Restoration of IGF2 imprinting by polycomb repressive complex 2 docking factor SUZ12 in colon cancer cells

Experimental Cell Research

Volumn 338, Issue 2, 2015, Pages 214-221

  Wang, Haibo ^a,c   Ge, Shengfang ^a   Qian, Guanxiang ^a   Li, Wei ^b   Cui, Jiuwei ^b   Wang, Guanjun ^b   Hoffman, Andrew R ^c   Hu, Ji Fan ^b,c  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b JILIN UNIVERSITY   (China)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CTCF; Epigenetics; Histone K27 methylation; IGF2 imprinting; Intrachromosomal loop; Polycomb repressive complex 2; Promoter; SUZ12

Indexed keywords

COMPLEMENTARY DNA; LENTIVIRUS VECTOR; POLYCOMB REPRESSIVE COMPLEX 2; SOMATOMEDIN B; SUZ12 PROTEIN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; HISTONE; IGF2 PROTEIN, HUMAN; SUZ12 PROTEIN, HUMAN;

ADENOCARCINOMA CELL LINE; ALLELE; ARTICLE; CHROMATIN CONFORMATION CAPTURE; CHROMATIN IMMUNOPRECIPITATION; COLON CANCER; COLON CANCER CELL LINE; DNA STRUCTURE; DOWN REGULATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMPRINTING CONTROL REGION; MOLECULAR CLONING; MOLECULAR DOCKING; MOLECULAR IMPRINTING; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VECTOR CONTROL; CELL LINE; COLON TUMOR; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; HT 29 CELL LINE; PROCEDURES; TUMOR CELL LINE;

ALLELES; CELL LINE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; COLONIC NEOPLASMS; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONES; HT29 CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR II; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC;

EID: 84944732896     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.09.016     Document Type: Article

References (53)

1. Thorvaldsen J.L., Duran K.L., Bartolomei M.S. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 1998, 12:3693-3702.
2. Szabo P.E., Tang S.H., Silva F.J., Tsark W.M., Mann J.R. Role of CTCF binding sites in the Igf2/H19 imprinting control region. Mol. Cell Biol. 2004, 24:4791-4800.
3. Srivastava M., Hsieh S., Grinberg A., Williams-Simons L., Huang S.P., Pfeifer K. H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared cis acting regulatory region upstream of H19. Genes Dev. 2000, 14:1186-1195.
4. Ogawa O., Eccles M.R., Szeto J., McNoe L.A., Yun K., Maw M.A., Smith P.J., Reeve A.E. Relaxation of insulin-like growth factor II gene imprinting implicated in Wilms' tumour. Nature 1993, 362:749-751.
5. Ohlsson R., Nystrom A., Pfeifer O.S., Tohonen V., Hedborg F., Schofield P., Flam F., Ekstrom T.J. IGF2 is parentally imprinted during human embryogenesis and in the Beckwith-Wiedemann syndrome. Nat. Genet. 1993, 4:94-97.
6. Rainier S., Johnson L.A., Dobry C.J., Ping A.J., Grundy P.E., Feinberg A.P. Relaxation of imprinted genes in human cancer. Nature 1993, 362:747-749.
7. Cui H., Horon I.L., Ohlsson R., Hamilton S.R., Feinberg A.P. Loss of imprinting in normal tissue of colorectal cancer patients with microsatellite instability. Nat. Med. 1998, 4:1276-1280.
8. Nishihara S., Hayashida T., Mitsuya K., Schulz T.C., Ikeguchi M., Kaibara N., Oshimura M. Multipoint imprinting analysis in sporadic colorectal cancers with and without microsatellite instability. Int. J. Oncol. 2000, 17:317-322.
9. Mann J.R., Szabo P.E., Reed M.R., Singer-Sam J. Methylated DNA sequences in genomic imprinting. Crit. Rev. Eukaryot. Gene Expr. 2000, 10:241-257.
10. Engel N., Bartolomei M.S. Mechanisms of insulator function in gene regulation and genomic imprinting. Int. Rev. Cytol. 2003, 232:89-127.
11. Murrell A., Heeson S., Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet. 2004, 36:889-893.
12. Li T., Hu J.F., Qiu X., Ling J., Chen H., Wang S., Hou A., Vu T.H., Hoffman A.R. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex-2 intrachromosomal loop. Mol. Cell. Biol. 2008, 28:6473-6482.
13. Yusufzai T.M., Tagami H., Nakatani Y., Felsenfeld G. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 2004, 13:291-298.
14. Zhang H., Niu B., Hu J.F., Ge S., Wang H., Li T., Ling J., Steelman B.N., Qian G., Hoffman A.R. Interruption of intrachromosomal looping by CCCTC binding factor decoy proteins abrogates genomic imprinting of human insulin-like growth factor II. J. Cell Biol. 2011, 193:475-487.
15. Allen M., Louise Jones J. Jekyll and Hyde: the role of the microenvironment on the progression of cancer. J. Pathol. 2011, 223:162-176.
16. Sewalt R.G., van der Vlag J., Gunster M.J., Hamer K.M., den Blaauwen J.L., Satijn D.P., Hendrix T., van Driel R., Otte A.P. Characterization of interactions between the mammalian polycomb-group proteins Enx1/EZH2 and EED suggests the existence of different mammalian polycomb-group protein complexes. Mol. Cell. Biol. 1998, 18:3586-3595.
17. van Lohuizen M., Tijms M., Voncken J.W., Schumacher A., Magnuson T., Wientjens E. Interaction of mouse polycomb-group (Pc-G) proteins Enx1 and Enx2 with Eed: indication for separate Pc-G complexes. Mol. Cell. Biol. 1998, 18:3572-3579.
18. Levine S.S., Weiss A., Erdjument-Bromage H., Shao Z., Tempst P., Kingston R.E. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol. Cell. Biol. 2002, 22:6070-6078.
19. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R.S., Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431:873-878.
20. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
21. Czermin B., Melfi R., McCabe D., Seitz V., Imhof A., Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002, 111:185-196.
22. Kirmizis A., Bartley S.M., Kuzmichev A., Margueron R., Reinberg D., Green R., Farnham P.J. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev. 2004, 18:1592-1605.
23. Rajasekhar V.K., Begemann M. Concise review: roles of polycomb group proteins in development and disease: a stem cell perspective. Stem Cells 2007, 25:2498-2510.
24. Jaenisch R., Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 2008, 132:567-582.
25. Sparmann A., van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 2006, 6:846-856.
26. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
27. Payer B., Lee J.T. X chromosome dosage compensation: how mammals keep the balance. Annu. Rev. Genet. 2008, 42:733-772.
28. Wu H.A., Bernstein E. Partners in imprinting: noncoding RNA and polycomb group proteins. Dev. Cell 2008, 15:637-638.
29. Pien S., Grossniklaus U. Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 2007, 1769:375-382.
30. Whitcomb S.J., Basu A., Allis C.D., Bernstein E. Polycomb Group proteins: an evolutionary perspective. Trends Genet. 2007, 23:494-502.
31. Chen H.L., Li T., Qiu X.W., Wu J., Ling J.Q., Sun Z.H., Wang W., Chen W., Hou A., Vu T.H., Hoffman A.R., Hu J.F. Correction of aberrant imprinting of IGF2 in human tumors by nuclear transfer-induced epigenetic reprogramming. EMBO J. 2006, 25:5329-5338.
32. Cui H., Niemitz E.L., Ravenel J.D., Onyango P., Brandenburg S.A., Lobanenkov V.V., Feinberg A.P. Loss of imprinting of insulin-like growth factor-II in Wilms' tumor commonly involves altered methylation but not mutations of CTCF or its binding site. Cancer Res. 2001, 61:4947-4950.
33. Sun J., Li W., Sun Y., Yu D., Wen X., Wang H., Cui J., Wang G., Hoffman A.R., Hu J.F. A novel antisense long noncoding RNA within the IGF1R gene locus is imprinted in hematopoietic malignancies. Nucleic Acids Res. 2014, 42:9588-9601.
34. Wang H., Li W., Guo R., Sun J., Cui J., Wang G., Hoffman A.R., Hu J.F. An intragenic long noncoding RNA interacts epigenetically with the RUNX1 promoter and enhancer chromatin DNA in hematopoietic malignancies. Int. J. Cancer 2014, 135:2783-2794.
35. Zhang S., Zhong B., Chen M., Yang G., Li Y., Wang H., Wang G., Li W., Cui J., Hoffman A.R., Hu J. Epigenetic reprogramming reverses the malignant epigenotype of the MMP/TIMP axis genes in tumor cells. Int. J. Cancer 2014, 134:1583-1594.
36. Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311.
37. Zhang H., Jiao W., Sun L., Fan J., Chen M., Wang H., Xu X., Shen A., Li T., Niu B., Ge S., Li W., Cui J., Wang G., Sun J., Fan X., Hu X., Mrsny R.J., Hoffman A.R., Hu J.F. Intrachromosomal looping is required for activation of endogenous pluripotency genes during reprogramming. Cell Stem Cell 2013, 13:30-35.
38. Vu T.H., Hoffman A.R. Promoter-specific imprinting of the human insulin-like growth factor-II gene. Nature 1994, 371:714-717.
39. Hu J.F., Vu T.H., Hoffman A.R. Genomic deletion of an imprint maintenance element abolishes imprinting of both insulin-like growth factor II and H19. J. Biol. Chem. 1997, 272:20715-20720.
40. Li T., Chen H., Li W., Cui J., Wang G., Hu X., Hoffman A.R., Hu J. Promoter histone H3K27 methylation in the control of IGF2 imprinting in human tumor cell lines. Hum. Mol. Genet. 2014, 23:117-128.
41. Donnelly M.L., Hughes L.E., Luke G., Mendoza H., ten Dam E., Gani D., Ryan M.D. The 'cleavage' activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring '2A-like' sequences. J. Gen. Virol. 2001, 82:1027-1041.
42. Vu T.H., Nguyen A.H., Hoffman A.R. Loss of IGF2 imprinting is associated with abrogation of long-range intrachromosomal interactions in human cancer cells. Hum. Mol. Genet. 2010, 19:901-919.
43. Bell A.C., Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000, 405:482-485.
44. 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.
45. Sparago A., Cerrato F., Vernucci M., Ferrero G.B., Silengo M.C., Riccio A. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nat. Genet. 2004, 36:958-960.
46. Cui H., Onyango P., Brandenburg S., Wu Y., Hsieh C.L., Feinberg A.P. Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res. 2002, 62:6442-6446.
47. Simon J.A., Kingston R.E. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 2009, 10:697-708.
48. Wang L., Brown J.L., Cao R., Zhang Y., Kassis J.A., Jones R.S. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 2004, 14:637-646.
49. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
50. Ringrose L., Paro R. Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 2007, 134:223-232.
51. Thomas M.J., Seto E. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key?. Gene 1999, 236:197-208.
52. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., Bell G.W., Otte A.P., Vidal M., Gifford D.K., Young R.A., Jaenisch R. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
53. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., Chevalier B., Johnstone S.E., Cole M.F., Isono K., Koseki H., Fuchikami T., Abe K., Murray H.L., Zucker J.P., Yuan B., Bell G.W., Herbolsheimer E., Hannett N.M., Sun K., Odom D.T., Otte A.P., Volkert T.L., Bartel D.P., Melton D.A., Gifford D.K., Jaenisch R., Young R.A. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.