Restricted and non-essential redundancy of RNAi and piRNA pathways in mouse oocytes


Autoři: Eliska Taborska aff001;  Josef Pasulka aff001;  Radek Malik aff001;  Filip Horvat aff001;  Irena Jenickova aff003;  Zoe Jelić Matošević aff002;  Petr Svoboda aff001
Působiště autorů: Institute of Molecular Genetics of the Czech Academy of Sciences, Prague 4, Czech Republic aff001;  Bioinformatics Group, Division of Molecular Biology, Department of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia aff002;  Czech Centre of Phenogenomics, Institute of Molecular Genetics of the Czech Academy of Sciences, Vestec, Czech Republic aff003
Vyšlo v časopise: Restricted and non-essential redundancy of RNAi and piRNA pathways in mouse oocytes. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008261
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008261

Souhrn

Germline genome defense evolves to recognize and suppress retrotransposons. One of defensive mechanisms is the PIWI-associated RNA (piRNA) pathway, which employs small RNAs for sequence-specific repression. The loss of the piRNA pathway in mice causes male sterility while females remain fertile. Unlike spermatogenic cells, mouse oocytes posses also RNA interference (RNAi), another small RNA pathway capable of retrotransposon suppression. To examine whether RNAi compensates the loss of the piRNA pathway, we produced a new RNAi pathway mutant DicerSOM and crossed it with a catalytically-dead mutant of Mili, an essential piRNA gene. Normal follicular and oocyte development in double mutants showed that RNAi does not suppress a strong ovarian piRNA knock-out phenotype. However, we observed redundant and non-redundant targeting of specific retrotransposon families illustrating stochasticity of recognition and targeting of invading retrotransposons. Intracisternal A Particle retrotransposon was mainly targeted by the piRNA pathway, MaLR and RLTR10 retrotransposons were targeted mainly by RNAi. Double mutants showed accumulations of LINE-1 retrotransposon transcripts. However, we did not find strong evidence for transcriptional activation and mobilization of retrotransposition competent LINE-1 elements suggesting that while both defense pathways are simultaneously expendable for ovarian oocyte development, yet another transcriptional silencing mechanism prevents mobilization of LINE-1 elements.

Klíčová slova:

Mammalian genomics – Mouse models – Oocytes – Retrotransposons – RNA interference – RNA sequencing – Small interfering RNAs – Transcriptome analysis


Zdroje

1. Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, et al. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199. doi: 10.1186/s13059-018-1577-z 30454069.

2. Craig NL, Chandler M, Gellert M, Lambowitz AM, Rice PA, Sandmeyer SB. Mobile DNA III. Craig NL, editor: AMS press; 2015.

3. International Human Genome Sequencing Consortium, Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860–921. doi: 10.1038/35057062 11237011.

4. Mouse Genome Sequencing Consortium, Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002;420(6915):520–62. doi: 10.1038/nature01262 12466850.

5. Kazazian HH Jr. Mobile elements and disease. Curr Opin Genet Dev. 1998;8(3):343–50. doi: 10.1016/s0959-437x(98)80092-0 9690999.

6. Kuff EL, Lueders KK. The intracisternal A-particle gene family: structure and functional aspects. Adv Cancer Res. 1988;51:183–276. doi: 10.1016/s0065-230x(08)60223-7 3146900.

7. Dewannieux M, Dupressoir A, Harper F, Pierron G, Heidmann T. Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat Genet. 2004;36(5):534–9. doi: 10.1038/ng1353 15107856.

8. Ostertag EM, Kazazian HH Jr. Biology of mammalian L1 retrotransposons. Annu Rev Genet. 2001;35:501–38. doi: 10.1146/annurev.genet.35.102401.091032 11700292.

9. DeBerardinis RJ, Kazazian HH Jr. Analysis of the promoter from an expanding mouse retrotransposon subfamily. Genomics. 1999;56(3):317–23. doi: 10.1006/geno.1998.5729 10087199.

10. Speek M. Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol. 2001;21(6):1973–85. doi: 10.1128/MCB.21.6.1973-1985.2001 11238933.

11. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, et al. Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol. 2001;21(4):1429–39. doi: 10.1128/MCB.21.4.1429-1439.2001 11158327.

12. Smit AFA, Hubley R, Green P. RepeatMasker Open-4.0. <http://www.repeatmasker.org>. 2013–2015.

13. Crichton JH, Dunican DS, Maclennan M, Meehan RR, Adams IR. Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline. Cellular and molecular life sciences: CMLS. 2014;71(9):1581–605. doi: 10.1007/s00018-013-1468-0 24045705.

14. Ernst C, Odom DT, Kutter C. The emergence of piRNAs against transposon invasion to preserve mammalian genome integrity. Nature communications. 2017;8(1):1411. doi: 10.1038/s41467-017-01049-7 29127279.

15. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–103. Epub 2007/03/10. doi: 10.1016/j.cell.2007.01.043 17346786.

16. Roovers EF, Rosenkranz D, Mahdipour M, Han CT, He N, de Chuva Sousa Lopes SM, et al. Piwi proteins and piRNAs in mammalian oocytes and early embryos. Cell Rep. 2015;10(12):2069–82. doi: 10.1016/j.celrep.2015.02.062 25818294.

17. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004;131(4):839–49. doi: 10.1242/dev.00973 14736746

18. Deng W, Lin HF. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Developmental Cell. 2002;2(6):819–30. doi: 10.1016/s1534-5807(02)00165-x 12062093

19. Carmell MA, Girard A, van de Kant HJG, Bourc'his D, Bestor TH, de Rooij DG, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Developmental Cell. 2007;12(4):503–14. doi: 10.1016/j.devcel.2007.03.001 17395546

20. Lim AK, Lorthongpanich C, Chew TG, Tan CW, Shue YT, Balu S, et al. The nuage mediates retrotransposon silencing in mouse primordial ovarian follicles. Development. 2013;140(18):3819–25. Epub 2013/08/09. doi: 10.1242/dev.099184 23924633.

21. Kabayama Y, Toh H, Katanaya A, Sakurai T, Chuma S, Kuramochi-Miyagawa S, et al. Roles of MIWI, MILI and PLD6 in small RNA regulation in mouse growing oocytes. Nucleic Acids Research. 2017;45(9):5387–98. doi: 10.1093/nar/gkx027 28115634

22. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Molecular Cell. 2008;31(6):785–99. doi: 10.1016/j.molcel.2008.09.003 18922463

23. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008;22(7):908–17. Epub 2008/04/03. doi: 10.1101/gad.1640708 18381894.

24. De Fazio S, Bartonicek N, Di Giacomo M, Abreu-Goodger C, Sankar A, Funaya C, et al. The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature. 2011;480(7376):259–63. doi: 10.1038/nature10547 22020280.

25. Watanabe T, Cui X, Yuan Z, Qi H, Lin H. MIWI2 targets RNAs transcribed from piRNA-dependent regions to drive DNA methylation in mouse prospermatogonia. EMBO J. 2018;37(18). doi: 10.15252/embj.201695329 30108053.

26. Pezic D, Manakov SA, Sachidanandam R, Aravin AA. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes & Development. 2014;28(13):1410–28. doi: 10.1101/gad.240895.114 24939875

27. Di Giacomo M, Comazzetto S, Saini H, De Fazio S, Carrieri C, Morgan M, et al. Multiple Epigenetic Mechanisms and the piRNA Pathway Enforce LINE1 Silencing during Adult Spermatogenesis. Molecular Cell. 2013;50(4):601–8. doi: 10.1016/j.molcel.2013.04.026 23706823

28. Manakov S, Pezic D, Marinov G, Pastor W, Sachidanandam R, Aravin A. MIWI2 and MILI Have Differential Effects on piRNA Biogenesis and DNA Methylation. Cell Reports. 2015;12(8):1234–43. doi: 10.1016/j.celrep.2015.07.036 26279574

29. Molaro A, Falciatori I, Hodges E, Aravin AA, Marran K, Rafii S, et al. Two waves of de novo methylation during mouse germ cell development. Genes & Development. 2014;28(14):1544–9. doi: 10.1101/gad.244350.114 25030694

30. Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, et al. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(26):11841–6. doi: 10.1073/pnas.1003953107 20534472

31. Stein P, Rozhkov NV, Li F, Cardenas FL, Davydenko O, Vandivier LE, et al. Essential Role for endogenous siRNAs during meiosis in mouse oocytes. PLoS Genet. 2015;11(2):e1005013. doi: 10.1371/journal.pgen.1005013 25695507.

32. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature. 2008;453(7194):534–8. Epub 2008/04/12. doi: 10.1038/nature06904 18404147.

33. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806–11. doi: 10.1038/35888 9486653.

34. Wianny F, Zernicka-Goetz M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol. 2000;2(2):70–5. doi: 10.1038/35000016 10655585

35. Svoboda P, Stein P, Hayashi H, Schultz RM. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development. 2000;127(19):4147–56. 10976047

36. Svoboda P. Renaissance of mammalian endogenous RNAi. FEBS Lett. 2014;588(15):2550–6. doi: 10.1016/j.febslet.2014.05.030 24873877.

37. Svoboda P, Stein P, Anger M, Bernstein E, Hannon GJ, Schultz RM. RNAi and expression of retrotransposons MuERV-L and IAP in preimplantation mouse embryos. Developmental biology. 2004;269(1):276–85. doi: 10.1016/j.ydbio.2004.01.028 15081373.

38. Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM, et al. Critical roles for Dicer in the female germline. Genes Dev. 2007;21(6):682–93. doi: 10.1101/gad.1521307 17369401.

39. Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, Sun YA, et al. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007;21(6):644–8. doi: 10.1101/gad.418707 17369397.

40. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature. 2008;453(7194):539–43. Epub 2008/04/12. doi: 10.1038/nature06908 18404146.

41. Garcia-Lopez J, Hourcade Jde D, Alonso L, Cardenas DB, del Mazo J. Global characterization and target identification of piRNAs and endo-siRNAs in mouse gametes and zygotes. Biochim Biophys Acta. 2014;1839(6):463–75. doi: 10.1016/j.bbagrm.2014.04.006 24769224.

42. Larriba E, Del Mazo J. An integrative piRNA analysis of mouse gametes and zygotes reveals new potential origins and gene regulatory roles. Sci Rep. 2018;8(1):12832. Epub 2018/08/29. doi: 10.1038/s41598-018-31032-1 30150632.

43. Yang Q, Lin J, Liu M, Li R, Tian B, Zhang X, et al. Highly sensitive sequencing reveals dynamic modifications and activities of small RNAs in mouse oocytes and early embryos. Sci Adv. 2016;2(6):e1501482. doi: 10.1126/sciadv.1501482 27500274.

44. Flemr M, Malik R, Franke V, Nejepinska J, Sedlacek R, Vlahovicek K, et al. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell. 2013;155(4):807–16. Epub 2013/11/12. doi: 10.1016/j.cell.2013.10.001 24209619.

45. Veselovska L, Smallwood SA, Saadeh H, Stewart KR, Krueger F, Maupetit-Mehouas S, et al. Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol. 2015;16:209. doi: 10.1186/s13059-015-0769-z 26408185.

46. Franke V, Ganesh S, Karlic R, Malik R, Pasulka J, Horvat F, et al. Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes. Genome Research. 2017;27(8):1384–94. doi: 10.1101/gr.216150.116 28522611

47. Much C, Auchynnikava T, Pavlinic D, Buness A, Rappsilber J, Benes V, et al. Endogenous Mouse Dicer Is an Exclusively Cytoplasmic Protein. Plos Genetics. 2016;12(6). doi: 10.1371/journal.pgen.1006095 27254021

48. Gan H, Cai T, Lin X, Wu Y, Wang X, Yang F, et al. Integrative proteomic and transcriptomic analyses reveal multiple post-transcriptional regulatory mechanisms of mouse spermatogenesis. Mol Cell Proteomics. 2013;12(5):1144–57. doi: 10.1074/mcp.M112.020123 23325766.

49. Deng Q, Ramskold D, Reinius B, Sandberg R. Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science. 2014;343(6167):193–6. doi: 10.1126/science.1245316 24408435.

50. Yamaguchi S, Hong K, Liu R, Inoue A, Shen L, Zhang K, et al. Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res. 2013;23(3):329–39. doi: 10.1038/cr.2013.22 23399596.

51. DeBerardinis RJ, Goodier JL, Ostertag EM, Kazazian HH Jr. Rapid amplification of a retrotransposon subfamily is evolving the mouse genome. Nat Genet. 1998;20(3):288–90. doi: 10.1038/3104 9806550.

52. Hardies SC, Wang L, Zhou L, Zhao Y, Casavant NC, Huang S. LINE-1 (L1) lineages in the mouse. Mol Biol Evol. 2000;17(4):616–28. doi: 10.1093/oxfordjournals.molbev.a026340 10742052.

53. Goodier JL, Ostertag EM, Du K, Kazazian HH Jr. A novel active L1 retrotransposon subfamily in the mouse. Genome Res. 2001;11(10):1677–85. doi: 10.1101/gr.198301 11591644.

54. Horvat F, Fulka H, Jankele R, Malik R, Jun M, Solcova K, et al. Role of Cnot6l in maternal mRNA turnover. Life Sci Alliance. 2018;1(4):e201800084. doi: 10.26508/lsa.201800084 30456367.

55. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell. 2007;129(1):69–82. doi: 10.1016/j.cell.2007.03.026 17418787

56. Nejepinska J, Malik R, Filkowski J, Flemr M, Filipowicz W, Svoboda P. dsRNA expression in the mouse elicits RNAi in oocytes and low adenosine deamination in somatic cells. Nucleic Acids Research. 2012;40(1):399–413. doi: 10.1093/nar/gkr702 21908396

57. Demeter T, Vaskovicova M, Malik R, Horvat F, Pasulka J, Svobodova E, et al. Main constraints for RNAi induced by expressed long dsRNA in mouse cells. Life Sci Alliance. 2019;2(1). doi: 10.26508/lsa.201800289 30808654.

58. Yang ZL, Chen KM, Pandey RR, Homolka D, Reuter M, Janeiro BKR, et al. PIWI Slicing and EXD1 Drive Biogenesis of Nuclear piRNAs from Cytosolic Targets of the Mouse piRNA Pathway. Molecular Cell. 2016;61(1):138–52. doi: 10.1016/j.molcel.2015.11.009 26669262

59. Zheng K, Wang PJ. Blockade of pachytene piRNA biogenesis reveals a novel requirement for maintaining post-meiotic germline genome integrity. PLoS Genet. 2012;8(11):e1003038. doi: 10.1371/journal.pgen.1003038 23166510.

60. Edson MA, Nagaraja AK, Matzuk MM. The mammalian ovary from genesis to revelation. Endocr Rev. 2009;30(6):624–712. doi: 10.1210/er.2009-0012 19776209.

61. Shin YH, Ren Y, Suzuki H, Golnoski KJ, Ahn HW, Mico V, et al. Transcription factors SOHLH1 and SOHLH2 coordinate oocyte differentiation without affecting meiosis I. J Clin Invest. 2017;127(6):2106–17. doi: 10.1172/JCI90281 28504655.

62. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science. 2007;318(5851):761–4. doi: 10.1126/science.1146484 17975059

63. Horman SR, Svoboda P, Luning Prak ET. The potential regulation of L1 mobility by RNA interference. J Biomed Biotechnol. 2006;2006(1):32713. doi: 10.1155/JBB/2006/32713 16877813.

64. Malki S, van der Heijden GW, O'Donnell KA, Martin SL, Bortvin A. A Role for Retrotransposon LINE-1 in Fetal Oocyte Attrition in Mice. Developmental Cell. 2014;29(5):521–33. doi: 10.1016/j.devcel.2014.04.027 24882376

65. Ecco G, Imbeault M, Trono D. KRAB zinc finger proteins. Development. 2017;144(15):2719–29. doi: 10.1242/dev.132605 28765213.

66. Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M, et al. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev. 2014;28(13):1397–409. doi: 10.1101/gad.241661.114 24939876.

67. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A. 1993;90(18):8424–8. doi: 10.1073/pnas.90.18.8424 8378314.

68. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281–308. doi: 10.1038/nprot.2013.143 24157548.

69. Nagy A. Manipulating the mouse embryo: a laboratory manual. 3rd ed. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; 2003. x, 764 p. p.

70. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi: 10.1093/bioinformatics/bts635 23104886.

71. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. doi: 10.1093/bioinformatics/btt656 24227677.

72. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281.

73. Di Giacomo M, Comazzetto S, Sampath SC, O'Carroll D. G9a co-suppresses LINE1 elements in spermatogonia. Epigenetics & Chromatin. 2014;7. doi: 10.1186/1756-8935-7-24 25276231

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2019 Číslo 12

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Nová éra v léčbě migrény
nový kurz
Autoři: MUDr. Eva Medová, MUDr. Tomáš Nežádal, Ph.D.

Význam nutraceutik u kardiovaskulárních onemocnění
Autoři:

Pneumowebinář
Autoři:

White paper - jak vidíme optimální péči o zubní náhrady
Autoři: MUDr. Jindřich Charvát, CSc.

Faktory ovlivňující léčbu levotyroxinem

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se