CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer

Cell Reports

Volumn 7, Issue 4, 2014, Pages 1020-1029

  Kemp, Christopher J ^a   Moore, James M ^a   Moser, Russell ^a   Bernard, Brady ^b   Teater, Matt ^c   Smith, Leslie E ^a   Rabaia, Natalia A ^a   Gurley, Kay E ^a   Guinney, Justin ^d   Busch, Stephanie E ^a   Shaknovich, Rita ^c   Lobanenkov, Victor V ^e   Liggitt, Denny ^f   Shmulevich, Ilya ^b   Melnick, Ari ^c   Filippova, Galina N ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d SAGE BIONETWORKS   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYLBENZ[A]ANTHRACENE; TRANSCRIPTION FACTOR CTCF; CCCTC-BINDING FACTOR; PROTEIN BINDING; REPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER SUSCEPTIBILITY; CHEMICALLY INDUCED DISORDER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENETIC STABILITY; HAPLOINSUFFICIENCY; HEMIZYGOTE; KNOCKOUT MOUSE; MALE; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RADIATION INDUCED NEOPLASM; TUMOR INVASION; TUMOR SUPPRESSOR GENE; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; MUTATION; NEOPLASM; SURVIVAL; TRANSGENIC MOUSE; TUMOR CELL LINE; ANIMAL CELL; CELL DIFFERENTIATION; CHEMICAL CARCINOGENESIS; CTCF GENE; EPITHELIUM CELL; GENE LOSS; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN TISSUE; MESENCHYME CELL; RADIATION CARCINOGENESIS;

MUS;

ANIMALS; CELL LINE, TUMOR; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; GENETIC PREDISPOSITION TO DISEASE; HAPLOINSUFFICIENCY; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEOPLASMS; PROTEIN BINDING; REPRESSOR PROTEINS; SURVIVAL ANALYSIS;

EID: 84901285464     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.004     Document Type: Article

References (24)

1. Akalin A., Garrett-Bakelman F.E., Kormaksson M., Busuttil J., Zhang L., Khrebtukova I., Milne T.A., Huang Y., Biswas D., Hess J.L., et al. Base-pair resolution DNA methylation sequencing reveals profoundly divergent epigenetic landscapes in acute myeloid leukemia. PLoS Genet. 2012, 8:e1002781.
2. Bell A.C., Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000, 405:482-485.
3. Berx G., Cleton-Jansen A.M., Strumane K., de Leeuw W.J., Nollet F., van Roy F., Cornelisse C. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 1996, 13:1919-1925.
4. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. Cancer Genome Atlas Network.
5. De S., Shaknovich R., Riester M., Elemento O., Geng H., Kormaksson M., Jiang Y., Woolcock B., Johnson N., Polo J.M., et al. Aberration in DNA methylation in B-cell lymphomas has a complex origin and increases with disease severity. PLoS Genet. 2013, 9:e1003137.
6. Filippova G.N. Genetics and epigenetics of the multifunctional protein CTCF. Curr. Top. Dev. Biol. 2008, 80:337-360.
7. Filippova G.N., Lindblom A., Meincke L.J., Klenova E.M., Neiman P.E., Collins S.J., Doggett N.A., Lobanenkov V.V. A widely expressed transcription factor with multiple DNA sequence specificity, CTCF, is localized at chromosome segment 16q22.1 within one of the smallest regions of overlap for common deletions in breast and prostate cancers. Genes Chromosomes Cancer 1998, 22:26-36.
8. Filippova G.N., Qi C.F., Ulmer J.E., Moore J.M., Ward M.D., Hu Y.J., Loukinov D.I., Pugacheva E.M., Klenova E.M., Grundy P.E., et al. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter tts DNA-binding specificity. Cancer Res. 2002, 62:48-52.
9. Gurley K.E., Moser A.R., Kemp C.J. Induction of lung tumors in mice with urethane. Mouse Models of Cancer 2014, 63-65. Cold Spring Harbor Laboratory, Cold Spring Harbor. C. Abate-Shen, K. Politi, L.A. Chodosh, K.P. Olive (Eds.).
10. Heath H., Ribeiro de Almeida C., Sleutels F., Dingjan G., van de Nobelen S., Jonkers I., Ling K.W., Gribnau J., Renkawitz R., Grosveld F., et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J. 2008, 27:2839-2850.
11. Hurtado A., Holmes K.A., Ross-Innes C.S., Schmidt D., Carroll J.S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 2011, 43:27-33.
12. Kandoth C., Schultz N., Cherniack A.D., Akbani R., Liu Y., Shen H., Robertson A.G., Pashtan I., Shen R., Benz C.C., et al. Integrated genomic characterization of endometrial carcinoma. Nature 2013, 497:67-73. Cancer Genome Atlas Research Network.
13. Kim T.H., Abdullaev Z.K., Smith A.D., Ching K.A., Loukinov D.I., Green R.D., Zhang M.Q., Lobanenkov V.V., Ren B. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007, 128:1231-1245.
14. Lawrence M.S., Stojanov P., Mermel C.H., Robinson J.T., Garraway L.A., Golub T.R., Meyerson M., Gabriel S.B., Lander E.S., Getz G. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014, 505:495-501.
15. Moore J.M., Rabaia N.A., Smith L.E., Fagerlie S., Gurley K.E., Loukinov D., Disteche C.M., Collins S.J., Kemp C.J., Lobanenkov V.V., Filippova G.N. Loss of maternal CTCF is associated with peri-implantation lethality of Ctcf null embryos. PLoS ONE 2012, 7:e34915.
16. Mukhopadhyay R., Yu W., Whitehead J., Xu J., Lezcano M., Pack S., Kanduri C., Kanduri M., Ginjala V., Vostrov A., et al. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genome-wide. Genome Res. 2004, 14:1594-1602.
17. Nakahashi H., Kwon K.R., Resch W., Vian L., Dose M., Stavreva D., Hakim O., Pruett N., Nelson S., Yamane A., et al. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep. 2013, 3:1678-1689.
18. Ong C.T., Corces V.G. CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 2014, 15:234-246.
19. Payne S.R., Kemp C.J. Tumor suppressor genetics. Carcinogenesis 2005, 26:2031-2045.
20. Phillips J.E., Corces V.G. CTCF: master weaver of the genome. Cell 2009, 137:1194-1211.
21. Rakha E.A., Green A.R., Powe D.G., Roylance R., Ellis I.O. Chromosome 16 tumor-suppressor genes in breast cancer. Genes Chromosomes Cancer 2006, 45:527-535.
22. Rasko J.E., Klenova E.M., Leon J., Filippova G.N., Loukinov D.I., Vatolin S., Robinson A.F., Hu Y.J., Ulmer J., Ward M.D., et al. Cell growth inhibition by the multifunctional multivalent zinc-finger factor CTCF. Cancer Res. 2001, 61:6002-6007.
23. Wang H., Maurano M.T., Qu H., Varley K.E., Gertz J., Pauli F., Lee K., Canfield T., Weaver M., Sandstrom R., et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 2012, 22:1680-1688.
24. Zampieri M., Guastafierro T., Calabrese R., Ciccarone F., Bacalini M.G., Reale A., Perilli M., Passananti C., Caiafa P. ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. Biochem. J. 2012, 441:645-652.