Co-option of the piRNA pathway for germline-specific alternative splicing of C. elegans TOR

Cell Reports

Volumn 8, Issue 6, 2014, Pages 1609-1616

  Barberán Soler, Sergio ^a   Fontrodona, Laura ^b   Ribó, Anna ^a   Lamm, Ayelet T ^c   Iannone, Camilla ^a,d   Cerón, Julián ^b   Lehner, Ben ^a,d,e   Valcárcel, Juan ^a,d,e  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; PIWI INTERACTING RNA; PROTEIN CSR1; PROTEIN PRG1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; COMPLEMENTARY RNA; CSR-1 PROTEIN, C ELEGANS; DOUBLE STRANDED RNA; ISOPROTEIN; PRG-1 PROTEIN, C ELEGANS; TARGET OF RAPAMYCIN KINASE;

ADULT; ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE; GENETIC TRANSCRIPTION; GERM LINE; INTRON; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN FUNCTION; TARGET OF RAPAMYCIN GENE; TRANSPOSON; ANIMAL; GENETICS; GERM CELL; MALE; METABOLISM; MUTATION; RNA INTERFERENCE; SEQUENCE ANALYSIS;

CAENORHABDITIS ELEGANS;

ALTERNATIVE SPLICING; ANIMALS; ARGONAUTE PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GERM CELLS; MALE; MUTATION; PROTEIN ISOFORMS; RNA INTERFERENCE; RNA, ANTISENSE; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; TOR SERINE-THREONINE KINASES;

EID: 84907404331     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.08.016     Document Type: Article

References (56)

1. Ahmed S., Hodgkin J. MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 2000, 403:159-164.
2. Alló M., Buggiano V., Fededa J.P., Petrillo E., Schor I., de la Mata M., Agirre E., Plass M., Eyras E., Elela S.A., et al. Control of alternative splicing through siRNA-mediated transcriptional gene silencing. Nat. Struct. Mol. Biol. 2009, 16:717-724.
3. Ameyar-Zazoua M., Rachez C., Souidi M., Robin P., Fritsch L., Young R., Morozova N., Fenouil R., Descostes N., Andrau J.C., et al. Argonaute proteins couple chromatin silencing to alternative splicing. Nat. Struct. Mol. Biol. 2012, 19:998-1004.
4. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106.
5. Ashe A., Sapetschnig A., Weick E.M., Mitchell J., Bagijn M.P., Cording A.C., Doebley A.L., Goldstein L.D., Lehrbach N.J., Le Pen J., et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 2012, 150:88-99.
6. Avgousti D.C., Palani S., Sherman Y., Grishok A. CSR-1 RNAi pathway positively regulates histone expression in C. elegans. EMBO J. 2012, 31:3821-3832.
7. Bagijn M.P., Goldstein L.D., Sapetschnig A., Weick E.M., Bouasker S., Lehrbach N.J., Simard M.J., Miska E.A. Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 2012, 337:574-578.
8. Batista P.J., Ruby J.G., Claycomb J.M., Chiang R., Fahlgren N., Kasschau K.D., Chaves D.A., Gu W., Vasale J.J., Duan S., et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C.elegans. Mol. Cell 2008, 31:67-78.
9. Batsché E., Yaniv M., Muchardt C. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat. Struct. Mol. Biol. 2006, 13:22-29.
10. Braunschweig U., Gueroussov S., Plocik A.M., Graveley B.R., Blencowe B.J. Dynamic integration of splicing within gene regulatory pathways. Cell 2013, 152:1252-1269.
11. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
12. Buckley B.A., Burkhart K.B., Gu S.G., Spracklin G., Kershner A., Fritz H., Kimble J., Fire A., Kennedy S. A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 2012, 489:447-451.
13. Bühler M., Verdel A., Moazed D. Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 2006, 125:873-886.
14. Burkhart K.B., Guang S., Buckley B.A., Wong L., Bochner A.F., Kennedy S. A pre-mRNA-associating factor links endogenous siRNAs to chromatin regulation. PLoS Genet. 2011, 7:e1002249.
15. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013, 14:100-112.
16. Cecere G., Hoersch S., O'Keeffe S., Sachidanandam R., Grishok A. Global effects of the CSR-1 RNA interference pathway on the transcriptional landscape. Nat. Struct. Mol. Biol. 2014, 21:358-365.
17. Claycomb J.M., Batista P.J., Pang K.M., Gu W., Vasale J.J., van Wolfswinkel J.C., Chaves D.A., Shirayama M., Mitani S., Ketting R.F., et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009, 139:123-134.
18. Cornu M., Albert V., Hall M.N. mTOR in aging, metabolism, and cancer. Curr. Opin. Genet. Dev. 2013, 23:53-62.
19. Das P.P., Bagijn M.P., Goldstein L.D., Woolford J.R., Lehrbach N.J., Sapetschnig A., Buhecha H.R., Gilchrist M.J., Howe K.L., Stark R., et al. Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol. Cell 2008, 31:79-90.
20. Gent J.I., Schvarzstein M., Villeneuve A.M., Gu S.G., Jantsch V., Fire A.Z., Baudrimont A. A Caenorhabditis elegans RNA-directed RNA polymerase in sperm development and endogenous RNA interference. Genetics 2009, 183:1297-1314.
21. Gent J.I., Lamm A.T., Pavelec D.M., Maniar J.M., Parameswaran P., Tao L., Kennedy S., Fire A.Z. Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans soma. Mol. Cell 2010, 37:679-689.
22. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
23. Greer E.L., Beese-Sims S.E., Brookes E., Spadafora R., Zhu Y., Rothbart S.B., Aristizábal-Corrales D., Chen S., Badeaux A.I., Jin Q., et al. A histone methylation network regulates transgenerational epigenetic memory in C. elegans. Cell Reports 2014, 7:113-126.
24. Gu W., Shirayama M., Conte D., Vasale J., Batista P.J., Claycomb J.M., Moresco J.J., Youngman E.M., Keys J., Stoltz M.J., et al. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol. Cell 2009, 36:231-244.
25. Guang S., Bochner A.F., Burkhart K.B., Burton N., Pavelec D.M., Kennedy S. Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 2010, 465:1097-1101.
26. Hubbard E.J., Korta D.Z., Dalfó D. Physiological control of germline development. Adv. Exp. Med. Biol. 2013, 757:101-131.
27. Jen C.H., Michalopoulos I., Westhead D.R., Meyer P. Natural antisense transcripts with coding capacity in Arabidopsis may have a regulatory role that is not linked to double-stranded RNA degradation. Genome Biol. 2005, 6:R51.
28. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
29. Kapitonov V.V., Jurka J. Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 2001, 98:8714-8719.
30. Kapitonov V.V., Jurka J. Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet. 2007, 23:521-529.
31. Kenyon C.J. The genetics of ageing. Nature 2010, 464:504-512.
32. Koelle M.R., Horvitz H.R. EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 1996, 84:115-125.
33. Lamm A.T., Stadler M.R., Zhang H., Gent J.I., Fire A.Z. Multimodal RNA-seq using single-strand, double-strand, and CircLigase-based capture yields a refined and extended description of the C. elegans transcriptome. Genome Res. 2011, 21:265-275.
34. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
35. Lee M.H., Schedl T. RNA insitu hybridization of dissected gonads. WormBook 2006, 1-7.
36. Lee H.C., Gu W., Shirayama M., Youngman E., Conte D., Mello C.C. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 2012, 150:78-87.
37. Lehner B., Williams G., Campbell R.D., Sanderson C.M. Antisense transcripts in the human genome. Trends Genet. 2002, 18:63-65.
38. Luteijn M.J., Ketting R.F. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat. Rev. Genet. 2013, 14:523-534.
39. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
40. Miller M.A. Sperm and oocyte isolation methods for biochemical and proteomic analysis. Methods Mol. Biol. 2006, 351:193-201.
41. Morrissy A.S., Griffith M., Marra M.A. Extensive relationship between antisense transcription and alternative splicing in the human genome. Genome Res. 2011, 21:1203-1212.
42. Nishida K.M., Saito K., Mori T., Kawamura Y., Nagami-Okada T., Inagaki S., Siomi H., Siomi M.C. Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA 2007, 13:1911-1922.
43. Okamura K., Chung W.J., Ruby J.G., Guo H., Bartel D.P., Lai E.C. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 2008, 453:803-806.
44. Pak J., Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 2007, 315:241-244.
45. Pasquinelli A.E. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 2012, 13:271-282.
46. Porta-de-la-Riva M., Fontrodona L., Villanueva A., Cerón J. Basic Caenorhabditis elegans methods: synchronization and observation. J.Vis. Exp. 2012, e4019.
47. Rouget C., Papin C., Boureux A., Meunier A.C., Franco B., Robine N., Lai E.C., Pelisson A., Simonelig M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467:1128-1132.
48. Seidel H.S., Kimble J. The oogenic germline starvation response in C. elegans. PLoS ONE 2011, 6:e28074.
49. Seth M., Shirayama M., Gu W., Ishidate T., Conte D., Mello C.C. The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression. Dev. Cell 2013, 27:656-663.
50. Shirayama M., Seth M., Lee H.C., Gu W., Ishidate T., Conte D., Mello C.C. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 2012, 150:65-77.
51. Simon M., Sarkies P., Ikegami K., Doebley A.L., Goldstein L.D., Mitchell J., Sakaguchi A., Miska E.A., Ahmed S. Reduced insulin/IGF-1 signaling restores germ cell immortality to caenorhabditis elegans Piwi mutants. Cell Reports 2014, 7:762-773.
52. Taliaferro J.M., Aspden J.L., Bradley T., Marwha D., Blanchette M., Rio D.C. Two new and distinct roles for Drosophila Argonaute-2 in the nucleus: alternative pre-mRNA splicing and transcriptional repression. Genes Dev. 2013, 27:378-389.
53. Urano J., Sato T., Matsuo T., Otsubo Y., Yamamoto M., Tamanoi F. Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc. Natl. Acad. Sci. USA 2007, 104:3514-3519.
54. Wang G., Reinke V. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr. Biol. 2008, 18:861-867.
55. Wedeles C.J., Wu M.Z., Claycomb J.M. Protection of germline gene expression by the C. elegans Argonaute CSR-1. Dev. Cell 2013, 27:664-671.
56. Yigit E., Batista P.J., Bei Y., Pang K.M., Chen C.C., Tolia N.H., Joshua-Tor L., Mitani S., Simard M.J., Mello C.C. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 2006, 127:747-757.