RNA-Mediated Epigenetic Heredity Requires the Cytosine Methyltransferase Dnmt2

PLoS Genetics

Volumn 9, Issue 5, 2013, Pages

  Kiani, Jafar ^a,b   Grandjean, Valérie ^a,b   Liebers, Reinhard ^c   Tuorto, Francesca ^c   Ghanbarian, Hossein ^a,b,d   Lyko, Frank ^c   Cuzin, François ^a,b   Rassoulzadegan, Minoo ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b INSERM   (France)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE 5) METHYLTRANSFERASE DNMT2; MICRORNA 124; RNA; TRANSCRIPTION FACTOR SOX6; TRANSFER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EPIGENETICS; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; HEREDITY; HETEROZYGOTE; MOUSE; NONHUMAN; PARAMUTATION; PHENOTYPE; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ANALYSIS; SPERM;

ANIMALS; COLOR; CYTOSINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HAIR; HEREDITY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICE; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; RNA, SMALL UNTRANSLATED; SOX9 TRANSCRIPTION FACTOR; SPERMATOZOA;

MUS;

EID: 84878498548     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003498     Document Type: Article

References (32)

1. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, et al. (2012) piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150: 88-99.
2. Chong S, Whitelaw E, (2004) Epigenetic germline inheritance. Current opinion in genetics & development 14: 692-696.
3. de Vanssay A, Bouge AL, Boivin A, Hermant C, Teysset L, et al. (2012) Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 490: 112-115.
4. Grandjean V, Gounon P, Wagner N, Martin L, Wagner KD, et al. (2009) The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136: 3647-3655.
5. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, et al. (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479: 365-371.
6. Johnson CL, Spence AM, (2011) Epigenetic licensing of germline gene expression by maternal RNA in C. elegans. Science 333: 1311-1314.
7. Nadeau JH, (2009) Transgenerational genetic effects on phenotypic variation and disease risk. Hum Mol Genet 18: R202-210.
8. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, et al. (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441: 469-474.
9. Shirayama M, Seth M, Lee HC, Gu W, Ishidate T, et al. (2012) piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150: 65-77.
10. Wagner KD, Wagner N, Ghanbarian H, Grandjean V, Gounon P, et al. (2008) RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 14: 962-969.
11. Gluckman PD, Hanson MA, Beedle AS, (2007) Non-genomic transgenerational inheritance of disease risk. BioEssays 29: 145-154.
12. Hemminki K, Forsti A, Bermejo JL, (2008) Estimating risks of common complex diseases: familial and population risks. J Med Genet 45: 126-127.
13. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, et al. (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14: 159-166.
14. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, et al. (2009) Finding the missing heritability of complex diseases. Nature 461: 747-753.
15. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA, (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429: 154.
16. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, et al. (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311: 395-398.
17. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, et al. (2010) RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes & development 24: 1590-1595.
18. Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S, et al. (2012) RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nature structural & molecular biology 19: 900-905.
19. Vassena R, Dee Schramm R, Latham KE, (2005) Species-dependent expression patterns of DNA methyltransferase genes in mammalian oocytes and preimplantation embryos. Mol Reprod Dev 72: 430-436.
20. Suzuki MM, Bird A, (2008) DNA methylation landscapes: provocative insights from epigenomics. Nature reviews Genetics 9: 465-476.
21. Stam M, Belele C, Dorweiler JE, Chandler VL, (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16: 1906-1918.
22. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, et al. (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic acids research 40: 5023-5033.
23. Mattick JS, Amaral PP, Dinger ME, Mercer TR, Mehler MF, (2009) RNA regulation of epigenetic processes. Bioessays 31: 51-59.
24. Mattick JS, Taft RJ, Faulkner GJ, (2010) A global view of genomic information-moving beyond the gene and the master regulator. Trends in genetics 26: 21-28.
25. Peng H, Shi J, Zhang Y, Zhang H, Liao S, et al. (2012) A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell research 22: 1609-1612.
26. Lykke-Andersen K, Gilchrist MJ, Grabarek JB, Das P, Miska E, et al. (2008) Maternal Argonaute 2 is essential for early mouse development at the maternal-zygotic transition. Molecular biology of the cell 19: 4383-4392.
27. Hogan B, Costantini F, Lacy L (1994) Manipulating the mouse embryo- a laboratory manual. Cold Spring Harbor, NY: Second edition, Cold Spring Harbor Laboratory.
28. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. 3 v. p.
29. Olive V, Wagner N, Chan S, Kastner P, Vannetti C, et al. (2007) PU.1 (Sfpi1), a pleiotropic regulator expressed from the first embryonic stages with a crucial function in germinal progenitors. Development 134: 3815-3825.
30. Bocker MT, Tuorto F, Raddatz G, Musch T, Yang FC, et al. (2012) Hydroxylation of 5-methylcytosine by TET2 maintains the active state of the mammalian HOXA cluster. Nature communications 3: 818.
31. Rohde C, Zhang Y, Reinhardt R, Jeltsch A, (2010) BISMA-fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinformatics 11: 230.
32. Schaefer M, Pollex T, Hanna K, Lyko F, (2009) RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res 37: e12.