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Research Paper

Epigenetic regulation of planarian stem cells by the SET1/MLL family of histone methyltransferases

, , , , &
Pages 79-91 | Published online: 12 Dec 2012

References

  • Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693 - 705; http://dx.doi.org/10.1016/j.cell.2007.02.005; PMID: 17320507
  • Shilatifard A. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 2012; 81:65 - 95; http://dx.doi.org/10.1146/annurev-biochem-051710-134100; PMID: 22663077
  • Ansari KI, Mandal SS. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J 2010; 277:1790 - 804; http://dx.doi.org/10.1111/j.1742-4658.2010.07606.x; PMID: 20236313
  • Nislow C, Ray E, Pillus L. SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 1997; 8:2421 - 36; PMID: 9398665
  • Wenzel D, Palladino F, Jedrusik-Bode M. Epigenetics in C. elegans: facts and challenges. Genesis 2011; 49:647 - 61; http://dx.doi.org/10.1002/dvg.20762; PMID: 21538806
  • Mohan M, Herz HM, Smith ER, Zhang Y, Jackson J, Washburn MP, et al. The COMPASS family of H3K4 methylases in Drosophila. Mol Cell Biol 2011; 31:4310 - 8; http://dx.doi.org/10.1128/MCB.06092-11; PMID: 21875999
  • Eissenberg JC, Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 2010; 339:240 - 9; http://dx.doi.org/10.1016/j.ydbio.2009.08.017; PMID: 19703438
  • Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, et al. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci U S A 2001; 98:12902 - 7; http://dx.doi.org/10.1073/pnas.231473398; PMID: 11687631
  • Lee JH, Skalnik DG. CpG-binding protein (CXXC finger protein 1) is a component of the mammalian Set1 histone H3-Lys4 methyltransferase complex, the analogue of the yeast Set1/COMPASS complex. J Biol Chem 2005; 280:41725 - 31; http://dx.doi.org/10.1074/jbc.M508312200; PMID: 16253997
  • Cho YW, Hong T, Hong S, Guo H, Yu H, Kim D, et al. PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 2007; 282:20395 - 406; http://dx.doi.org/10.1074/jbc.M701574200; PMID: 17500065
  • Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, et al. Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol 2008; 28:7337 - 44; http://dx.doi.org/10.1128/MCB.00976-08; PMID: 18838538
  • Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, et al. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 2004; 24:5639 - 49; http://dx.doi.org/10.1128/MCB.24.13.5639-5649.2004; PMID: 15199122
  • Ernst P, Vakoc CR. WRAD: enabler of the SET1-family of H3K4 methyltransferases. Brief Funct Genomics 2012; 11:217 - 26; http://dx.doi.org/10.1093/bfgp/els017; PMID: 22652693
  • Krivtsov AV, Armstrong SA. MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer 2007; 7:823 - 33; http://dx.doi.org/10.1038/nrc2253; PMID: 17957188
  • Smith E, Lin C, Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev 2011; 25:661 - 72; http://dx.doi.org/10.1101/gad.2015411; PMID: 21460034
  • Faber J, Armstrong SA. Mixed lineage leukemia translocations and a leukemia stem cell program. Cancer Res 2007; 67:8425 - 8; http://dx.doi.org/10.1158/0008-5472.CAN-07-0972; PMID: 17875678
  • Cozzio A, Passegué E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17:3029 - 35; http://dx.doi.org/10.1101/gad.1143403; PMID: 14701873
  • Elliott SA, Sánchez Alvarado A. The history and enduring contributions of planarians to the study of animal regeneration. Wiley Interdisciplinary Reviews: Developmental Biology 2012; http://dx.doi.org/10.1002/wdev.82
  • Reddien PW. Constitutive gene expression and the specification of tissue identity in adult planarian biology. Trends Genet 2011; 27:277 - 85; http://dx.doi.org/10.1016/j.tig.2011.04.004; PMID: 21680047
  • Baguñà J. The planarian neoblast: the rambling history of its origin and some current black boxes. Int J Dev Biol 2012; 56:19 - 37; http://dx.doi.org/10.1387/ijdb.113463jb; PMID: 22252540
  • Wagner DE, Wang IE, Reddien PW. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011; 332:811 - 6; http://dx.doi.org/10.1126/science.1203983; PMID: 21566185
  • Labbé RM, Irimia M, Currie KW, Lin A, Zhu SJ, Brown DDR, et al. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 2012; 30:1734 - 45; http://dx.doi.org/10.1002/stem.1144; PMID: 22696458
  • Önal P, Grün D, Adamidi C, Rybak A, Solana J, Mastrobuoni G, et al. Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO J 2012; 31:2755 - 69; http://dx.doi.org/10.1038/emboj.2012.110; PMID: 22543868
  • Resch AM, Palakodeti D, Lu YC, Horowitz M, Graveley BR. Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS One 2012; 7:e34447; http://dx.doi.org/10.1371/journal.pone.0034447; PMID: 22496805
  • Qian C, Zhou MM. SET domain protein lysine methyltransferases: Structure, specificity and catalysis. Cell Mol Life Sci 2006; 63:2755 - 63; http://dx.doi.org/10.1007/s00018-006-6274-5; PMID: 17013555
  • Adamidi C, Wang Y, Gruen D, Mastrobuoni G, You X, Tolle D, et al. De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics. Genome Res 2011; 21:1193 - 200; http://dx.doi.org/10.1101/gr.113779.110; PMID: 21536722
  • Glaser S, Schaft J, Lubitz S, Vintersten K, van der Hoeven F, Tufteland KR, et al. Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 2006; 133:1423 - 32; http://dx.doi.org/10.1242/dev.02302; PMID: 16540515
  • Emerling BM, Bonifas J, Kratz CP, Donovan S, Taylor BR, Green ED, et al. MLL5, a homolog of Drosophila trithorax located within a segment of chromosome band 7q22 implicated in myeloid leukemia. Oncogene 2002; 21:4849 - 54; http://dx.doi.org/10.1038/sj.onc.1205615; PMID: 12101424
  • Newmark PA, Reddien PW, Cebrià F, Sánchez Alvarado A. Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci U S A 2003; 100:Suppl 1 11861 - 5; http://dx.doi.org/10.1073/pnas.1834205100; PMID: 12917490
  • Rompolas P, Patel-King RS, King SM. Chapter 4 - Schmidtea mediterranea: A Model System for Analysis of Motile Cilia. In: Stephen MK, Gregory JP, eds. Methods in Cell Biology: Academic Press, 2009:81-98.
  • Rink JC, Vu HT, Sánchez Alvarado A. The maintenance and regeneration of the planarian excretory system are regulated by EGFR signaling. Development 2011; 138:3769 - 80; http://dx.doi.org/10.1242/dev.066852; PMID: 21828097
  • Eisenhoffer GT, Kang H, Sánchez Alvarado A. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 2008; 3:327 - 39; http://dx.doi.org/10.1016/j.stem.2008.07.002; PMID: 18786419
  • Hayashi T, Asami M, Higuchi S, Shibata N, Agata K. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 2006; 48:371 - 80; http://dx.doi.org/10.1111/j.1440-169X.2006.00876.x; PMID: 16872450
  • Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, et al, ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57 - 74; http://dx.doi.org/10.1038/nature11247; PMID: 22955616
  • Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, et al, modENCODE Consortium. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010; 330:1787 - 97; http://dx.doi.org/10.1126/science.1198374; PMID: 21177974
  • Barrero MJ, Izpisua Belmonte JC. Regenerating the epigenome. EMBO Rep 2011; 12:208 - 15; http://dx.doi.org/10.1038/embor.2011.10; PMID: 21311559
  • Katsuyama T, Paro R. Epigenetic reprogramming during tissue regeneration. FEBS Lett 2011; 585:1617 - 24; http://dx.doi.org/10.1016/j.febslet.2011.05.010; PMID: 21569771
  • Bonuccelli L, Rossi L, Lena A, Scarcelli V, Rainaldi G, Evangelista M, et al. An RbAp48-like gene regulates adult stem cells in planarians. J Cell Sci 2010; 123:690 - 8; http://dx.doi.org/10.1242/jcs.053900; PMID: 20124416
  • Scimone ML, Meisel J, Reddien PW. The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 2010; 137:1231 - 41; http://dx.doi.org/10.1242/dev.042051; PMID: 20223763
  • Wagner DE, Ho JJ, Reddien PW. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 2012; 10:299 - 311; http://dx.doi.org/10.1016/j.stem.2012.01.016; PMID: 22385657
  • Rossi L, Salvetti A, Marincola FM, Lena A, Deri P, Mannini L, et al. Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol 2007; 8:R62; http://dx.doi.org/10.1186/gb-2007-8-4-r62; PMID: 17445279
  • Hallson G, Hollebakken RE, Li T, Syrzycka M, Kim I, Cotsworth S, et al. dSet1 is the main H3K4 di- and tri-methyltransferase throughout Drosophila development. Genetics 2012; 190:91 - 100; http://dx.doi.org/10.1534/genetics.111.135863; PMID: 22048023
  • Ardehali MB, Mei A, Zobeck KL, Caron M, Lis JT, Kusch T. Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. EMBO J 2011; 30:2817 - 28; http://dx.doi.org/10.1038/emboj.2011.194; PMID: 21694722
  • Xiao Y, Bedet C, Robert VJ, Simonet T, Dunkelbarger S, Rakotomalala C, et al. Caenorhabditis elegans chromatin-associated proteins SET-2 and ASH-2 are differentially required for histone H3 Lys 4 methylation in embryos and adult germ cells. Proc Natl Acad Sci U S A 2011; 108:8305 - 10; http://dx.doi.org/10.1073/pnas.1019290108; PMID: 21527717
  • Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 2005; 121:859 - 72; http://dx.doi.org/10.1016/j.cell.2005.03.036; PMID: 15960974
  • Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nature Structural &#38. Mol Biol 2006; 13:713 - 9
  • Steward MM, Lee J-S, O'Donovan A, Wyatt M, Bernstein BE, Shilatifard A. Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nature Structural &#38. Mol Biol 2006; 13:852 - 4
  • Jiang H, Shukla A, Wang X, Chen WY, Bernstein BE, Roeder RG. Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 2011; 144:513 - 25; http://dx.doi.org/10.1016/j.cell.2011.01.020; PMID: 21335234
  • Patel A, Dharmarajan V, Vought VE, Cosgrove MS. On the mechanism of multiple lysine methylation by the human mixed lineage leukemia protein-1 (MLL1) core complex. J Biol Chem 2009; 284:24242 - 56; http://dx.doi.org/10.1074/jbc.M109.014498; PMID: 19556245
  • Dehé PM, Dichtl B, Schaft D, Roguev A, Pamblanco M, Lebrun R, et al. Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation. J Biol Chem 2006; 281:35404 - 12; http://dx.doi.org/10.1074/jbc.M603099200; PMID: 16921172
  • Lee JH, Skalnik DG. Wdr82 is a C-terminal domain-binding protein that recruits the Setd1A Histone H3-Lys4 methyltransferase complex to transcription start sites of transcribed human genes. Mol Cell Biol 2008; 28:609 - 18; http://dx.doi.org/10.1128/MCB.01356-07; PMID: 17998332
  • Clouaire T, Webb S, Skene P, Illingworth R, Kerr A, Andrews R, et al. Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev 2012; 26:1714 - 28; http://dx.doi.org/10.1101/gad.194209.112; PMID: 22855832
  • Narayanan A, Ruyechan WT, Kristie TM. The coactivator host cell factor-1 mediates Set1 and MLL1 H3K4 trimethylation at herpesvirus immediate early promoters for initiation of infection. Proc Natl Acad Sci U S A 2007; 104:10835 - 40; http://dx.doi.org/10.1073/pnas.0704351104; PMID: 17578910
  • Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, et al. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 2007; 131:1084 - 96; http://dx.doi.org/10.1016/j.cell.2007.09.046; PMID: 18083099
  • Ang YS, Tsai SY, Lee DF, Monk J, Su J, Ratnakumar K, et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 2011; 145:183 - 97; http://dx.doi.org/10.1016/j.cell.2011.03.003; PMID: 21477851
  • Cowles MW, Hubert A, Zayas RMA. A Lissencephaly-1 homologue is essential for mitotic progression in the planarian Schmidtea mediterranea. Dev Dyn 2012; 241:901 - 10; http://dx.doi.org/10.1002/dvdy.23775; PMID: 22411224
  • Lee JH, You J, Dobrota E, Skalnik DG. Identification and characterization of a novel human PP1 phosphatase complex. J Biol Chem 2010; 285:24466 - 76; http://dx.doi.org/10.1074/jbc.M110.109801; PMID: 20516061
  • Jude CD, Climer L, Xu D, Artinger E, Fisher JK, Ernst P. Unique and independent roles for MLL in adult hematopoietic stem cells and progenitors. Cell Stem Cell 2007; 1:324 - 37; http://dx.doi.org/10.1016/j.stem.2007.05.019; PMID: 18371366
  • Saló E, Tauler J, Jimenez E, Ramón Bayascas J, Gonzalez-Linares J, Garcia-Fernàndez J, et al. Hox and ParaHox Genes in Flatworms: Characterization and Expression. Am Zool 2001; 41:652 - 63; http://dx.doi.org/10.1668/0003-1569(2001)041[0652:HAPGIF]2.0.CO;2
  • Bayascas JR, Castillo E, Muñoz-Mármol AM, Saló E. Planarian Hox genes: novel patterns of expression during regeneration. Development 1997; 124:141 - 8; PMID: 9006075
  • Orii H, Kato K, Umesono Y, Sakurai T, Agata K, Watanabe K. The planarian HOM/HOX homeobox genes (Plox) expressed along the anteroposterior axis. Dev Biol 1999; 210:456 - 68; http://dx.doi.org/10.1006/dbio.1999.9275; PMID: 10357903
  • Rink JC, Gurley KA, Elliott SA, Sánchez Alvarado A. Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 2009; 326:1406 - 10; http://dx.doi.org/10.1126/science.1178712; PMID: 19933103
  • Scimone ML, Srivastava M, Bell GW, Reddien PW. A regulatory program for excretory system regeneration in planarians. Development 2011; 138:4387 - 98; http://dx.doi.org/10.1242/dev.068098; PMID: 21937596
  • Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007; 449:731 - 4; http://dx.doi.org/10.1038/nature06145; PMID: 17713478
  • Fujiki R, Chikanishi T, Hashiba W, Ito H, Takada I, Roeder RG, et al. GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature 2009; 459:455 - 9; http://dx.doi.org/10.1038/nature07954; PMID: 19377461
  • Cheng F, Liu J, Zhou SH, Wang XN, Chew JF, Deng LW. RNA interference against mixed lineage leukemia 5 resulted in cell cycle arrest. Int J Biochem Cell Biol 2008; 40:2472 - 81; http://dx.doi.org/10.1016/j.biocel.2008.04.012; PMID: 18573682
  • Deng LW, Chiu I, Strominger JL. MLL 5 protein forms intranuclear foci, and overexpression inhibits cell cycle progression. Proc Natl Acad Sci U S A 2004; 101:757 - 62; http://dx.doi.org/10.1073/pnas.2036345100; PMID: 14718661
  • Sambasivan R, Pavlath GK, Dhawan J. A gene-trap strategy identifies quiescence-induced genes in synchronized myoblasts. J Biosci 2008; 33:27 - 44; http://dx.doi.org/10.1007/s12038-008-0019-6; PMID: 18376068
  • Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, Pavlath GK, et al. MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci U S A 2009; 106:4719 - 24; http://dx.doi.org/10.1073/pnas.0807136106; PMID: 19264965
  • Madan V, Madan B, Brykczynska U, Zilbermann F, Hogeveen K, Döhner K, et al. Impaired function of primitive hematopoietic cells in mice lacking the Mixed-Lineage-Leukemia homolog MLL5. Blood 2009; 113:1444 - 54; http://dx.doi.org/10.1182/blood-2008-02-142638; PMID: 18952892
  • Regev A, Lamb MJ, Jablonka E. The Role of DNA Methylation in Invertebrates: Developmental Regulation or Genome Defense?. Mol Biol Evol 1998; 15:880; http://dx.doi.org/10.1093/oxfordjournals.molbev.a025992
  • Cebrià F, Newmark PA. Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 2005; 132:3691 - 703; http://dx.doi.org/10.1242/dev.01941; PMID: 16033796
  • Robb SMC, Ross E, Sánchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res 2008; 36:Database issue D599 - 606; http://dx.doi.org/10.1093/nar/gkm684; PMID: 17881371
  • Zayas RM, Hernández A, Habermann B, Wang Y, Stary JM, Newmark PA. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci U S A 2005; 102:18491 - 6; http://dx.doi.org/10.1073/pnas.0509507102; PMID: 16344473
  • Sandmann T, Vogg MC, Owlarn S, Boutros M, Bartscherer K. The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol 2011; 12:R76; http://dx.doi.org/10.1186/gb-2011-12-8-r76; PMID: 21846378
  • de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 2006; 34:Web Server issue W362-5; http://dx.doi.org/10.1093/nar/gkl124; PMID: 16845026
  • Collins JJ 3rd, Hou X, Romanova EV, Lambrus BG, Miller CM, Saberi A, et al. Genome-wide analyses reveal a role for peptide hormones in planarian germline development. PLoS Biol 2010; 8:e1000509; http://dx.doi.org/10.1371/journal.pbio.1000509; PMID: 20967238
  • Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, Sánchez Alvarado A. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 2009; 238:443 - 50; http://dx.doi.org/10.1002/dvdy.21849; PMID: 19161223
  • Gurley KA, Rink JC, Sánchez Alvarado A. β-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 2008; 319:323 - 7; http://dx.doi.org/10.1126/science.1150029; PMID: 18063757
  • Aslanidis C, de Jong PJ. Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 1990; 18:6069 - 74; http://dx.doi.org/10.1093/nar/18.20.6069; PMID: 2235490
  • Abramoff MD, Magalhães PJ, Ram SJ. Image Processing with ImageJ. Biophotonics International 2004; 11:36 - 42
  • Kang H, Sánchez Alvarado A. Flow cytometry methods for the study of cell-cycle parameters of planarian stem cells. Dev Dyn 2009; 238:1111 - 7; http://dx.doi.org/10.1002/dvdy.21928; PMID: 19322765