmit ‘germline immortality’ in the form of small RNAs, selected for their ability to promote fertility, across generational boundaries. Epigenetic information is frequently erased near the start of each new generation1. In some cases, however, epigenetic information can be transmitted from parent to progeny (multigenerational epigenetic inheritance)2. A particularly notable example of this type of epigenetic inheritance is double-stranded RNA-mediated gene silencing in Caenorhabditis elegans. This RNA-mediated interference (RNAi) can be inherited for more than five generations3,4,5,6,7,8. To understand this process, here we conduct a genetic screen for nematodes defective in transmitting RNAi silencing signals to future generations. This screen identified the heritable RNAi defective 1 (hrde-1) gene. hrde-1 encodes an Argonaute protein that associates with small interfering RNAs in the germ cells of progeny of animals exposed to double-stranded RNA. In the nuclei of these germ cells, HRDE-1 engages the nuclear RNAi defective pathway to direct the trimethylation of histone H3 at Lys 9 (H3K9me3) at RNAi-targeted genomic loci and promote RNAi inheritance. Under normal growth conditions, HRDE-1 associates with endogenously expressed short interfering RNAs, which direct nuclear gene silencing in germ cells. In hrde-1- or nuclear RNAi-deficient animals, germline silencing is lost over generational time. Concurrently, these animals exhibit steadily worsening defects in gamete formation and function that ultimately lead to sterility. These results establish that the Argonaute protein HRDE-1 directs gene-silencing events in germ-cell nuclei that drive multigenerational RNAi inheritance and promote immortality of the germ-cell lineage. We propose that C. elegans use the RNAi inheritance machinery to transmit epigenetic information, accrued by past generations, into future generations to regulate important biological processes.

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464 citations

Cites background from "Distinct argonaute-mediated 22G-RNA..."

...RNAs templates (10,15), suggesting that the HRDE-1 22G siRNAs are synthesized via RdRP activity in germ cells (see supplemental discussion)....
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...3 is predicted to encode an Ago not known to contribute to gene-silencing (9,10)....
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...3 was referred to once previously in the literature as worm Ago (wago)-9 (10)....
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Journal Article•DOI•

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

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Oded Rechavi¹, Oded Rechavi², Leah Houri-Zeevi², Sarit Anava², Wee Siong Sho Goh³, Sze Yen Kerk¹, Gregory J. Hannon³, Oliver Hobert¹ - Show less +4 more•Institutions (3)

Columbia University Medical Center¹, Tel Aviv University², Watson School of Biological Sciences³

17 Jul 2014-Cell

TL;DR: It is found that starvation-induced developmental arrest, a natural and drastic environmental change, leads to the generation of small RNAs that are inherited through at least three consecutive generations, and genes that are essential for this multigenerational effect are defined.

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436 citations

Cites background from "Distinct argonaute-mediated 22G-RNA..."

...These are 22 nt long transcripts that possess a 50 guanosine, which are amplified by RdRPs and constitute themost abundant type of endogenous small RNAs (Gu et al., 2009; Pak and Fire, 2007)....
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...…Biophysics, Howard Hughes Medical Institute, New York, NY 10032, USA 3Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, Howard Hughes Medical Institute, New York 11724, USA *Correspondence: odedrechavi@gmail.com http://dx.doi.org/10.1016/j.cell.2014.06.020...
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References

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Journal Article•DOI•

The genetics of caenorhabditis elegans

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Sydney Brenner¹•Institutions (1)

Laboratory of Molecular Biology¹

01 May 1974-Genetics

TL;DR: In this paper, the authors describe methods for the isolation, complementation and mapping of mutants of Caenorhabditis elegans, a small free-living nematode worm.

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Abstract: Methods are described for the isolation, complementation and mapping of mutants of Caenorhabditis elegans, a small free-living nematode worm. About 300 EMS-induced mutants affecting behavior and morphology have been characterized and about one hundred genes have been defined. Mutations in 77 of these alter the movement of the animal. Estimates of the induced mutation frequency of both the visible mutants and X chromosome lethals suggests that, just as in Drosophila, the genetic units in C. elegans are large.

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13,247 citations

Journal Article•DOI•

Gene Expression Omnibus: NCBI gene expression and hybridization array data repository

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Ron Edgar¹, Michael Domrachev¹, Alex E. Lash¹•Institutions (1)

National Institutes of Health¹

01 Jan 2002-Nucleic Acids Research

TL;DR: The Gene Expression Omnibus (GEO) project was initiated in response to the growing demand for a public repository for high-throughput gene expression data and provides a flexible and open design that facilitates submission, storage and retrieval of heterogeneous data sets from high-power gene expression and genomic hybridization experiments.

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Abstract: The Gene Expression Omnibus (GEO) project was initiated in response to the growing demand for a public repository for high-throughput gene expression data. GEO provides a flexible and open design that facilitates submission, storage and retrieval of heterogeneous data sets from high-throughput gene expression and genomic hybridization experiments. GEO is not intended to replace in house gene expression databases that benefit from coherent data sets, and which are constructed to facilitate a particular analytic method, but rather complement these by acting as a tertiary, central data distribution hub. The three central data entities of GEO are platforms, samples and series, and were designed with gene expression and genomic hybridization experiments in mind. A platform is, essentially, a list of probes that define what set of molecules may be detected. A sample describes the set of molecules that are being probed and references a single platform used to generate its molecular abundance data. A series organizes samples into the meaningful data sets which make up an experiment. The GEO repository is publicly accessible through the World Wide Web at http://www.ncbi.nlm.nih.gov/geo.

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10,968 citations

"Distinct argonaute-mediated 22G-RNA..." refers methods in this paper

...These data are also available from GEO as a combined ‘‘Superseries’’ under the accession number GSE18231....
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...Microarray data are available from the Gene Expression Omnibus (GEO) (Edgar et al., 2002) under the accession number GSE18230....
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...Illumina data are available from GEO under the accession number GSE18215....
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Journal Article•

Genetics of Caenorhabditis elegans

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Munakata N

01 Apr 1989-Tanpakushitsu kakusan koso. Protein nucleic acid enzyme

8,375 citations

"Distinct argonaute-mediated 22G-RNA..." refers background or methods in this paper

...Worm Strains C. elegans culture and genetics were essentially as described (Brenner, 1974)....
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...elegans culture and genetics were essentially as described (Brenner, 1974)....
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Journal Article•DOI•

Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila

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Julius Brennecke¹, Alexei A. Aravin¹, Alexander Stark², Monica Dus¹, Manolis Kellis², Ravi Sachidanandam¹, Gregory J. Hannon¹ - Show less +3 more•Institutions (2)

Watson School of Biological Sciences¹, Broad Institute²

23 Mar 2007-Cell

TL;DR: Examination of piwi-interacting RNAs associated with each Drosophila Piwi protein finds that Piwi and Aubergine bind RNAs that are predominantly antisense to transposons, whereas Ago3 complexes contain predominantly sense piRNAs.

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2,303 citations

"Distinct argonaute-mediated 22G-RNA..." refers background in this paper

...In flies, PIWI-mediated cleavage events appear to define the 5′ ends of new piRNAs (Brennecke et al., 2007; Gunawardane et al., 2007), whereas 3′ end maturation occurs through an undefined mechanism that ultimately results in the 2′-O-methylation of the 3′ residue (Klattenhoff and Theurkauf, 2008)....
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...In flies, PIWI-mediated cleavage events appear to define the 50 ends of new piRNAs (Brennecke et al., 2007; Gunawardane et al., 2007), whereas 30 end maturation occurs through an undefined mechanism that ultimately results in the 20-O-methylation of the 30 residue (Klattenhoff and Theurkauf, 2008)....
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Journal Article•DOI•

Small silencing RNAs: an expanding universe

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Megha Ghildiyal¹, Phillip D. Zamore¹•Institutions (1)

University of Massachusetts Medical School¹

01 Feb 2009-Nature Reviews Genetics

TL;DR: Since the discovery in 1993 of the first small silencing RNA, a dizzying number of small RNA classes have been identified, including microRNAs (miRNAs), small interfering RNAs (siRNAs) and Piwi-interacting RNAs.

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Abstract: Since the discovery in 1993 of the first small silencing RNA, a dizzying number of small RNA classes have been identified, including microRNAs (miRNAs), small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). These classes differ in their biogenesis, their modes of target regulation and in the biological pathways they regulate. There is a growing realization that, despite their differences, these distinct small RNA pathways are interconnected, and that small RNA pathways compete and collaborate as they regulate genes and protect the genome from external and internal threats.

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2,266 citations

"Distinct argonaute-mediated 22G-RNA..." refers background in this paper

...Mo can be distinguished based on a number of factors, including mechanism of biogenesis, mode of regulation or function, and the Argonaute (AGO) proteins with which they interact (Ghildiyal and Zamore, 2009)....
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...Small RNA classes Mo can be distinguished based on a number of factors, including mechanism of biogenesis, mode of regulation or function, and the Argonaute (AGO) proteins with which they interact (Ghildiyal and Zamore, 2009)....
[...]