Chromatin-modifying genetic interventions suppress age-associated transposable element activation and extend life span in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 40, 2016, Pages 11277-11282

  Wood, Jason G ^a   Jones, Brian C ^a   Jiang, Nan ^a   Chang, Chengyi ^a   Hosier, Suzanne ^a   Wickremesinghe, Priyan ^a   Garcia, Meyrolin ^a   Hartnett, Davis A ^a   Burhenn, Lucas ^a   Neretti, Nicola ^a   Helfand, Stephen L ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Aging; Dietary restriction; Heterochromatin; Silencing; Transposable elements

Indexed keywords

DOUBLE STRANDED DNA; LAMIVUDINE; DCR-2 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; RIBONUCLEASE III; RNA HELICASE;

ADAR GENE; ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DICER 2 GENE; DIET RESTRICTION; DNA CONTENT; DOUBLE STRANDED DNA BREAK; DROSOPHILA MELANOGASTER; EPIGENETICS; GENE; GENE LOCATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENOME; HETEROCHROMATIN; LIFESPAN; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; SIR2 GENE; SU(VAR)3 9 GENE; TRANSPOSON; ANIMAL; CALORIC RESTRICTION; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; LONGEVITY; METABOLISM; PHYSIOLOGY; RETROPOSON; UPREGULATION;

ANIMALS; CALORIC RESTRICTION; CHROMATIN; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GENOTYPE; HETEROCHROMATIN; LAMIVUDINE; LONGEVITY; RETROELEMENTS; RIBONUCLEASE III; RNA HELICASES; UP-REGULATION;

EID: 84989845321     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1604621113     Document Type: Article

References (35)

1. Wood JG, Helfand SL (2013) Chromatin structure and transposable elements in organismal aging. Front Genet 4(December):274.
2. Feser J, Tyler J (2011) Chromatin structure as a mediator of aging. FEBS Lett 585(13):2041-2048.
3. Dang W, et al. (2009) Histone H4 lysine 16 acetylation regulates cellular lifespan. Nature 459(7248):802-807.
4. Benayoun BA, Pollina EA, Brunet A (2015) Epigenetic regulation of ageing: Linking environmental inputs to genomic stability. Nat Rev Mol Cell Biol 16(10):593-610.
5. Wood JG, et al. (2010) Chromatin remodeling in the aging genome of Drosophila. Aging Cell 9(6):971-978.
6. Jiang N, et al. (2013) Dietary and genetic effects on age-related loss of gene silencing reveal epigenetic plasticity of chromatin repression during aging. Aging (Albany, NY) 5(11):813-824.
7. De Cecco M, et al. (2013) Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 12(2):247-256.
8. De Cecco M, et al. (2013) Transposable elements become active and mobile in the genomes of aging mammalian somatic tissues. Aging (Albany, NY) 5(12):867-883.
9. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8(4):272-285.
10. Wang J, et al. (2011) Inhibition of activated pericentromeric SINE/Alu repeat transcription in senescent human adult stem cells reinstates self-renewal. Cell Cycle 10(17):3016-3030.
11. Ambati J, Fowler BJ (2012) Mechanisms of age-related macular degeneration. Neuron 75(1):26-39.
12. Van Meter M, et al. (2014) SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age. Nat Commun 5:5011.
13. Dennis S, Sheth U, Feldman JL, English KA, Priess JR (2012) C. elegans germ cells show temperature and age-dependent expression of Cer1, a Gypsy/Ty3-related retrotransposon. PLoS Pathog 8(3):e1002591.
14. Maxwell PH, Burhans WC, Curcio MJ (2011) Retrotransposition is associated with genome instability during chronological aging. Proc Natl Acad Sci USA 108(51):20376-20381.
15. Li W, et al. (2013) Activation of transposable elements during aging and neuronal decline in Drosophila. Nat Neurosci 16(5):529-531.
16. Chen H, Zheng X, Xiao D, Zheng Y (2016) Age-associated de-repression of retrotransposons in the Drosophila fat body, its potential cause and consequence. Aging Cell 15(3):542-552.
17. Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16(2):71-84.
18. Schotta G, et al. (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21(5):1121-1131.
19. Ghildiyal M, Zamore PD (2009) Small silencing RNAs: An expanding universe. Nat Rev Genet 10(2):94-108.
20. Castel SE, Martienssen RA (2013) RNA interference in the nucleus: Roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14(2):100-112.
21. Savva YA, et al. (2013) RNA editing regulates transposon-mediated heterochromatic gene silencing. Nat Commun 4:2745.
22. Rosenberg MI, Parkhurst SM (2002) Drosophila Sir2 is required for heterochromatic silencing and by euchromatic Hairy/E(Spl) bHLH repressors in segmentation and sex determination. Cell 109(4):447-458.
23. Oberdoerffer P, et al. (2008) SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 135(5):907-918.
24. Lim DH, et al. (2011) The endogenous siRNA pathway in Drosophila impacts stress resistance and lifespan by regulating metabolic homeostasis. FEBS Lett 585(19):3079-3085.
25. Whitaker R, et al. (2013) Increased expression of Drosophila Sir2 extends life span in a dose-dependent manner. Aging (Albany, NY) 5(9):682-691.
26. Viswanathan M, Guarente L (2011) Regulation of Caenorhabditis elegans lifespan by sir-2.1 transgenes. Nature 477(7365):E1-E2.
27. Burnett C, et al. (2011) Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477(7365):482-485.
28. Hoffmann J, Romey R, Fink C, Yong L, Roeder T (2013) Overexpression of Sir2 in the adult fat body is sufficient to extend lifespan of male and female Drosophila. Aging (Albany, NY) 5(4):315-327.
29. Riddle NC, et al. (2011) Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res 21(2):147-163.
30. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23:251-287.
31. Dej KJ, Gerasimova T, Corces VG, Boeke JD (1998) A hotspot for the Drosophila gypsy retroelement in the ovo locus. Nucleic Acids Res 26(17):4019-4025.
32. Ghildiyal M, et al. (2008) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320(5879):1077-1081.
33. Criscione SW, Zhang Y, Thompson W, Sedivy JM, Neretti N (2014) Transcriptional landscape of repetitive elements in normal and cancer human cells. BMC Genomics 15(1):583.
34. Boeke J, et al. (2010) Phosphorylation of SU(VAR)3-9 by the chromosomal kinase JIL-1. PLoS One 5(4):e10042.
35. Yang JS, et al. (2011) OASIS: Online application for the survival analysis of lifespan assays performed in aging research. PLoS One 6(8):e23525.