Home LiteratureArticle Details
PMID: 18571452 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans.

Molecular cell ·Vol. 31 ·No. 1 ·2008-07-11 ·Pages 67-78

Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, Kasschau KD, Chaves DA, Gu W, Vasale JJ, Duan S, Conte D, Luo S, Schroth GP, Carrington JC, Bartel DP, Mello CC

Abstract

In metazoans, Piwi-related Argonaute proteins have been linked to germline maintenance, and to a class of germline-enriched small RNAs termed piRNAs. Here we show that an abundant class of 21 nucleotide small RNAs (21U-RNAs) are expressed in the C. elegans germline, interact with the C. elegans Piwi family member PRG-1, and depend on PRG-1 activity for their accumulation. The PRG-1 protein is expressed throughout development and localizes to nuage-like structures called P granules. Although 21U-RNA loci share a conserved upstream sequence motif, the mature 21U-RNAs are not conserved and, with few exceptions, fail to exhibit complementarity or evidence for direct regulation of other expressed sequences. Our findings demonstrate that 21U-RNAs are the piRNAs of C. elegans and link this class of small RNAs and their associated Piwi Argonaute to the maintenance of temperature-dependent fertility.

MeSH Terms
Animals Argonaute Proteins Base Sequence Caenorhabditis elegans/cytology,genetics,metabolism Caenorhabditis elegans Proteins/metabolism Fertility Gene Expression Regulation Germ Cells/cytology,metabolism Models, Biological Molecular Sequence Data Mutation/genetics Protein Binding RNA, Helminth/metabolism RNA, Small Interfering/metabolism RNA-Induced Silencing Complex Regulatory Sequences, Nucleic Acid/genetics
Chemicals
Argonaute Proteins Caenorhabditis elegans Proteins PRG-1 protein, C elegans RNA, Helminth RNA, Small Interfering RNA-Induced Silencing Complex
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Batista Pedro J
Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.
Ruby J Graham
Claycomb Julie M
Chiang Rosaria
Fahlgren Noah
Kasschau Kristin D
Chaves Daniel A
Gu Weifeng
Vasale Jessica J
Duan Shenghua
Conte Darryl
Luo Shujun
Schroth Gary P
Carrington James C
Bartel David P
Mello Craig C
References (40)
40 references, click to expand
  1. The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs.
    RNA. 2007 Sep;13(9):1397-401 PMID: 17652135
  2. MicroRNA targeting specificity in mammals: determinants beyond seed pairing.
    Mol Cell. 2007 Jul 6;27(1):91-105 PMID: 17612493
  3. Characterization of the piRNA complex from rat testes.
    Science. 2006 Jul 21;313(5785):363-7 PMID: 16778019
  4. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC.
    Curr Biol. 2007 Jul 17;17(14):1265-72 PMID: 17604629
  5. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans.
    Science. 2001 Oct 26;294(5543):858-62 PMID: 11679671
  6. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis.
    Dev Cell. 2002 Jun;2(6):819-30 PMID: 12062093
  7. 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
  8. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish.
    Cell. 2007 Apr 6;129(1):69-82 PMID: 17418787
  9. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila.
    Science. 2007 Mar 16;315(5818):1587-90 PMID: 17322028
  10. A genome-wide screen identifies 27 genes involved in transposon silencing in C. elegans.
    Curr Biol. 2003 Aug 5;13(15):1311-6 PMID: 12906791
  11. A germline-specific class of small RNAs binds mammalian Piwi proteins.
    Nature. 2006 Jul 13;442(7099):199-202 PMID: 16751776
  12. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways.
    Cell. 2006 Jan 27;124(2):343-54 PMID: 16439208
  13. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction.
    Genes Dev. 2001 Jun 1;15(11):1349-60 PMID: 11390355
  14. Argonaute proteins: key players in RNA silencing.
    Nat Rev Mol Cell Biol. 2008 Jan;9(1):22-32 PMID: 18073770
  15. Developmentally regulated piRNA clusters implicate MILI in transposon control.
    Science. 2007 May 4;316(5825):744-7 PMID: 17446352
  16. MicroRNAs and other tiny endogenous RNAs in C. elegans.
    Curr Biol. 2003 May 13;13(10):807-18 PMID: 12747828
  17. The evolution of the scrotum and testicular descent in mammals: a phylogenetic view.
    J Theor Biol. 1999 Jan 7;196(1):61-72 PMID: 9892556
  18. PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans.
    Curr Biol. 2002 Sep 3;12(17):1535-40 PMID: 12225671
  19. Efficient target-selected mutagenesis in Caenorhabditis elegans: toward a knockout for every gene.
    Genome Res. 2007 May;17(5):649-58 PMID: 17416746
  20. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans.
    Cell. 2006 Dec 15;127(6):1193-207 PMID: 17174894
  21. Aligning multiple genomic sequences with the threaded blockset aligner.
    Genome Res. 2004 Apr;14(4):708-15 PMID: 15060014
  22. A novel class of small RNAs bind to MILI protein in mouse testes.
    Nature. 2006 Jul 13;442(7099):203-7 PMID: 16751777
  23. A novel class of small RNAs in mouse spermatogenic cells.
    Genes Dev. 2006 Jul 1;20(13):1709-14 PMID: 16766680
  24. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA.
    Dev Biol. 2000 Mar 15;219(2):315-33 PMID: 10694425
  25. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans.
    Cell. 1998 Sep 4;94(5):635-45 PMID: 9741628
  26. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome.
    Genes Dev. 2006 Aug 15;20(16):2214-22 PMID: 16882972
  27. Biogenesis and germline functions of piRNAs.
    Development. 2008 Jan;135(1):3-9 PMID: 18032451
  28. A gene expression map for Caenorhabditis elegans.
    Science. 2001 Sep 14;293(5537):2087-92 PMID: 11557892
  29. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells.
    Development. 2000 Feb;127(3):503-14 PMID: 10631171
  30. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila.
    Cell. 2007 Mar 23;128(6):1089-103 PMID: 17346786
  31. Sequence-specific inhibition of small RNA function.
    PLoS Biol. 2004 Apr;2(4):E98 PMID: 15024405
  32. Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi- interacting RNAs at their 3' ends.
    Genes Dev. 2007 Jul 1;21(13):1603-8 PMID: 17606638
  33. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  34. Photocleavable fluorescent nucleotides for DNA sequencing on a chip constructed by site-specific coupling chemistry.
    Proc Natl Acad Sci U S A. 2004 Apr 13;101(15):5488-93 PMID: 15064393
  35. The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated.
    Nat Struct Mol Biol. 2007 Apr;14(4):349-50 PMID: 17384646
  36. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis.
    Development. 2004 Feb;131(4):839-49 PMID: 14736746
  37. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal.
    Genes Dev. 1998 Dec 1;12(23):3715-27 PMID: 9851978
  38. piRNAs in the germ line.
    Science. 2007 Apr 20;316(5823):397 PMID: 17446387
  39. Specification of the germ line.
    WormBook. 2005 Jul 28;:1-10 PMID: 18050414
  40. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1982 Mar;79(5):1558-62 PMID: 7041123
Article Info
Journal
Molecular cell
Abbr.
Mol Cell
ISSN
1097-4164
Published
2008-07-11
Epub
2008-00-19
Pages
67-78
Language
English
Region
United States
NLM ID
9802571
PMCID
PMC2570341
Subset
IM
Grants
NIGMS NIH HHS · GM67031 · United States
NIGMS NIH HHS · R37 GM058800 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · R01 GM067031 · United States
NIGMS NIH HHS · R01 GM058800 · United States
NIGMS NIH HHS · R01 GM058800-10 · United States
NIGMS NIH HHS · GM58800 · United States
Databases
GEO
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: product@genelibs.com