1,526
Views
58
CrossRef citations to date
0
Altmetric
Review Article

From Waddington’s epigenetic landscape to small noncoding RNA: some important milestones in the history of epigenetics research

Pages 252-274 | Published online: 16 Apr 2011

References

  • Aapola U, Kawasaki K, Scott HS, Ollila J, Vihinen M, Heino M, Shintani A, Kawasaki K, Minoshima S, Krohn K, Antonarakis SE, Shimizu N, Kudoh J, Peterson P. 2000. Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics 65:293–298.
  • Aapola U, Lyle R, Krohn K, Antonarakis SE, Peterson P. 2001. Isolation and initial characterization of the mouse Dnmt3l gene. Cytogenet Cell Genet 92:122–126.
  • Allfrey VG, Faulkner R, Mirsky AE. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51:786–794.
  • Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T. 2003. A uniform system for microRNA annotation. RNA 9:277–279.
  • Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA. 2001. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11:1017–1027.
  • Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T. 2003. The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350.
  • Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207.
  • Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124.
  • Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N. 1991. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349:84–87.
  • Bartolomei MS, Zemel S, Tilghman SM. 1991. Parental imprinting of the mouse H19 gene. Nature 351:153–155.
  • Barton SC, Surani MA, Norris ML. 1984. Role of paternal and maternal genomes in mouse development. Nature 311:374–376.
  • Bell AC, Felsenfeld G. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–485.
  • Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366.
  • Berry RJ, Searle AG. 1963. Epigenetic polymorphism of the rodent skeleton. Proc Zool Soc. Lond 140:577–615.
  • Carolineberry A, Berry RJ. 1967. Epigenetic variation in the human cranium. J Anat 101:361–379.
  • Bestor TH, Ingram VM. 1983. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc Natl Acad Sci USA 80:5559–5563.
  • Bestor TH, Ingram VM. 1985. Growth-dependent expression of multiple species of DNA methyltransferase in murine erythroleukemia cells. Proc Natl Acad Sci USA 82:2674–2678.
  • Bestor T, Laudano A, Mattaliano R, Ingram V. 1988. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 203:971–983.
  • Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539.
  • Bohnsack MT, Czaplinski K, Gorlich D. 2004. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10:185–191.
  • Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103.
  • Brink RA. 1958. Paramutation at the R locus in maize. Cold Spring Harb Symp Quant Biol 23:379–391.
  • Brownell JE, Allis CD. 1995. An activity gel assay detects a single, catalytically active histone acetyltransferase subunit in Tetrahymena macronuclei. Proc Natl Acad Sci USA 92:6364–6368.
  • Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843–851.
  • Cattanach BM, Kirk M. 1985. Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315:496–498.
  • Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. 2010. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465:584–589.
  • Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, Aswad DW, Stallcup MR. 1999. Regulation of transcription by a protein methyltransferase. Science 284:2174–2177.
  • Cheung P, Tanner KG, Cheung WL, Sassone-Corsi P, Denu JM, Allis CD. 2000. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell 5:905–915.
  • Choudhuri S. 2009. Lesser known relatives of miRNA. Biochem Biophys Res Commun 388:177–180.
  • Choudhuri S. 2010. Small noncoding RNAs: biogenesis, function, and emerging significance in toxicology. J Biochem Mol Toxicol 24:195–216.
  • Choudhuri S, Cui Y, Klaassen CD. 2010. Molecular targets of epigenetic regulation and effectors of environmental influences. Toxicol Appl Pharmacol 245:378–393.
  • Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. 2010. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328:1694–1698.
  • Czermin B, Schotta G, Hülsmann BB, Brehm A, Becker PB, Reuter G, Imhof A. 2001. Physical and functional association of SU(VAR)3-9 and HDAC1 in Drosophila. EMBO Rep 2:915–919.
  • Davie JR, Murphy LC. 1990. Level of ubiquitinated histone H2B in chromatin is coupled to ongoing transcription. Biochemistry 29:4752–4757.
  • Davie JR, Murphy LC. 1994. Inhibition of transcription selectively reduces the level of ubiquitinated histone H2B in chromatin. Biochem Biophys Res Commun 203:344–350.
  • Dawson MA, Bannister AJ, Göttgens B, Foster SD, Bartke T, Green AR, Kouzarides T. 2009. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461:819–822.
  • DeChiara TM, Robertson EJ, Efstratiadis A. 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–859.
  • Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432:231–235.
  • Djikeng A, Shi H, Tschudi C, Ullu E. 2001. RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA 7:1522–1530.
  • Doskocil J, Šorm F. 1962. Distribution of 5-methylcytosine in pyrimidine sequences of deoxyribonucleic acids. Biochim Biophys Acta 55:953–959.
  • Dover J, Schneider J, Tawiah-Boateng MA, Wood A, Dean K, Johnston M, Shilatifard A. 2002. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 277:28368–28371.
  • Durrin LK, Mann RK, Kayne PS, Grunstein M. 1991. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell 65:1023–1031.
  • Efstratiadis A. 1994. Parental imprinting of autosomal mammalian genes. Curr Opin Genet Dev 4:265–280.
  • Elbashir SM, Lendeckel W, Tuschl T. 2001a. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188–200.
  • Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001b. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494–498.
  • Ender C, Krek A, Friedländer MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G. 2008. A human snoRNA with microRNA-like functions. Mol Cell 32:519–528.
  • Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS. 2003. MicroRNA targets in Drosophila. Genome Biol 5:R1.
  • Ephrussi B. 1958. The cytoplasm and somatic cell variation. J Cell Physiol Suppl 52:35–49; discussion 49.
  • Feinberg AP, Vogelstein B. 1983a. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301:89–92.
  • Feinberg AP, Vogelstein B. 1983b. Hypomethylation of ras oncogenes in primary human cancers. Biochem Biophys Res Commun 111:47–54.
  • Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y. 2002. Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 12:1052–1058.
  • Ferguson-Smith AC, Cattanach BM, Barton SC, Beechey CV, Surani MA. 1991. Embryological and molecular investigations of parental imprinting on mouse chromosome 7. Nature 351:667–670.
  • Ferguson-Smith AC, Sasaki H, Cattanach BM, Surani MA. 1993. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 362:751–755.
  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811.
  • Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. USA 80:1579–1583.
  • Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. 2003. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278:4035–4040.
  • Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442:199–202.
  • Goldknopf IL, Taylor CW, Baum RM, Yeoman LC, Olson MO, Prestayko AW, Busch H. 1975. Isolation and characterization of protein A24, a “histone-like” non-histone chromosomal protein. J Biol Chem 250:7182–7187.
  • Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. 2004. The Microprocessor complex mediates the genesis of microRNAs. Nature 432:235–240.
  • Griffiths-Jones S. 2004. The microRNA Registry. Nucleic Acids Res 32:D109–D111.
  • Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, Ha I, Baillie DL, Fire A, Ruvkun G, Mello CC. 2001. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106:23–34.
  • Grivna ST, Beyret E, Wang Z, Lin H. 2006. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20:1709–1714.
  • Gold JD, Pedersen RA. 1994. Mechanisms of genomic imprinting in mammals. Curr Top Dev Biol 29:227–280.
  • Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH. 2006. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311:395–398.
  • Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M. 1999. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 274:25543–25549.
  • Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. 2007. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315:1587–1590.
  • Gurley LR, Walters RA, Tobey RA. 1974. Cell cycle-specific changes in histone phosphorylation associated with cell proliferation and chromosome condensation. J Cell Biol 60:356–364.
  • Gurley LR, D’Anna JA, Barham SS, Deaven LL, Tobey RA. 1978. Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur J Biochem 84:1–15.
  • Haig D. 2004. The (dual) origin of epigenetics. Cold Spring Harb Symp Quant Biol 69:67–70.
  • Hamilton AJ, Baulcombe DC. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952.
  • Hammond SM, Bernstein E, Beach D, Hannon GJ. 2000. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296.
  • Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. 2004. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18:3016–3027.
  • Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT, Kim VN. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125:887–901.
  • Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–489.
  • Hata K, Okano M, Lei H, Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983–1993.
  • Hayatsu H, Wataya Y, Kazushige K. 1970. The addition of sodium bisulfite to uracil and to cytosine. J Am Chem Soc 92:724–726.
  • Hebbes TR, Thorne AW, Crane-Robinson C. 1988. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7:1395–1402.
  • Hebbes TR, Thorne AW, Clayton AL, Crane-Robinson C. 1992. Histone acetylation and globin gene switching. Nucleic Acids Res 20:1017–1022.
  • Hendrich B, Bird A. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18:6538–6547.
  • Holliday R. 1979. A new theory of carcinogenesis. Br J Cancer 40:513–522.
  • Holliday R, Pugh JE. 1975. DNA modification mechanisms and gene activity during development. Science 187:226–232.
  • Hotchkiss RD. 1948. The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J Biol Chem 175:315–332.
  • Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293:834–838.
  • Huxley J. 1956. Book review: Principles of Embryology by Prof. C.H. Waddington. Nature 177:807–809.
  • Isenberg I. 1979. Histones. Annu Rev Biochem 48:159–191.
  • Johnson TB, Coghill RD. 1925. Researches on pyrimidines. C111. The discovery of 5-methylcytosine in tuberculinic acid, the nucleic acid of the tubercle bacillus. J Am Chem Soc 47:2838–2844.
  • Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, Ohlsson R, Lobanenkov VV. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 10:853–856.
  • Kangaspeska S, Stride B, Métivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G. 2008. Transient cyclical methylation of promoter DNA. Nature 452:112–115.
  • Kayne PS, Kim UJ, Han M, Mullen JR, Yoshizaki F, Grunstein M. 1988. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell 55:27–39.
  • Khvorova A, Reynolds A, Jayasena SD. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115:209–216.
  • Kim J, Guermah M, McGinty RK, Lee JS, Tang Z, Milne TA, Shilatifard A, Muir TW, Roeder RG. 2009. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137:459–471.
  • Kleff S, Andrulis ED, Anderson CW, Sternglanz R. 1995. Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270:24674–24677.
  • Kornberg RD. 1974. Chromatin structure: a repeating unit of histones and DNA. Science 184:868–871.
  • Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120.
  • Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294:853–858.
  • Landthaler M, Yalcin A, Tuschl T. 2004. The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 14:2162–2167.
  • Lau NC, Lim LP, Weinstein EG, Bartel DP. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862.
  • Lee RC, Feinbaum RL, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854.
  • Lee RC, Ambros V. 2001. An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864.
  • Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419.
  • Lei H, Oh SP, Okano M, Jüttermann R, Goss KA, Jaenisch R, Li E. 1996. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122:3195–3205.
  • Lewis EB. 1954. The theory and application of a new method of detecting chromosomal rearrangements in Drosophila melanogaster. Am Nat 88:225–239.
  • Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A. 1992. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69:905–914.
  • Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. 2003. Prediction of mammalian microRNA targets. Cell 115:787–798.
  • Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20.
  • Li E, Bestor TH, Jaenisch R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926.
  • Li C, Vagin VV, Lee S, Xu J, Ma S, Xi H, Seitz H, Horwich MD, Syrzycka M, Honda BM, Kittler EL, Zapp ML, Klattenhoff C, Schulz N, Theurkauf WE, Weng Z, Zamore PD. 2009. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137:509–521.
  • Liang G, Lin JC, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA, Jones PA. 2004. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci USA 101:7357–7362.
  • Lin WJ, Gary JD, Yang MC, Clarke S, Herschman HR. 1996. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem 271:15034–15044.
  • Lo WS, Trievel RC, Rojas JR, Duggan L, Hsu JY, Allis CD, Marmorstein R, Berger SL. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell 5:917–926.
  • Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. 2004. Nuclear export of microRNA precursors. Science 303:95–98.
  • Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373.
  • Mahadevan LC, Willis AC, Barratt MJ. 1991. Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65:775–783.
  • Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137:522–535.
  • Markert CL. 1968. Neoplasia: a disease of cell differentiation. Cancer Res 28:1908–1914.
  • McGrath J, Solter D. 1984. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183.
  • Meehan RR, Lewis JD, McKay S, Kleiner EL, Bird AP. 1989. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 58:499–507.
  • Meehan RR, Lewis JD, Bird AP. 1992. Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA. Nucleic Acids Res 20:5085–5092.
  • Métivier R, Gallais R, Tiffoche C, Le Péron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G. 2008. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452:45–50.
  • Monk M. 1988. Genomic imprinting. Genes Dev 2:921–925.
  • Murray K. 1964. The occurrence of epsilon-N-methyl lysine in histones. Biochemistry 3:10–15.
  • Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110–113.
  • Nan X, Meehan RR, Bird A. 1993. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res 21:4886–4892.
  • Nan X, Campoy FJ, Bird A. 1997. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471–481.
  • Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389.
  • Nanney DL. 1958. Epigenetic control systems. Proc Natl Acad Sci USA 44:712–717.
  • Napoli C, Lemieux C, Jorgensen R. 1990. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. Plant Cell 2:279–289.
  • Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O’Carroll D, Firestein R, Cleary M, Jenuwein T, Herrera RE, Kouzarides T. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561–565.
  • Nickel BE, Davie JR. 1989. Structure of polyubiquitinated histone H2A. Biochemistry 28:964–968.
  • Nickel BE, Allis CD, Davie JR. 1989. Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. Biochemistry 28:958–963.
  • Okano M, Xie S, Li E. 1998a. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19:219–220.
  • Okano M, Xie S, Li E. 1998b. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 26:2536–2540.
  • Okano M, Bell DW, Haber DA, Li E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257.
  • Paik WK, Kim S. 1967. ϵ- N-Dimethyllysine in histones. Biochem. Biophys. Res. Commun. 27:479–483.
  • Paik WK, Kim S. 1971. Protein methylation. Science 174:114–119.
  • Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G. 2000. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86–89.
  • Paulson JR, Taylor SS. 1982. Phosphorylation of histones 1 and 3 and nonhistone high mobility group 14 by an endogenous kinase in HeLa metaphase chromosomes. J Biol Chem 257:6064–6072.
  • Preuss U, Landsberg G, Scheidtmann KH. 2003. Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res 31:878–885.
  • Queitsch C, Sangster TA, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624.
  • Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599.
  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906.
  • Riggs AD. 1975. X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet 14:9–25.
  • Riggs MG, Whittaker RG, Neumann JR, Ingram VM. 1977. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 268:462–464.
  • Riggs AD, Martienssen RA, Russo VEA. 1996. Introduction. In: Russo VEA et al. (eds) Epigenetic Mechanisms of Gene Regulation. CSHL Press, Cold Spring Harbor, NY, pp. 1–4.
  • Ruby JG, Jan CH, Bartel DP. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86.
  • Rutherford SL, Lindquist S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336–342.
  • Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419:407–411.
  • Saraiya AA, Wang CC. 2008. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4:e1000224.
  • Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6:73–77.
  • Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208.
  • ShapiroR Servis, RE, Welcher M. 1970. Reactions of uracil and cytosine derivatives with sodium bisulfite. A specific deamination method. J Am Chem Soc 92:422–424.
  • Shiio Y, Eisenman RN. 2003. Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100:13225–13230.
  • Slack JM. 2002. Conrad Hal Waddington: the last Renaissance biologist? Nat Rev Genet 3:889–895.
  • Stark A, Brennecke J, Russell RB, Cohen SM. 2003. Identification of Drosophila MicroRNA targets. PLoS Biol 1:E60.
  • Strahl BD, Ohba R, Cook RG, Allis CD. 1999. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci USA 96:14967–14972.
  • Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403:41–45.
  • Surani MA, Barton SC, Norris ML. 1984. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550.
  • Taunton J, Hassig CA, Schreiber SL. 1996. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408–411.
  • Thorne AW, Sautiere P, Briand G, Crane-Robinson C. 1987. The structure of ubiquitinated histone H2B. EMBO J 6:1005–1010.
  • Thorvaldsen JL, Duran KL, Bartolomei MS. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev 12:3693–3702.
  • Turner BM. 2000. Histone acetylation and an epigenetic code. Bioessays 22:836–845.
  • Vakoc CR, Mandat SA, Olenchock BA, Blobel GA. 2005. Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19:381–391.
  • van der Krol AR, Mur LA, Beld M, Mol JN, Stuitje AR. 1990. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299.
  • Van den Wyngaert I, Sprengel J, Kass SU, Luyten WH. 1998. Cloning and analysis of a novel human putative DNA methyltransferase. FEBS Lett 426:283–289.
  • Van Holde KE. 1988. Histone modifications. In Chromatin (ed. A., Rich)), Springer, New York, pp. 111–148.
  • Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, Baltissen MP, Stunnenberg HG, Mann M, Timmers HT. 2007. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58–69.
  • Waddington CH 1941. The pupal contraction as an epigenetic crisis in Drosophila. Proc Zool Soc Lond A 111:181–188.
  • Waddington CH 1942a. The epigenotype. Endeavour Jan:18–20.
  • Waddington CH 1942b. Canalization of development and their inheritance of acquired characters. Nature 150:563–565.
  • Waddington CH. 1957. The Strategy of Genes: A Discussion of Some Aspects of Theoretical Biology. George Allen & Unwin, London, pp. 262.
  • Wang H, Huang ZQ, Xia L, Feng Q, Erdjument-Bromage H, Strahl BD, Briggs SD, Allis CD, Wong J, Tempst P, Zhang Y. 2001a. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293:853–857.
  • Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, Zhang Y. 2001b. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8:1207–1217.
  • Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H. 2006. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20:1732–1743.
  • West MH, Bonner WM. 1980. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res 8:4671–4680.
  • Wu RS, Kohn KW, Bonner WM. 1981. Metabolism of ubiquitinated histones. J Biol Chem 256:5916–5920.
  • Wyatt GR. 1950. Occurrence of 5-methylcytosine in nucleic acids. Nature 166:237–238.
  • Wyatt GR. 1951a. Recognition and estimation of 5-methylcytosine in nucleic acids. Biochem J 48:581–584.
  • Wyatt GR. 1951b. The purine and pyrimidine composition of deoxypentose nucleic acids. Biochem J 48:584–590.
  • Xie S, Wang Z, Okano M, Nogami M, Li Y, He WW, Okumura K, Li E. 1999. Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene 236:87–95.
  • Yang JS, Maurin T, Robine N, Rasmussen KD, Jeffrey KL, Chandwani R, Papapetrou EP, Sadelain M, O’Carroll D, Lai EC. 2010. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci USA 107:15163–15168.
  • Yi R, Qin Y, Macara IG, Cullen BR. 2003. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17:3011–3016.
  • Yoder JA, Bestor TH. 1998. A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum Mol Genet 7:279–284.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.