Multiple Epigenetic Mechanisms and the piRNA Pathway Enforce LINE1 Silencing during Adult Spermatogenesis

Molecular Cell

Volumn 50, Issue 4, 2013, Pages 601-608

  DiGiacomo, Monica ^a   Comazzetto, Stefano ^a   Saini, Harpreet ^b   DeFazio, Serena ^a   Carrieri, Claudia ^a   Morgan, Marcos ^a   Vasiliauskaite, Lina ^a   Benes, Vladimir ^c   Enright, AntonJ ^b   O'Carroll, Dónal ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^b EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LYSINE; NUCLEIC ACID BINDING PROTEIN; PIWI INTERACTING RNA; PIWI PROTEIN; PROTEIN MILI; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DNA METHYLATION; EPIGENETICS; GENE; GENE SILENCING; LINE1 GENE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SPERMATOGENESIS; TESTIS; TRANSPOSON;

AGE FACTORS; ANIMALS; ARGONAUTE PROTEINS; BLOTTING, WESTERN; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION; GENE SILENCING; HISTONES; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; LYSINE; MALE; METHYLATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MITOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

EID: 84878205591     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.04.026     Document Type: Article

References (30)

1. Aravin A.A., Sachidanandam R., Girard A., Fejes-Toth K., Hannon G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007, 316:744-747.
2. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 2008, 31:785-799.
3. Blanco-Rodríguez J. gammaH2AX marks the main events of the spermatogenic process. Microsc. Res. Tech. 2009, 72:823-832.
4. Bourc'his D., Bestor T.H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004, 431:96-99.
5. Branciforte D., Martin S.L. Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol. Cell. Biol. 1994, 14:2584-2592.
6. Brown J.P., Bullwinkel J., Baron-Lühr B., Billur M., Schneider P., Winking H., Singh P.B. HP1gamma function is required for male germ cell survival and spermatogenesis. Epigenetics Chromatin 2010, 3:9.
7. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 2007, 12:503-514.
8. De Fazio S., Bartonicek N., Di Giacomo M., Abreu-Goodger C., Sankar A., Funaya C., Antony C., Moreira P.N., Enright A.J., O'Carroll D. The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 2011, 480:259-263.
9. Deng W., Lin H. miwi, a murine homolog of piwi, encodesa cytoplasmic protein essential for spermatogenesis. Dev. Cell 2002, 2:819-830.
10. Farley F.W., Soriano P., Steffen L.S., Dymecki S.M. Widespread recombinase expression using FLPeR (flipper) mice. Genesis 2000, 28:106-110.
11. Hobbs R.M., Fagoonee S., Papa A., Webster K., Altruda F., Nishinakamura R., Chai L., Pandolfi P.P. Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 2012, 10:284-298.
12. Ishizu H., Siomi H., Siomi M.C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012, 26:2361-2373.
13. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131:839-849.
14. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., Asada N., Kojima K., Yamaguchi Y., Ijiri T.W., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008, 22:908-917.
15. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodríguez J., Jasin M., Keeney S., Bonner W.M., Burgoyne P.S. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 2001, 27:271-276.
16. Monesi V. Ribonucleic Acid Synthesis during Mitosis and Meiosis in the Mouse Testis. J.Cell Biol. 1964, 22:521-532.
17. Paronetto M.P., Messina V., Barchi M., Geremia R., Richard S., Sette C. Sam68 marks the transcriptionally active stages of spermatogenesis and modulates alternative splicing in male germ cells. Nucleic Acids Res. 2011, 39:4961-4974.
18. Patel D.J., Ma J.B., Yuan Y.R., Ye K., Pei Y., Kuryavyi V., Malinina L., Meister G., Tuschl T. Structural biology of RNA silencing and its functional implications. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:81-93.
19. Peters A.H., Kubicek S., Mechtler K., O'Sullivan R.J., Derijck A.A., Perez-Burgos L., Kohlmaier A., Opravil S., Tachibana M., Shinkai Y., et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 2003, 12:1577-1589.
20. Pillai R.S., Chuma S. piRNAs and their involvement in male germline development in mice. Dev. Growth Differ. 2012, 54:78-92.
21. Reuter M., Berninger P., Chuma S., Shah H., Hosokawa M., Funaya C., Antony C., Sachidanandam R., Pillai R.S. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 2011, 480:264-267.
22. Sadate-Ngatchou P.I., Payne C.J., Dearth A.T., Braun R.E. Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 2008, 46:738-742.
23. Schwenk F., Baron U., Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995, 23:5080-5081.
24. Song J.J., Smith S.K., Hannon G.J., Joshua-Tor L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 2004, 305:1434-1437.
25. Soper S.F., van der Heijden G.W., Hardiman T.C., Goodheart M., Martin S.L., de Boer P., Bortvin A. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 2008, 15:285-297.
26. Tachibana M., Sugimoto K., Fukushima T., Shinkai Y. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J.Biol. Chem. 2001, 276:25309-25317.
27. Tachibana M., Sugimoto K., Nozaki M., Ueda J., Ohta T., Ohki M., Fukuda M., Takeda N., Niida H., Kato H., Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 2002, 16:1779-1791.
28. Tachibana M., Nozaki M., Takeda N., Shinkai Y. Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J. 2007, 26:3346-3359.
29. Webster K.E., O'Bryan M.K., Fletcher S., Crewther P.E., Aapola U., Craig J., Harrison D.K., Aung H., Phutikanit N., Lyle R., et al. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl. Acad. Sci. USA 2005, 102:4068-4073.
30. Wen J., Brogna S. Nonsense-mediated mRNA decay. Biochem. Soc. Trans. 2008, 36:514-516.