Metabolic Inputs into the Epigenome

Cell Metabolism

Volumn 25, Issue 3, 2017, Pages 544-558

  Sharma, Upasna ^a   Rando, Oliver J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

epigenetics; epigenome; metabolism; transgenerational inheritance

Indexed keywords

CYTOSINE; MICRORNA; CHROMATIN;

CHROMATIN STRUCTURE; DNA METHYLATION; EPIGENETICS; GERMLINE STEM CELL; HUMAN; METABOLIC REGULATION; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN METHYLATION; REVIEW; SOMATIC CELL; ANIMAL; CHROMATIN; GENETICS; GERM CELL; METABOLISM;

ANIMALS; CHROMATIN; DNA METHYLATION; EPIGENOMICS; GERM CELLS; HUMANS; METABOLISM; MICRORNAS;

EID: 85014540321     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2017.02.003     Document Type: Review

References (156)

1. Alarcón, C.R., Goodarzi, H., Lee, H., Liu, X., Tavazoie, S., Tavazoie, S.F., HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA processing events. Cell 162 (2015), 1299–1308.
2. Aldrich, J.C., Maggert, K.A., Transgenerational inheritance of diet-induced genome rearrangements in Drosophila. PLoS Genet., 11, 2015, e1005148.
3. Almer, A., Rudolph, H., Hinnen, A., Hörz, W., Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5 (1986), 2689–2696.
4. Andersen, K.L., Collins, K., Several RNase T2 enzymes function in induced tRNA and rRNA turnover in the ciliate Tetrahymena. Mol. Biol. Cell 23 (2012), 36–44.
5. Anderson, P., Ivanov, P., tRNA fragments in human health and disease. FEBS Lett. 588 (2014), 4297–4304.
6. Aravin, A.A., Chan, D.C., piRNAs meet mitochondria. Dev. Cell 20 (2011), 287–288.
7. Aravin, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K., Hannon, G.J., Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316 (2007), 744–747.
8. Arteaga-Vazquez, M.A., Chandler, V.L., Paramutation in maize: RNA mediated trans-generational gene silencing. Curr. Opin. Genet. Dev. 20 (2010), 156–163.
9. Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
10. Bartolomei, M.S., Ferguson-Smith, A.C., Mammalian genomic imprinting. Cold Spring Harb. Perspect. Biol., 3, 2011, 10.1101/cshperspect.a002592.
11. Batista, P.J., Ruby, J.G., Claycomb, J.M., Chiang, R., Fahlgren, N., Kasschau, K.D., Chaves, D.A., Gu, W., Vasale, J.J., Duan, S., et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 31 (2008), 67–78.
12. Baubec, T., Colombo, D.F., Wirbelauer, C., Schmidt, J., Burger, L., Krebs, A.R., Akalin, A., Schübeler, D., Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520 (2015), 243–247.
13. Beyret, E., Lin, H., Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev. Biol. 355 (2011), 215–226.
14. Blaschke, K., Ebata, K.T., Karimi, M.M., Zepeda-Martínez, J.A., Goyal, P., Mahapatra, S., Tam, A., Laird, D.J., Hirst, M., Rao, A., et al. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature 500 (2013), 222–226.
15. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., Benning, C., AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17 (1998), 170–180.
16. Boke, E., Ruer, M., Wühr, M., Coughlin, M., Lemaitre, R., Gygi, S.P., Alberti, S., Drechsel, D., Hyman, A.A., Mitchison, T.J., Amyloid-like self-assembly of a cellular compartment. Cell 166 (2016), 637–650.
17. Bourc'his, D., Voinnet, O., A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330 (2010), 617–622.
18. Bourc'his, D., Xu, G.L., Lin, C.S., Bollman, B., Bestor, T.H., Dnmt3L and the establishment of maternal genomic imprints. Science 294 (2001), 2536–2539.
19. Brangwynne, C.P., Eckmann, C.R., Courson, D.S., Rybarska, A., Hoege, C., Gharakhani, J., Jülicher, F., Hyman, A.A., Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324 (2009), 1729–1732.
20. Brykczynska, U., Hisano, M., Erkek, S., Ramos, L., Oakeley, E.J., Roloff, T.C., Beisel, C., Schübeler, D., Stadler, M.B., Peters, A.H., Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17 (2010), 679–687.
21. Carey, B.W., Finley, L.W., Cross, J.R., Allis, C.D., Thompson, C.B., Intracellular α-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518 (2015), 413–416.
22. Carone, B.R., Fauquier, L., Habib, N., Shea, J.M., Hart, C.E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P.D., et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143 (2010), 1084–1096.
23. Carone, B.R., Hung, J.H., Hainer, S.J., Chou, M.T., Carone, D.M., Weng, Z., Fazzio, T.G., Rando, O.J., High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm. Dev. Cell 30 (2014), 11–22.
24. Chan, S.W., Zilberman, D., Xie, Z., Johansen, L.K., Carrington, J.C., Jacobsen, S.E., RNA silencing genes control de novo DNA methylation. Science, 303, 2004, 1336.
25. Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G.H., Peng, H., Zhang, X., Zhang, Y., et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351 (2016), 397–400.
26. Chong, S., Vickaryous, N., Ashe, A., Zamudio, N., Youngson, N., Hemley, S., Stopka, T., Skoultchi, A., Matthews, J., Scott, H.S., et al. Modifiers of epigenetic reprogramming show paternal effects in the mouse. Nat. Genet. 39 (2007), 614–622.
27. Chung, T.L., Brena, R.M., Kolle, G., Grimmond, S.M., Berman, B.P., Laird, P.W., Pera, M.F., Wolvetang, E.J., Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells 28 (2010), 1848–1855.
28. Couvillion, M.T., Sachidanandam, R., Collins, K., A growth-essential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev. 24 (2010), 2742–2747.
29. Couvillion, M.T., Bounova, G., Purdom, E., Speed, T.P., Collins, K., A Tetrahymena Piwi bound to mature tRNA 3′ fragments activates the exonuclease Xrn2 for RNA processing in the nucleus. Mol. Cell 48 (2012), 509–520.
30. Czech, B., Hannon, G.J., Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12 (2011), 19–31.
31. Czerwoniec, A., Dunin-Horkawicz, S., Purta, E., Kaminska, K.H., Kasprzak, J.M., Bujnicki, J.M., Grosjean, H., Rother, K., MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res. 37 (2009), D118–D121.
32. Dang, L., White, D.W., Gross, S., Bennett, B.D., Bittinger, M.A., Driggers, E.M., Fantin, V.R., Jang, H.G., Jin, S., Keenan, M.C., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462 (2009), 739–744.
33. Daxinger, L., Whitelaw, E., Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 13 (2012), 153–162.
34. de Castro Barbosa, T., Ingerslev, L.R., Alm, P.S., Versteyhe, S., Massart, J., Rasmussen, M., Donkin, I., Sjögren, R., Mudry, J.M., Vetterli, L., et al. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol. Metab. 5 (2015), 184–197.
35. Deaton, A.M., Bird, A., CpG islands and the regulation of transcription. Genes Dev. 25 (2011), 1010–1022.
36. Donkin, I., Versteyhe, S., Ingerslev, L.R., Qian, K., Mechta, M., Nordkap, L., Mortensen, B., Appel, E.V., Jørgensen, N., Kristiansen, V.B., et al. Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans. Cell Metab. 23 (2016), 369–378.
37. El Yacoubi, B., Bailly, M., de Crécy-Lagard, V., Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu. Rev. Genet. 46 (2012), 69–95.
38. Elbarbary, R.A., Takaku, H., Uchiumi, N., Tamiya, H., Abe, M., Takahashi, M., Nishida, H., Nashimoto, M., Modulation of gene expression by human cytosolic tRNase Z(L) through 5′-half-tRNA. PLoS ONE, 4, 2009, e5908.
39. Esteban, M.A., Wang, T., Qin, B., Yang, J., Qin, D., Cai, J., Li, W., Weng, Z., Chen, J., Ni, S., et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6 (2010), 71–79.
40. Etchegaray, J.P., Mostoslavsky, R., Interplay between metabolism and epigenetics: a nuclear adaptation to environmental changes. Mol. Cell 62 (2016), 695–711.
41. Forneris, F., Binda, C., Vanoni, M.A., Mattevi, A., Battaglioli, E., Histone demethylation catalysed by LSD1 is a flavin-dependent oxidative process. FEBS Lett. 579 (2005), 2203–2207.
42. Fu, H., Feng, J., Liu, Q., Sun, F., Tie, Y., Zhu, J., Xing, R., Sun, Z., Zheng, X., Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett. 583 (2009), 437–442.
43. Fullston, T., Ohlsson Teague, E.M., Palmer, N.O., DeBlasio, M.J., Mitchell, M., Corbett, M., Print, C.G., Owens, J.A., Lane, M., Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 27 (2013), 4226–4243.
44. Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., Mansuy, I.M., Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17 (2014), 667–669.
45. Gassmann, R., Rechtsteiner, A., Yuen, K.W., 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 484 (2012), 534–537.
46. Gaydos, L.J., Wang, W., Strome, S., Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 345 (2014), 1515–1518.
47. Ghildiyal, M., Zamore, P.D., Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10 (2009), 94–108.
48. Gibbons, J.G., Branco, A.T., Yu, S., Lemos, B., Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat. Commun., 5, 2014, 4850.
49. Goodarzi, H., Liu, X., Nguyen, H.C., Zhang, S., Fish, L., Tavazoie, S.F., Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 161 (2015), 790–802.
50. Grandjean, V., Fourré, S., De Abreu, D.A., Derieppe, M.A., Remy, J.J., Rassoulzadegan, M., RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep., 5, 2015, 18193.
51. Greer, E.L., Maures, T.J., Ucar, D., Hauswirth, A.G., Mancini, E., Lim, J.P., Benayoun, B.A., Shi, Y., Brunet, A., Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479 (2011), 365–371.
52. Gu, W., Lee, H.C., Chaves, D., Youngman, E.M., Pazour, G.J., Conte, D. Jr., Mello, C.C., CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 151 (2012), 1488–1500.
53. Guan, H., Liu, C., Chen, Z., Wang, L., Li, C., Zhao, J., Yu, Y., Zhang, P., Chen, W., Jiang, A., 1,25-Dihydroxyvitamin D3 up-regulates expression of hsa-let-7a-2 through the interaction of VDR/VDRE in human lung cancer A549 cells. Gene 522 (2013), 142–146.
54. Hackett, J.A., Surani, M.A., DNA methylation dynamics during the mammalian life cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 2013, 20110328.
55. Hammoud, S.S., Nix, D.A., Zhang, H., Purwar, J., Carrell, D.T., Cairns, B.R., Distinctive chromatin in human sperm packages genes for embryo development. Nature 460 (2009), 473–478.
56. Hammoud, S.S., Low, D.H., Yi, C., Carrell, D.T., Guccione, E., Cairns, B.R., Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell 15 (2014), 239–253.
57. Handler, D., Meixner, K., Pizka, M., Lauss, K., Schmied, C., Gruber, F.S., Brennecke, J., The genetic makeup of the Drosophila piRNA pathway. Mol. Cell 50 (2013), 762–777.
58. Heard, E., Martienssen, R.A., Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157 (2014), 95–109.
59. Hino, S., Sakamoto, A., Nagaoka, K., Anan, K., Wang, Y., Mimasu, S., Umehara, T., Yokoyama, S., Kosai, K., Nakao, M., FAD-dependent lysine-specific demethylase-1 regulates cellular energy expenditure. Nat. Commun., 3, 2012, 758.
60. Hoagland, M.B., Stephenson, M.L., Scott, J.F., Hecht, L.I., Zamecnik, P.C., A soluble ribonucleic acid intermediate in protein synthesis. J. Biol. Chem. 231 (1958), 241–257.
61. Holland, M.L., Lowe, R., Caton, P.W., Gemma, C., Carbajosa, G., Danson, A.F., Carpenter, A.A., Loche, E., Ozanne, S.E., Rakyan, V.K., Early-life nutrition modulates the epigenetic state of specific rDNA genetic variants in mice. Science 353 (2016), 495–498.
62. Hsieh, L.C., Lin, S.I., Shih, A.C., Chen, J.W., Lin, W.Y., Tseng, C.Y., Li, W.H., Chiou, T.J., Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151 (2009), 2120–2132.
63. Huang, H., Gao, Q., Peng, X., Choi, S.Y., Sarma, K., Ren, H., Morris, A.J., Frohman, M.A., piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev. Cell 20 (2011), 376–387.
64. Hughes, A.L., Rando, O.J., Mechanisms underlying nucleosome positioning in vivo. Annu. Rev. Biophys. 43 (2014), 41–63.
65. Hutvágner, G., McLachlan, J., Pasquinelli, A.E., Bálint, E., Tuschl, T., Zamore, P.D., A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293 (2001), 834–838.
66. Huypens, P., Sass, S., Wu, M., Dyckhoff, D., Tschöp, M., Theis, F., Marschall, S., Hrabě de Angelis, M., Beckers, J., Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nat. Genet. 48 (2016), 497–499.
67. Inoue, A., Zhang, Y., Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science, 334, 2011, 194.
68. Iqbal, K., Jin, S.G., Pfeifer, G.P., Szabó, P.E., Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc. Natl. Acad. Sci. USA 108 (2011), 3642–3647.
69. Ivanov, P., Emara, M.M., Villen, J., Gygi, S.P., Anderson, P., Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 43 (2011), 613–623.
70. Jacobsen, S.E., Meyerowitz, E.M., Hypermethylated SUPERMAN epigenetic alleles in arabidopsis. Science 277 (1997), 1100–1103.
71. Janke, R., Dodson, A.E., Rine, J., Metabolism and epigenetics. Annu. Rev. Cell Dev. Biol. 31 (2015), 473–496.
72. Jarosz, D.F., Brown, J.C., Walker, G.A., Datta, M.S., Ung, W.L., Lancaster, A.K., Rotem, A., Chang, A., Newby, G.A., Weitz, D.A., et al. Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158 (2014), 1083–1093.
73. Jobson, M.A., Jordan, J.M., Sandrof, M.A., Hibshman, J.D., Lennox, A.L., Baugh, L.R., Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans. Genetics 201 (2015), 201–212.
74. Johnston, D.S., Jelinsky, S.A., Bang, H.J., DiCandeloro, P., Wilson, E., Kopf, G.S., Turner, T.T., The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol. Reprod. 73 (2005), 404–413.
75. Jones, P.A., DNA methylation errors and cancer. Cancer Res. 56 (1996), 2463–2467.
76. Jordan, S.D., Krüger, M., Willmes, D.M., Redemann, N., Wunderlich, F.T., Brönneke, H.S., Merkwirth, C., Kashkar, H., Olkkonen, V.M., Böttger, T., et al. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 13 (2011), 434–446.
77. Judson, R.L., Babiarz, J.E., Venere, M., Blelloch, R., Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat. Biotechnol. 27 (2009), 459–461.
78. Katan-Khaykovich, Y., Struhl, K., Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors. Genes Dev. 16 (2002), 743–752.
79. Katz, D.J., Edwards, T.M., Reinke, V., Kelly, W.G., A C. elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory. Cell 137 (2009), 308–320.
80. Kaufmann, G., Anticodon nucleases. Trends Biochem. Sci. 25 (2000), 70–74.
81. Keam, S.P., Hutvagner, G., tRNA-derived fragments (tRFs): emerging new roles for an ancient RNA in the regulation of gene expression. Life (Basel) 5 (2015), 1638–1651.
82. Kirino, Y., Kim, N., de Planell-Saguer, M., Khandros, E., Chiorean, S., Klein, P.S., Rigoutsos, I., Jongens, T.A., Mourelatos, Z., Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat. Cell Biol. 11 (2009), 652–658.
83. Klattenhoff, C., Xi, H., Li, C., Lee, S., Xu, J., Khurana, J.S., Zhang, F., Schultz, N., Koppetsch, B.S., Nowosielska, A., et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138 (2009), 1137–1149.
84. Kornberg, R.D., Lorch, Y., Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98 (1999), 285–294.
85. Kumar, P., Kuscu, C., Dutta, A., Biogenesis and function of transfer RNA-related fragments (tRFs). Trends Biochem. Sci. 41 (2016), 679–689.
86. Kustatscher, G., Hothorn, M., Pugieux, C., Scheffzek, K., Ladurner, A.G., Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12 (2005), 624–625.
87. Law, J.A., Jacobsen, S.E., Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11 (2010), 204–220.
88. Laxman, S., Sutter, B.M., Wu, X., Kumar, S., Guo, X., Trudgian, D.C., Mirzaei, H., Tu, B.P., Sulfur amino acids regulate translational capacity and metabolic homeostasis through modulation of tRNA thiolation. Cell 154 (2013), 416–429.
89. Lee, S.R., Collins, K., Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J. Biol. Chem. 280 (2005), 42744–42749.
90. Lee, R.C., Feinbaum, R.L., Ambros, V., The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 (1993), 843–854.
91. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S., Kim, V.N., The nuclear RNase III Drosha initiates microRNA processing. Nature 425 (2003), 415–419.
92. Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H., Kim, V.N., MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23 (2004), 4051–4060.
93. Lee, Y.S., Shibata, Y., Malhotra, A., Dutta, A., A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 23 (2009), 2639–2649.
94. Lewis, E.B., A gene complex controlling segmentation in Drosophila. Nature 276 (1978), 565–570.
95. Li, E., Bestor, T.H., Jaenisch, R., Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69 (1992), 915–926.
96. Li, B., Carey, M., Workman, J.L., The role of chromatin during transcription. Cell 128 (2007), 707–719.
97. Li, X.Z., Roy, C.K., Dong, X., Bolcun-Filas, E., Wang, J., Han, B.W., Xu, J., Moore, M.J., Schimenti, J.C., Weng, Z., Zamore, P.D., An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol. Cell 50 (2013), 67–81.
98. Lin, S.J., Defossez, P.A., Guarente, L., Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289 (2000), 2126–2128.
99. Liou, G.G., Tanny, J.C., Kruger, R.G., Walz, T., Moazed, D., Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation. Cell 121 (2005), 515–527.
100. Lo, W.S., Trievel, R.C., Rojas, J.R., Duggan, L., Hsu, J.Y., Allis, C.D., Marmorstein, R., Berger, S.L., Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5 (2000), 917–926.
101. Mendenhall, E.M., Koche, R.P., Truong, T., Zhou, V.W., Issac, B., Chi, A.S., Ku, M., Bernstein, B.E., GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet., 6, 2010, e1001244.
102. Mitchell, M., Bakos, H.W., Lane, M., Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95 (2011), 1349–1353.
103. Okano, M., Bell, D.W., Haber, D.A., Li, E., DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99 (1999), 247–257.
104. Olivieri, D., Sykora, M.M., Sachidanandam, R., Mechtler, K., Brennecke, J., An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 29 (2010), 3301–3317.
105. Ooi, S.K., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument-Bromage, H., Tempst, P., Lin, S.P., Allis, C.D., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448 (2007), 714–717.
106. Öst, A., Lempradl, A., Casas, E., Weigert, M., Tiko, T., Deniz, M., Pantano, L., Boenisch, U., Itskov, P.M., Stoeckius, M., et al. Paternal diet defines offspring chromatin state and intergenerational obesity. Cell 159 (2014), 1352–1364.
107. Padmanabhan, N., Jia, D., Geary-Joo, C., Wu, X., Ferguson-Smith, A.C., Fung, E., Bieda, M.C., Snyder, F.F., Gravel, R.A., Cross, J.C., Watson, E.D., Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 155 (2013), 81–93.
108. Peng, H., Shi, J., Zhang, Y., Zhang, H., Liao, S., Li, W., Lei, L., Han, C., Ning, L., Cao, Y., et al. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res. 22 (2012), 1609–1612.
109. Phizicky, E.M., Hopper, A.K., tRNA processing, modification, and subcellular dynamics: past, present, and future. RNA 21 (2015), 483–485.
110. Ptashne, M., On the use of the word “epigenetic”. Curr. Biol. 17 (2007), R233–R236.
111. Radford, E.J., Ito, M., Shi, H., Corish, J.A., Yamazawa, K., Isganaitis, E., Seisenberger, S., Hore, T.A., Reik, W., Erkek, S., et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science, 345, 2014, 1255903.
112. Radman-Livaja, M., Liu, C.L., Friedman, N., Schreiber, S.L., Rando, O.J., Replication and active demethylation represent partially overlapping mechanisms for erasure of H3K4me3 in budding yeast. PLoS Genet., 6, 2010, e1000837.
113. Rando, O.J., Simmons, R.A., I'm eating for two: parental dietary effects on offspring metabolism. Cell 161 (2015), 93–105.
114. Rando, O.J., Verstrepen, K.J., Timescales of genetic and epigenetic inheritance. Cell 128 (2007), 655–668.
115. Rando, O.J., Winston, F., Chromatin and transcription in yeast. Genetics 190 (2012), 351–387.
116. Rechavi, O., Houri-Ze'evi, L., Anava, S., Goh, W.S., Kerk, S.Y., Hannon, G.J., Hobert, O., Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158 (2014), 277–287.
117. Rinaudo, P., Wang, E., Fetal programming and metabolic syndrome. Annu. Rev. Physiol. 74 (2012), 107–130.
118. Ringrose, L., Paro, R., Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38 (2004), 413–443.
119. Rodgers, A.B., Morgan, C.P., Leu, N.A., Bale, T.L., Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. USA 112 (2015), 13699–13704.
120. Saikia, M., Jobava, R., Parisien, M., Putnam, A., Krokowski, D., Gao, X.H., Guan, B.J., Yuan, Y., Jankowsky, E., Feng, Z., et al. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol. Cell. Biol. 34 (2014), 2450–2463.
121. Saito, K., Ishizu, H., Komai, M., Kotani, H., Kawamura, Y., Nishida, K.M., Siomi, H., Siomi, M.C., Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 24 (2010), 2493–2498.
122. Schaefer, M., Pollex, T., Hanna, K., Tuorto, F., Meusburger, M., Helm, M., Lyko, F., RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev. 24 (2010), 1590–1595.
123. Serio, T.R., Lindquist, S.L., [PSI+]: an epigenetic modulator of translation termination efficiency. Annu. Rev. Cell Dev. Biol. 15 (1999), 661–703.
124. Sharma, U., Conine, C.C., Shea, J.M., Boskovic, A., Derr, A.G., Bing, X.Y., Belleannee, C., Kucukural, A., Serra, R.W., Sun, F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351 (2016), 391–396.
125. Shea, J.M., Serra, R.W., Carone, B.R., Shulha, H.P., Kucukural, A., Ziller, M.J., Vallaster, M.P., Gu, H., Tapper, A.R., Gardner, P.D., et al. Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev. Cell 35 (2015), 750–758.
126. Siklenka, K., Erkek, S., Godmann, M., Lambrot, R., McGraw, S., Lafleur, C., Cohen, T., Xia, J., Suderman, M., Hallett, M., et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science, 350, 2015, aab2006.
127. Siomi, H., Siomi, M.C., Posttranscriptional regulation of microRNA biogenesis in animals. Mol. Cell 38 (2010), 323–332.
128. Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzić, M., Becker, J.D., Feijó, J.A., Martienssen, R.A., Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136 (2009), 461–472.
129. Smith, J.S., Brachmann, C.B., Celic, I., Kenna, M.A., Muhammad, S., Starai, V.J., Avalos, J.L., Escalante-Semerena, J.C., Grubmeyer, C., Wolberger, C., Boeke, J.D., A phylogenetically conserved NAD+-dependent protein deacetylase activity in the Sir2 protein family. Proc. Natl. Acad. Sci. USA 97 (2000), 6658–6663.
130. Sobala, A., Hutvagner, G., Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdiscip. Rev. RNA 2 (2011), 853–862.
131. Sobala, A., Hutvagner, G., Small RNAs derived from the 5′ end of tRNA can inhibit protein translation in human cells. RNA Biol. 10 (2013), 553–563.
132. Stadler, M.B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Schöler, A., van Nimwegen, E., Wirbelauer, C., Oakeley, E.J., Gaidatzis, D., et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480 (2011), 490–495.
133. Starlard-Davenport, A., Tryndyak, V., Kosyk, O., Ross, S.R., Rusyn, I., Beland, F.A., Pogribny, I.P., Dietary methyl deficiency, microRNA expression and susceptibility to liver carcinogenesis. J. Nutrigenet. Nutrigenomics 3 (2010), 259–266.
134. Su, X., Wellen, K.E., Rabinowitz, J.D., Metabolic control of methylation and acetylation. Curr. Opin. Chem. Biol. 30 (2016), 52–60.
135. Tan, M., Luo, H., Lee, S., Jin, F., Yang, J.S., Montellier, E., Buchou, T., Cheng, Z., Rousseaux, S., Rajagopal, N., et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146 (2011), 1016–1028.
136. Tang, W.W., Kobayashi, T., Irie, N., Dietmann, S., Surani, M.A., Specification and epigenetic programming of the human germ line. Nat. Rev. Genet. 17 (2016), 585–600.
137. Tanner, K.G., Landry, J., Sternglanz, R., Denu, J.M., Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc. Natl. Acad. Sci. USA 97 (2000), 14178–14182.
138. Thompson, D.M., Lu, C., Green, P.J., Parker, R., tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14 (2008), 2095–2103.
139. Tsai, C.C., Su, P.F., Huang, Y.F., Yew, T.L., Hung, S.C., Oct4 and Nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cells. Mol. Cell 47 (2012), 169–182.
140. Tuorto, F., Liebers, R., Musch, T., Schaefer, M., Hofmann, S., Kellner, S., Frye, M., Helm, M., Stoecklin, G., Lyko, F., RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat. Struct. Mol. Biol. 19 (2012), 900–905.
141. van der Knaap, J.A., Verrijzer, C.P., Undercover: gene control by metabolites and metabolic enzymes. Genes Dev. 30 (2016), 2345–2369.
142. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., Martienssen, R.A., Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297 (2002), 1833–1837.
143. von Horsten, H.H., Johnson, S.S., SanFrancisco, S.K., Hastert, M.C., Whelly, S.M., Cornwall, G.A., Oligomerization and transglutaminase cross-linking of the cystatin CRES in the mouse epididymal lumen: potential mechanism of extracellular quality control. J. Biol. Chem. 282 (2007), 32912–32923.
144. 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 20 (2011), 364–375.
145. Waterland, R.A., Jirtle, R.L., Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23 (2003), 5293–5300.
146. Waterland, R.A., Lin, J.R., Smith, C.A., Jirtle, R.L., Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum. Mol. Genet. 15 (2006), 705–716.
147. Wei, Y., Yang, C.R., Wei, Y.P., Zhao, Z.A., Hou, Y., Schatten, H., Sun, Q.Y., Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc. Natl. Acad. Sci. USA 111 (2014), 1873–1878.
148. Weigel, D., Colot, V., Epialleles in plant evolution. Genome Biol., 13, 2012, 249.
149. Wickner, R.B., [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264 (1994), 566–569.
150. Wu, H., Zhang, Y., Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156 (2014), 45–68.
151. Yamasaki, S., Ivanov, P., Hu, G.F., Anderson, P., Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 185 (2009), 35–42.
152. Yang, Q., Liang, X., Sun, X., Zhang, L., Fu, X., Rogers, C.J., Berim, A., Zhang, S., Wang, S., Wang, B., et al. AMPK/α-ketoglutarate axis dynamically mediates DNA demethylation in the Prdm16 promoter and brown adipogenesis. Cell Metab. 24 (2016), 542–554.
153. Ye, P., Liu, Y., Chen, C., Tang, F., Wu, Q., Wang, X., Liu, C.G., Liu, X., Liu, R., Liu, Y., Zheng, P., An mTORC1-Mdm2-Drosha axis for miRNA biogenesis in response to glucose- and amino acid-deprivation. Mol. Cell 57 (2015), 708–720.
154. Yoo, A.S., Sun, A.X., Li, L., Shcheglovitov, A., Portmann, T., Li, Y., Lee-Messer, C., Dolmetsch, R.E., Tsien, R.W., Crabtree, G.R., MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476 (2011), 228–231.
155. Young, J.I., Züchner, S., Wang, G., Regulation of the epigenome by vitamin C. Annu. Rev. Nutr. 35 (2015), 545–564.
156. Zeybel, M., Hardy, T., Wong, Y.K., Mathers, J.C., Fox, C.R., Gackowska, A., Oakley, F., Burt, A.D., Wilson, C.L., Anstee, Q.M., et al. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat. Med. 18 (2012), 1369–1377.