In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions

Molecular Cell

Volumn 44, Issue 3, 2011, Pages 361-372

  Quenneville, Simon ^a   Verde, Gaetano ^b,d   Corsinotti, Andrea ^a   Kapopoulou, Adamandia ^a   Jakobsson, Johan ^a,e   Offner, Sandra ^a   Baglivo, Ilaria ^c   Pedone, Paolo V ^c   Grimaldi, Giovanna ^b   Riccio, Andrea ^b,c   Trono, Didier ^a  

^a EPFL   (Switzerland)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; HETEROCHROMATIN PROTEIN 1; HISTONE METHYLTRANSFERASE; KRAB ASSOCIATED PROTEIN 1; KRUPPEL LIKE FACTOR; NP95 ENZYME; NUCLEOTIDE; SETDB1 ENZYME; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN 57;

ALLELE; ARTICLE; CHROMATIN; DNA BINDING; DNA METHYLATION; EMBRYONIC STEM CELL; GENOME IMPRINTING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; DNA MODIFICATION METHYLASES; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; GENOMIC IMPRINTING; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEOTIDE MOTIFS; PROTEIN METHYLTRANSFERASES; REPRESSOR PROTEINS;

MAMMALIA;

EID: 80555156105     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.08.032     Document Type: Article

References (43)

1. Akagi T., Usuda M., Matsuda T., Ko M.S., Niwa H., Asano M., Koide H., Yokota T. Identification of Zfp-57 as a downstream molecule of STAT3 and Oct-3/4 in embryonic stem cells. Biochem. Biophys. Res. Commun. 2005, 331:23-30.
2. Alonso M.B., Zoidl G., Taveggia C., Bosse F., Zoidl C., Rahman M., Parmantier E., Dean C.H., Harris B.S., Wrabetz L., et al. Identification and characterization of ZFP-57, a novel zinc finger transcription factor in the mammalian peripheral nervous system. J. Biol. Chem. 2004, 279:25653-25664.
3. Arita K., Ariyoshi M., Tochio H., Nakamura Y., Shirakawa M. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 2008, 455:818-821.
4. Avvakumov G.V., Walker J.R., Xue S., Li Y., Duan S., Bronner C., Arrowsmith C.H., Dhe-Paganon S. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 2008, 455:822-825.
5. Bilodeau S., Kagey M.H., Frampton G.M., Rahl P.B., Young R.A. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev. 2009, 23:2484-2489.
6. Bostick M., Kim J.K., Estève P.O., Clark A., Pradhan S., Jacobsen S.E. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 317:1760-1764.
7. Ciccone D.N., Chen T. Histone lysine methylation in genomic imprinting. Epigenetics 2009, 4:216-220.
8. Conlon E.M., Liu X.S., Lieb J.D., Liu J.S. Integrating regulatory motif discovery and genome-wide expression analysis. Proc. Natl. Acad. Sci. USA 2003, 100:3339-3344.
9. Delaval K., Govin J., Cerqueira F., Rousseaux S., Khochbin S., Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 2007, 26:720-729.
10. Ficz G., Branco M.R., Seisenberger S., Santos F., Krueger F., Hore T.A., Marques C.J., Andrews S., Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473:398-402.
11. Groner A.C., Meylan S., Ciuffi A., Zangger N., Ambrosini G., Dénervaud N., Bucher P., Trono D. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet. 2010, 6:e1000869.
12. Hark A.T., Schoenherr C.J., Katz D.J., Ingram R.S., Levorse J.M., Tilghman S.M. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000, 405:486-489.
13. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
14. Jakobsson J., Cordero M.I., Bisaz R., Groner A.C., Busskamp V., Bensadoun J.C., Cammas F., Losson R., Mansuy I.M., Sandi C., Trono D. KAP1-mediated epigenetic repression in the forebrain modulates behavioral vulnerability to stress. Neuron 2008, 60:818-831.
15. Kacem S., Feil R. Chromatin mechanisms in genomic imprinting. Mamm. Genome 2009, 20:544-556.
16. Koerner M.V., Pauler F.M., Huang R., Barlow D.P. The function of non-coding RNAs in genomic imprinting. Development 2009, 136:1771-1783.
17. Lane N., Dean W., Erhardt S., Hajkova P., Surani A., Walter J., Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003, 35:88-93.
18. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
19. Lehnertz B., Ueda Y., Derijck A.A., Braunschweig U., Perez-Burgos L., Kubicek S., Chen T., Li E., Jenuwein T., Peters A.H. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 2003, 13:1192-1200.
20. Li X., Ito M., Zhou F., Youngson N., Zuo X., Leder P., Ferguson-Smith A.C. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 2008, 15:547-557.
21. Mackay D.J., Callaway J.L., Marks S.M., White H.E., Acerini C.L., Boonen S.E., Dayanikli P., Firth H.V., Goodship J.A., Haemers A.P., et al. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat. Genet. 2008, 40:949-951.
22. Mager J., Montgomery N.D., de Villena F.P., Magnuson T. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat. Genet. 2003, 33:502-507.
23. Matsui T., Leung D., Miyashita H., Maksakova I.A., Miyachi H., Kimura H., Tachibana M., Lorincz M.C., Shinkai Y. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 2010, 464:927-931.
24. Meilinger D., Fellinger K., Bultmann S., Rothbauer U., Bonapace I.M., Klinkert W.E., Spada F., Leonhardt H. Np95 interacts with de novo DNA methyltransferases, Dnmt3a and Dnmt3b, and mediates epigenetic silencing of the viral CMV promoter in embryonic stem cells. EMBO Rep. 2009, 10:1259-1264.
25. Nagano T., Mitchell J.A., Sanz L.A., Pauler F.M., Ferguson-Smith A.C., Feil R., Fraser P. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 2008, 322:1717-1720.
26. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007, 447:425-432.
27. Renda M., Baglivo I., Burgess-Beusse B., Esposito S., Fattorusso R., Felsenfeld G., Pedone P.V. Critical DNA binding interactions of the insulator protein CTCF: a small number of zinc fingers mediate strong binding, and a single finger-DNA interaction controls binding at imprinted loci. J. Biol. Chem. 2007, 282:33336-33345.
28. Riclet R., Chendeb M., Vonesch J.L., Koczan D., Thiesen H.J., Losson R., Cammas F. Disruption of the interaction between transcriptional intermediary factor 1beta and heterochromatin protein 1 leads to a switch from DNA hyper- to hypomethylation and H3K9 to H3K27 trimethylation on the MEST promoter correlating with gene reactivation. Mol. Biol. Cell 2009, 20:296-305.
29. Rowe H.M., Jakobsson J., Mesnard D., Rougemont J., Reynard S., Aktas T., Maillard P.V., Layard-Liesching H., Verp S., Marquis J., et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 2010, 463:237-240.
30. Sanz L.A., Chamberlain S., Sabourin J.C., Henckel A., Magnuson T., Hugnot J.P., Feil R., Arnaud P. A mono-allelic bivalent chromatin domain controls tissue-specific imprinting at Grb10. EMBO J. 2008, 27:2523-2532.
31. Sasai N., Nakao M., Defossez P.A. Sequence-specific recognition of methylated DNA by human zinc-finger proteins. Nucleic Acids Res. 2010, 38:5015-5022.
32. Schultz D.C., Friedman J.R., Rauscher F.J. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev. 2001, 15:428-443.
33. Schultz D.C., Ayyanathan K., Negorev D., Maul G.G., Rauscher F.J. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 2002, 16:919-932.
34. Sharif J., Muto M., Takebayashi S., Suetake I., Iwamatsu A., Endo T.A., Shinga J., Mizutani-Koseki Y., Toyoda T., Okamura K., et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
35. Sripathy S.P., Stevens J., Schultz D.C. The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol. Cell. Biol. 2006, 26:8623-8638.
36. Stedman W., Kang H., Lin S., Kissil J.L., Bartolomei M.S., Lieberman P.M. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 2008, 27:654-666.
37. Tsumura A., Hayakawa T., Kumaki Y., Takebayashi S., Sakaue M., Matsuoka C., Shimotohno K., Ishikawa F., Li E., Ueda H.R., et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 2006, 11:805-814.
38. Wagschal A., Sutherland H.G., Woodfine K., Henckel A., Chebli K., Schulz R., Oakey R.J., Bickmore W.A., Feil R. G9a histone methyltransferase contributes to imprinting in the mouse placenta. Mol. Cell. Biol. 2008, 28:1104-1113.
39. Weaver J.R., Sarkisian G., Krapp C., Mager J., Mann M.R., Bartolomei M.S. Domain-specific response of imprinted genes to reduced DNMT1. Mol. Cell Biol. 2010, 30:3916-3928.
40. Wiznerowicz M., Jakobsson J., Szulc J., Liao S., Quazzola A., Beermann F., Aebischer P., Trono D. The Kruppel-associated box repressor domain can trigger de novo promoter methylation during mouse early embryogenesis. J. Biol. Chem. 2007, 282:34535-34541.
41. Wolf D., Goff S.P. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
42. Yuan P., Han J., Guo G., Orlov Y.L., Huss M., Loh Y.H., Yaw L.P., Robson P., Lim B., Ng H.H. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 2009, 23:2507-2520.
43. Zhang Y., Liu T., Meyer C.A., Eeckhoute J., Johnson D.S., Bernstein B.E., Nusbaum C., Myers R.M., Brown M., Li W., Liu X.S. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008, 9:R137.