Homeland security in the C. elegans germ line: Insights into the biogenesis and function of pirnas

Epigenetics

Volumn 9, Issue 1, 2014, Pages 62-74

  Kasper, Dionna M ^a   Gardner, Kathryn E ^a   Reinke, Valerie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

22g RNA; Argonaute proteins; Biogenesis; C. elegans; Epigenetics; Germ line; piRNA 21U RNA; Piwi PRG 1; Transgenerational silencing

Indexed keywords

SMALL INTERFERING RNA; TRANSPOSON;

ANIMAL; CAENORHABDITIS ELEGANS; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; GENOMIC INSTABILITY; GERM CELL; HUMAN; METABOLISM; REPRODUCTION; TRANSPOSON;

ANIMALS; CAENORHABDITIS ELEGANS; DNA TRANSPOSABLE ELEMENTS; EPIGENESIS, GENETIC; GENOMIC INSTABILITY; GERM CELLS; HUMANS; REPRODUCTION; RNA, SMALL INTERFERING;

EID: 84891923717     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.26647     Document Type: Article

References (67)

1. Siomi MC, Sato K, Pezic D, Aravin AA. PIWIinteracting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 2011; 12:246-58. PMID:21427766; http://dx.doi.org/10.1038/nrm3089
2. Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997; 124:2463-76. PMID:9199372
3. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006; 442:203-7. PMID:16751777
4. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006; 442:199-202. PMID:16751776
5. Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 2006; 20:1709-14. PMID:16766680; http://dx.doi.org/10.1101/gad.1434406
6. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 2006; 20:1732-43. PMID:16766679; http://dx.doi.org/10.1101/gad.1425706
7. Ishizu H, Siomi H, Siomi MC. Biology of PIWIinteracting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev 2012; 26:2361-73. PMID:23124062; http://dx.doi.org/10.1101/gad.203786.112
8. Luteijn MJ, Ketting RF. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet 2013; 14:523-34. PMID:23797853; http://dx.doi.org/10.1038/nrg3495
9. Saxe JP, Lin H. Small noncoding RNAs in the germline. Cold Spring Harb Perspect Biol 2011; 3:a002717. PMID:21669983; http://dx.doi.org/10.1101/cshperspect.a002717
10. Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, Kasschau KD, Chaves DA, Gu W, Vasale JJ, 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. PMID:18571452; http://dx.doi.org/10.1016/j.molcel.2008.06.002
11. Das PP, Bagijn MP, Goldstein LD, Woolford JR, Lehrbach NJ, Sapetschnig A, Buhecha HR, Gilchrist MJ, Howe KL, 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. PMID:18571451; http://dx.doi.org/10.1016/j.molcel.2008.06.003
12. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006; 127:1193-207. PMID:17174894; http://dx.doi.org/10.1016/j.cell.2006.10.040
13. Wang G, Reinke VA. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr Biol 2008; 18:861-7. PMID:18501605; http://dx.doi.org/10.1016/j.cub.2008.05.009
14. Billi AC, Alessi AF, Khivansara V, Han T, Freeberg M, Mitani S, Kim JK. The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs. PLoS Genet 2012; 8:e1002617. PMID:22548001; http://dx.doi.org/10.1371/journal.pgen.1002617
15. Kamminga LM, van Wolfswinkel JC, Luteijn MJ, Kaaij LJ, Bagijn MP, Sapetschnig A, Miska EA, Berezikov E, Ketting RF. Differential impact of the HEN1 homolog HENN-1 on 21U and 26G RNAs in the germline of Caenorhabditis elegans. PLoS Genet 2012; 8:e1002702. PMID:22829772; http://dx.doi.org/10.1371/journal.pgen.1002702
16. Montgomery TA, Rim YS, Zhang C, Dowen RH, Phillips CM, Fischer SE, Ruvkun G. PIWI associated siRNAs and piRNAs specifically require the Caenorhabditis elegans HEN1 ortholog henn-1. PLoS Genet 2012; 8:e1002616. PMID:22536158; http://dx.doi.org/10.1371/journal.pgen.1002616
17. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 1998; 12:3715-27. PMID:9851978; http://dx.doi.org/10.1101/gad.12.23.3715
18. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006; 313:320-4. PMID:16809489; http://dx.doi.org/10.1126/science.1129333
19. de Wit E, Linsen SE, Cuppen E, Berezikov E. Repertoire and evolution of miRNA genes in four divergent nematode species. Genome Res 2009; 19:2064-74. PMID:19755563; http://dx.doi.org/10.1101/gr.093781.109
20. Shi Z, Montgomery TA, Qi Y, Ruvkun G. Highthroughput sequencing reveals extraordinary fluidity of miRNA, piRNA, and siRNA pathways in nematodes. Genome Res 2013; 23:497-508. PMID:23363624; http://dx.doi.org/10.1101/gr.149112.112
21. Billi AC, Freeberg MA, Day AM, Chun SY, Khivansara V, Kim JK. A conserved upstream motif orchestrates autonomous, germline-enriched expression of Caenorhabditis elegans piRNAs. PLoS Genet 2013; 9:e1003392. PMID:23516384; http://dx.doi.org/10.1371/journal.pgen.1003392
22. Cecere G, Zheng GX, Mansisidor AR, Klymko KE, Grishok A. Promoters recognized by forkhead proteins exist for individual 21U-RNAs. Mol Cell 2012; 47:734-45. PMID:22819322; http://dx.doi.org/10.1016/j.molcel.2012.06.021
23. Gu W, Lee HC, Chaves D, Youngman EM, Pazour GJ, Conte D Jr., Mello CC. CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 2012; 151:1488-500. PMID:23260138; http://dx.doi.org/10.1016/j.cell.2012.11.023
24. Seila AC, Core LJ, Lis JT, Sharp PA. Divergent transcription: a new feature of active promoters. Cell Cycle 2009; 8:2557-64. PMID:19597342; http://dx.doi.org/10.4161/cc.8.16.9305
25. Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA. piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrialsurface lipid signaling. Dev Cell 2011; 20:376-87. PMID:21397848; http://dx.doi.org/10.1016/j.devcel.2011.01.004
26. Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, Matsumoto N, Nishizawa T, Nakanaga K, Aoki J, et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 2012; 491:284-7. PMID:23064230; http://dx.doi.org/10.1038/nature11509
27. Pane A, Wehr K, Schüpbach T. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 2007; 12:851-62. PMID:17543859; http://dx.doi.org/10.1016/j.devcel.2007.03.022
28. Watanabe T, Chuma S, Yamamoto Y, Kuramochi- Miyagawa S, Totoki Y, Toyoda A, Hoki Y, Fujiyama A, Shibata T, Sado T, et al. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell 2011; 20:364-75. PMID:21397847; http://dx.doi.org/10.1016/j.devcel.2011.01.005
29. Kawaoka S, Izumi N, Katsuma S, Tomari Y. 3′ end formation of PIWI-interacting RNAs in vitro. Mol Cell 2011; 43:1015-22. PMID:21925389; http://dx.doi.org/10.1016/j.molcel.2011.07.029
30. Horwich MD, Li C, Matranga C, Vagin V, Farley G, Wang P, Zamore PD. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 2007; 17:1265-72. PMID:17604629; http://dx.doi.org/10.1016/j.cub.2007.06.030
31. Saito K, Sakaguchi Y, Suzuki T, Suzuki T, Siomi H, Siomi MC. Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 3′ ends. Genes Dev 2007; 21:1603-8. PMID:17606638; http://dx.doi.org/10.1101/gad.1563607
32. Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 2006; 127:747-57. PMID:17110334; http://dx.doi.org/10.1016/j.cell.2006.09.033
33. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 2009; 25:355-76. PMID:19575643; http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175327
34. Bessereau JL. Transposons in C. elegans. WormBook 2006; 18:1-13. PMID:18023126
35. Sijen T, Plasterk RH. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 2003; 426:310-4. PMID:14628056; http://dx.doi.org/10.1038/nature02107
36. Claycomb JM. Caenorhabditis elegans small RNA pathways make their mark on chromatin. DNA Cell Biol 2012; 31(Suppl 1):S17-33. PMID:23046453; http://dx.doi.org/10.1089/dna.2012.1611
37. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D. MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol 2003; 13:807-18. PMID:12747828; http://dx.doi.org/10.1016/S0960-9822(03)00287-2
38. Gu W, Shirayama M, Conte D Jr., Vasale J, Batista PJ, Claycomb JM, Moresco JJ, Youngman EM, Keys J, Stoltz MJ, et al. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 2009; 36:231-44. PMID:19800275; http://dx.doi.org/10.1016/j.molcel.2009.09.020
39. Vastenhouw NL, Fischer SE, Robert VJ, Thijssen KL, Fraser AG, Kamath RS, Ahringer J, Plasterk RH. A genome-wide screen identifies 27 genes involved in transposon silencing in C. elegans. Curr Biol 2003; 13:1311-6. PMID:12906791; http://dx.doi.org/10.1016/S0960-9822(03)00539-6
40. Bagijn MP, Goldstein LD, Sapetschnig A, Weick EM, Bouasker S, Lehrbach NJ, Simard MJ, Miska EA. Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 2012; 337:574-8. PMID:22700655; http://dx.doi.org/10.1126/science.1220952
41. Lee HC, Gu W, Shirayama M, Youngman E, Conte D Jr., Mello CC. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 2012; 150:78-87. PMID:22738724; http://dx.doi.org/10.1016/j.cell.2012.06.016
42. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, Cording AC, Doebley AL, Goldstein LD, Lehrbach NJ, Le Pen J, et al. Pirnas can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 2012; 150:88-99. PMID:22738725; http://dx.doi.org/10.1016/j.cell.2012.06.018
43. Shirayama M, Seth M, Lee HC, Gu W, Ishidate T, Conte D Jr., Mello CC. PiRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 2012; 150:65-77. PMID:22738726; http://dx.doi.org/10.1016/j.cell.2012.06.015
44. Luteijn MJ, van Bergeijk P, Kaaij LJ, Almeida MV, Roovers EF, Berezikov E, Ketting RF. Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans. EMBO J 2012; 31:3422-30. PMID:22850670; http://dx.doi.org/10.1038/emboj.2012.213
45. Bessler JB, Andersen EC, Villeneuve AM. Differential localization and independent acquisition of the H3K9me2 and H3K9me3 chromatin modifications in the Caenorhabditis elegans adult germ line. PLoS Genet 2010; 6:e1000830. PMID:20107519; http://dx.doi.org/10.1371/journal.pgen.1000830
46. Buckley BA, Burkhart KB, Gu SG, Spracklin G, Kershner A, Fritz H, Kimble J, Fire A, Kennedy S. A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 2012; 489:447-51. PMID:22810588; http://dx.doi.org/10.1038/nature11352
47. Gu SG, Pak J, Guang S, Maniar JM, Kennedy S, Fire A. Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint. Nat Genet 2012; 44:157-64. PMID:22231482; http://dx.doi.org/10.1038/ng.1039
48. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, et al.; modENCODE Consortium. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2010; 330:1775-87. PMID:21177976; http://dx.doi.org/10.1126/science.1196914
49. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E, et al. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 2011; 21:245-54. PMID:21177963; http://dx.doi.org/10.1101/gr.114587.110
50. Zhong M, Niu W, Lu ZJ, Sarov M, Murray JI, Janette J, Raha D, Sheaffer KL, Lam HY, Preston E, et al. Genome-wide identification of binding sites defines distinct functions for Caenorhabditis elegans PHA-4/ FOXA in development and environmental response. PLoS Genet 2010; 6:e1000848. PMID:20174564; http://dx.doi.org/10.1371/journal.pgen.1000848
51. Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung MS, Ercan S, Ikegami K, Jensen M, Kolasinska-Zwierz P, et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 2011; 21:227-36. PMID:21177964; http://dx.doi.org/10.1101/gr.115519.110
52. Claycomb JM, Batista PJ, Pang KM, Gu W, Vasale JJ, van Wolfswinkel JC, Chaves DA, Shirayama M, Mitani S, Ketting RF, et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009; 139:123-34. PMID:19804758; http://dx.doi.org/10.1016/j.cell.2009.09.014
53. Updike D, Strome S. P granule assembly and function in Caenorhabditis elegans germ cells. J Androl 2010; 31:53-60. PMID:19875490; http://dx.doi.org/10.2164/jandrol.109.008292
54. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, Schultz N, Vreven T, Meignin C, Davis I, Zamore PD, et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 2012; 151:871-84. PMID:23141543; http://dx.doi.org/10.1016/j.cell.2012.09.040
55. Meister G. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 2013; 14:447-59. PMID:23732335; http://dx.doi.org/10.1038/nrg3462
56. Guang S, Bochner AF, Pavelec DM, Burkhart KB, Harding S, Lachowiec J, Kennedy S. An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science 2008; 321:537-41. PMID:18653886; http://dx.doi.org/10.1126/science.1157647
57. Burkhart KB, Guang S, Buckley BA, Wong L, Bochner AF, Kennedy S. A pre-mRNA-associating factor links endogenous siRNAs to chromatin regulation. PLoS Genet 2011; 7:e1002249. PMID:21901112; http://dx.doi.org/10.1371/journal.pgen.1002249
58. Burton NO, Burkhart KB, Kennedy S. Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2011; 108:19683-8. PMID:22106253; http://dx.doi.org/10.1073/pnas.1113310108
59. Alcazar RM, Lin R, Fire AZ. Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 2008; 180:1275-88. PMID:18757930; http://dx.doi.org/10.1534/genetics.108.089433
60. Vastenhouw NL, Brunschwig K, Okihara KL, Müller F, Tijsterman M, Plasterk RH. Gene expression: long-term gene silencing by RNAi. Nature 2006; 442:882. PMID:16929289; http://dx.doi.org/10.1038/442882a
61. Gassmann R, Rechtsteiner A, Yuen KW, Muroyama A, Egelhofer T, Gaydos L, Barron F, Maddox P, Essex A, Monen J, et al. An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 2012; 484:534-7. PMID:22495302; http://dx.doi.org/10.1038/nature10973
62. Aravin AA, Hannon GJ, Brennecke J. The PiwipiRNA pathway provides an adaptive defense in the transposon arms race. Science 2007; 318:761-4. PMID:17975059; http://dx.doi.org/10.1126/science.1146484
63. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. Discrete small RNAgenerating loci as master regulators of transposon activity in Drosophila. Cell 2007; 128:1089-103. PMID:17346786; http://dx.doi.org/10.1016/j.cell.2007.01.043
64. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 2007; 315:1587-90. PMID:17322028; http://dx.doi.org/10.1126/science.1140494
65. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA, Tóth KF. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 2013; 27:390-9. PMID:23392610; http://dx.doi.org/10.1101/gad.209841.112
66. Rozhkov NV, Hammell M, Hannon GJ. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 2013; 27:400-12. PMID:23392609; http://dx.doi.org/10.1101/gad.209767.112
67. Sienski G, Dönertas D, Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 2012; 151:964-80. PMID:23159368; http://dx.doi.org/10.1016/j.cell.2012.10.040