1,188
Views
12
CrossRef citations to date
0
Altmetric
Research Paper

A cross-talk between DNA methylation and H3 lysine 9 dimethylation at the KvDMR1 region controls the induction of Cdkn1c in muscle cells

, , , , &
Pages 791-803 | Received 11 Mar 2016, Accepted 25 Aug 2016, Published online: 01 Nov 2016

References

  • Pateras IS, Apostolopoulou K, Niforou K, Kotsinas A, Gorgoulis VG. p57KIP2: “Kip”ing the cell under control. Mol Cancer Res 2009; 7:1902-19; PMID:19934273; http://dx.doi.org/10.1158/1541-7786.MCR-09-0317
  • Yan Y, Frisen J, Lee MH, Massague J, Barbacid M. Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev 1997; 11:973-83; PMID:9136926; http://dx.doi.org/10.1101/gad.11.8.973
  • Zhang P, Liegeois NJ, Wong C, Finegold M, Hou H, Thompson JC, Silverman A, Harper JW, DePinho RA, Elledge SJ. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 1997; 387:151-8; PMID:9144284; http://dx.doi.org/10.1038/387151a0
  • Eggermann T, Binder G, Brioude F, Maher ER, Lapunzina P, Cubellis MV, Bergada I, Prawitt D, Begemann M. CDKN1C mutations: two sides of the same coin. Trends Mol Med 2014; 20:614-22; PMID:25262539; http://dx.doi.org/10.1016/j.molmed.2014.09.001
  • Lee MH, Reynisdottir I, Massague J. Cloning or P57(Kip2), a Cyclin-Dependent Kinase Inhibitor with Unique Domain-Structure and Tissue Distribution. Genes Dev 1995; 9:639-49; PMID:7729683; http://dx.doi.org/10.1101/gad.9.6.639
  • Matsuoka S, Edwards MC, Bai C, Parker S, Zhang PM, Baldini A, Harper JW, Elledge SJ. P57(Kip2), a Structurally Distinct Member of the P21(Cip1) Cdk Inhibitor Family, Is a Candidate Tumor-Suppressor Gene. Genes Dev 1995; 9:650-62; PMID:7729684; http://dx.doi.org/10.1101/gad.9.6.650
  • Susaki E, Nakayama K, Yamasaki L, Nakayama KI. Common and specific roles of the related CDK inhibitors p27 and p57 revealed by a knock-in mouse model. Proc Nat Acad Sci U S A 2009; 106:5192-7; PMID:19276117; http://dx.doi.org/10.1073/pnas.0811712106
  • Nagahama H, Hatakeyama S, Nakayama K, Nagata M, Tomita K, Nakayama K. Spatial and temporal expression patterns of the cyclin-dependent kinase (CDK) inhibitors p27(Kip1) and p57(Kip2) during mouse development. Anat Embryol 2001; 203:77-87; PMID:11218061; http://dx.doi.org/10.1007/s004290000146
  • Hatada I, Mukai T. Genomic imprinting of p57KIP2, a cyclin-dependent kinase inhibitor, in mouse. Nat Genet 1995; 11:204-6; PMID:7550351; http://dx.doi.org/10.1038/ng1095-204
  • Matsuoka S, Thompson JS, Edwards MC, Bartletta JM, Grundy P, Kalikin LM, Harper JW, Elledge SJ, Feinberg AP. Imprinting of the gene encoding a human cyclin-dependent kinase inhibitor, p57KIP2, on chromosome 11p15. Proc Nat Acad Sci U S A 1996; 93:3026-30; PMID:8610162; http://dx.doi.org/10.1073/pnas.93.7.3026
  • Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet 2002; 32:426-31; PMID:12410230; http://dx.doi.org/10.1038/ng988
  • Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, Higgins M, Feil R, Reik W. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet 2004; 36:1291-5; PMID:15516931; http://dx.doi.org/10.1038/ng1468
  • Smilinich NJ, Day CD, Fitzpatrick GV, Caldwell GM, Lossie AC, Cooper PR, Smallwood AC, Joyce JA, Schofield PN, Reik W, et al. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc Nat Acad Sci U S A 1999; 96:8064-9; PMID:10393948; http://dx.doi.org/10.1073/pnas.96.14.8064
  • Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, Feil R. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet 2004; 36:1296-300; PMID:15516932; http://dx.doi.org/10.1038/ng1467
  • Fitzpatrick GV, Pugacheva EM, Shin JY, Abdullaev Z, Yang Y, Khatod K, Lobanenkov VV, Higgins MJ. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol Cell Biol 2007; 27:2636-47; PMID:17242189; http://dx.doi.org/10.1128/MCB.02036-06
  • Mancini-DiNardo D, Steele SJS, Ingram RS, Tilghman SM. A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer. Hum Mol Genet 2003; 12:283-94; PMID:12554682; http://dx.doi.org/10.1093/hmg/ddg024
  • Kanduri C. Kcnq1ot1: A chromatin regulatory RNA. Semin Cell Dev Biol 2011; 22:343-50; PMID:21345374; http://dx.doi.org/10.1016/j.semcdb.2011.02.020
  • Demars J, Gicquel C. Epigenetic and genetic disturbance of the imprinted 11p15 region in Beckwith-Wiedemann and Silver-Russell syndromes. Clin Genet 2012; 81:350-61; PMID:22150955; http://dx.doi.org/10.1111/j.1399-0004.2011.01822.x
  • Figliola R, Maione R. MyoD induces the expression of p57Kip2 in cells lacking p21Cip1/Waf1: overlapping and distinct functions of the two cdk inhibitors. J Cell Physiol 2004; 200:468-75; PMID:15254975; http://dx.doi.org/10.1002/jcp.20044
  • Berkes CA, Tapscott SJ. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 2005; 16:585-95; PMID:16099183; http://dx.doi.org/10.1016/j.semcdb.2005.07.006
  • Figliola R, Busanello A, Vaccarello G, Maione R. Regulation of p57(KIP2) during muscle differentiation: role of Egr1, Sp1 and DNA hypomethylation. J Mol Biol 2008; 380:265-77; PMID:18513743; http://dx.doi.org/10.1016/j.jmb.2008.05.004
  • Vaccarello G, Figliola R, Cramerotti S, Novelli F, Maione R. p57Kip2 is induced by MyoD through a p73-dependent pathway. J Mol Biol 2006; 356:578-88; PMID:16405903; http://dx.doi.org/10.1016/j.jmb.2005.12.024
  • Battistelli C, Busanello A, Maione R. Functional interplay between MyoD and CTCF in regulating long-range chromatin interactions during differentiation. J Cell Sci 2014; 127:3757-67; PMID:25002401; http://dx.doi.org/10.1242/jcs.149427
  • Busanello A, Battistelli C, Carbone M, Mostocotto C, Maione R. MyoD regulates p57(kip2) expression by interacting with a distant cis-element and modifying a higher order chromatin structure. Nucleic Acids Res 2012; 40:8266-75; PMID:22740650; http://dx.doi.org/10.1093/nar/gks619
  • Balint E, Phillips AC, Kozlov S, Stewart CL, Vousden KH. Induction of p57(KIP2) expression by p73 beta. Proc Nat Acad Sci U S A 2002; 99:3529-34; PMID:11891335; http://dx.doi.org/10.1073/pnas.0624-91899
  • Rothschild G, Zhao X, Iavarone A, Lasorella A. E Proteins and Id2 converge on p57Kip2 to regulate cell cycle in neural cells. Mol Cell Biol 2006; 26:4351-61; PMID:16705184; http://dx.doi.org/10.1128/MCB.01743-05
  • Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 2002; 9:587-600; PMID:11931766; http://dx.doi.org/10.1016/S1097-2765(02)00481-1
  • Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, et al. Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 2010; 18:662-74; PMID:20412780; http://dx.doi.org/10.1016/j.devcel.2010.02.014
  • Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011; 25:1010-22; PMID:21576262; http://dx.doi.org/10.1101/gad.2037511
  • Espada J, Esteller M. DNA methylation and the functional organization of the nuclear compartment. Semin Cell Dev Biol 2010; 21:238-46; PMID:19892028; http://dx.doi.org/10.1016/j.semcdb.2009.10.006
  • Schubeler D. Function and information content of DNA methylation. Nature 2015; 517:321-6; PMID:25592537; http://dx.doi.org/10.1038/nature14192
  • Miranda TB, Jones PA. DNA methylation: The nuts and bolts of repression. J Cell Physiol 2007; 213:384-90; PMID:17708532; http://dx.doi.org/10.1002/jcp.21224
  • Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009; 10:295-304; PMID:19308066; http://dx.doi.org/10.1038/nrg2540
  • Clouaire T, Stancheva I. Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci 2008; 65:1509-22; PMID:18322651; http://dx.doi.org/10.1007/s00018-008-7324-y
  • Tate PH, Bird AP. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr Opin Genet Dev 1993; 3:226-31; PMID:8504247; http://dx.doi.org/10.1016/0959-437X(93)90027-M
  • Bhogal B, Arnaudo A, Dymkowski A, Best A, Davis TL. Methylation at mouse Cdkn1c is acquired during postimplantation development and functions to maintain imprinted expression. Genomics 2004; 84:961-70; PMID:15533713; http://dx.doi.org/10.1016/j.ygeno.2004.08.004
  • Kikuchi T, Toyota M, Itoh F, Suzuki H, Obata T, Yamamoto H, Kakiuchi H, Kusano M, Issa JP, Tokino T, et al. Inactivation of p57KIP2 by regional promoter hypermethylation and histone deacetylation in human tumors. Oncogene 2002; 21:2741-9; PMID:11965547; http://dx.doi.org/10.1038/sj.onc.1205376
  • Kuang SQ, Ling X, Sanchez-Gonzalez B, Yang H, Andreeff M, Garcia-Manero G. Differential tumor suppressor properties and transforming growth factor-beta responsiveness of p57KIP2 in leukemia cells with aberrant p57KIP2 promoter DNA methylation. Oncogene 2007; 26:1439-48; PMID:16936778; http://dx.doi.org/10.1038/sj.onc.1209907
  • Li Y, Nagai H, Ohno T, Yuge M, Hatano S, Ito E, Mori N, Saito H, Kinoshita T. Aberrant DNA methylation of p57(KIP2) gene in the promoter region in lymphoid malignancies of B-cell phenotype. Blood 2002; 100:2572-7; PMID:12239171; http://dx.doi.org/10.1182/blood-2001-11-0026
  • Shin JY, Kim HS, Park J, Park JB, Lee JY. Mechanism for inactivation of the KIP family cyclin-dependent kinase inhibitor genes in gastric cancer cells. Cancer Res 2000; 60:262-5; PMID:10667572
  • Fuso A, Ferraguti G, Grandoni F, Ruggeri R, Scarpa S, Strom R, Lucarelli M. Early demethylation of non-CpG, CpC-rich, elements in the myogenin 5′-flanking region: a priming effect on the spreading of active demethylation. Cell Cycle 2010; 9:3965-76; PMID:20935518; http://dx.doi.org/10.4161/cc.9.19.13193
  • Konieczny SF, Emerson CP, Jr. 5-Azacytidine induction of stable mesodermal stem cell lineages from 10T1/2 cells: evidence for regulatory genes controlling determination. Cell 1984; 38:791-800; PMID:6207933; http://dx.doi.org/10.1016/0092-8674(84)90274-5
  • Taylor SM, Jones PA. Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 1979; 17:771-9; PMID:90553; http://dx.doi.org/10.1016/0092-8674(79)90317-9
  • Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987; 51:987-1000; PMID:3690668; http://dx.doi.org/10.1016/0092-8674(87)90585-X
  • Lassar AB, Paterson BM, Weintraub H. Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell 1986; 47:649-56; PMID:2430720; http://dx.doi.org/10.1016/0092-8674(86)90507-6
  • El Kharroubi A, Piras G, Stewart CL. DNA demethylation reactivates a subset of imprinted genes in uniparental mouse embryonic fibroblasts. J Biol Chem 2001; 276:8674-80; PMID:11124954; http://dx.doi.org/10.1074/jbc.M009392200
  • Chandra S, Baribault C, Lacey M, Ehrlich M. Myogenic differential methylation: diverse associations with chromatin structure. Biology 2014; 3:426-51; PMID:24949935; http://dx.doi.org/10.3390/biology30-20426
  • Tsumagari K, Baribault C, Terragni J, Varley KE, Gertz J, Pradhan S, Badoo M, Crain CM, Song L, Crawford GE, et al. Early de novo DNA methylation and prolonged demethylation in the muscle lineage. Epigenetics 2013; 8:317-32; PMID:23417056; http://dx.doi.org/10.4161/epi.23989
  • Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2010; 2:657-69; PMID:21339843; http://dx.doi.org/10.2217/epi.10.44
  • Torres IO, Fujimori DG. Functional coupling between writers, erasers and readers of histone and DNA methylation. Curr Opin Struct Biol 2015; 35:68-75; PMID:26496625; http://dx.doi.org/10.1016/j.sbi.2015.09.007
  • Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 2003; 12:1591-8; PMID:14690610; http://dx.doi.org/10.1016/S1097-2765(03)00479-9
  • Rao VK, Ow JR, Shankar SR, Bharathy N, Manikandan J, Wang Y, Taneja R. G9a promotes proliferation and inhibits cell cycle exit during myogenic differentiation. Nucleic Acids Res 2016.
  • Cheng X. Structural and functional coordination of DNA and histone methylation. Cold Spring Harb Perspect Biol 2014; 6; PMID:25085914; http://dx.doi.org/10.1101/cshperspect.a018747
  • Egger G, Aparicio AM, Escobar SG, Jones PA. Inhibition of histone deacetylation does not block resilencing of p16 after 5-aza-2′-deoxycytidine treatment. Cancer Res 2007; 67:346-53; PMID:17210717; http://dx.doi.org/10.1158/0008-5472.CAN-06-2845
  • McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, Baylin SB. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res 2006; 66:3541-9; PMID:16585178; http://dx.doi.org/10.1158/0008-5472.CAN-05-2481
  • Yang X, Karuturi RK, Sun F, Aau M, Yu K, Shao R, Miller LD, Tan PB, Yu Q. CDKN1C (p57) is a direct target of EZH2 and suppressed by multiple epigenetic mechanisms in breast cancer cells. Plos One 2009; 4:e5011; PMID:19340297; http://dx.doi.org/10.1371/journal.pone.0005011
  • Mozzetta C, Boyarchuk E, Pontis J, Ait-Si-Ali S. Sound of silence: the properties and functions of repressive Lys methyltransferases. Nat Rev Mol Cell Biol 2015; 16:499-513; PMID:26204160; http://dx.doi.org/10.1038/nrm4029
  • Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet 2009; 41:246-50; PMID:19151716; http://dx.doi.org/10.1038/ng.297
  • Ling BM, Gopinadhan S, Kok WK, Shankar SR, Gopal P, Bharathy N, Wang Y, Taneja R. G9a mediates Sharp-1-dependent inhibition of skeletal muscle differentiation. Mol Biol Cell 2012; 23:4778-85; PMID:23087213; http://dx.doi.org/10.1091/mbc.E12-04-0311
  • Mal A, Harter ML. MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc Nat Acad Sci U S A 2003; 100:1735-9; PMID:12578986; http://dx.doi.org/10.1073/pnas.0437843100
  • Ling BM, Bharathy N, Chung TK, Kok WK, Li S, Tan YH, Rao VK, Gopinadhan S, Sartorelli V, Walsh MJ, et al. Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation. Proc Nat Acad Sci U S A 2012; 109:841-6; PMID:22215600; http://dx.doi.org/10.1073/pnas.1111628109
  • Nguyen CT, Weisenberger DJ, Velicescu M, Gonzales FA, Lin JC, Liang G, Jones PA. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res 2002; 62:6456-61; PMID:12438235
  • Wozniak RJ, Klimecki WT, Lau SS, Feinstein Y, Futscher BW. 5-Aza-2′-deoxycytidine-mediated reductions in G9A histone methyltransferase and histone H3 K9 di-methylation levels are linked to tumor suppressor gene reactivation. Oncogene 2007; 26:77-90; PMID:16799634; http://dx.doi.org/10.1038/sj.onc.1209763
  • Kury P, Greiner-Petter R, Cornely C, Jurgens T, Muller HW. Mammalian achaete scute homolog 2 is expressed in the adult sciatic nerve and regulates the expression of Krox24, Mob-1, CXCR4, and p57kip2 in Schwann cells. J Neurosci 2002; 22:7586-95; PMID:12196582

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.