Mutational analysis of the poly(ADP-ribosyl)ation sites of the transcription factor CTCF provides an insight into the mechanism of its regulation by poly(ADP-Ribosyl)ation

Molecular and Cellular Biology

Volumn 30, Issue 5, 2010, Pages 1199-1216

  Farrar, Dawn ^a   Rai, Sushma ^a,d   Chernukhin, Igor ^a   Jagodic, Maja ^b,e   Ito, Yoko ^b   Yammine, Samer ^c   Ohlsson, Rolf ^c   Murrell, Adele ^b   Klenova, Elena ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^c KAROLINSKA INSTITUTE   (Sweden)

^d ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF;

ARTICLE; BIOINFORMATICS; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CELL PROLIFERATION; DNA PRIMERS; GENOMIC IMPRINTING; HELA CELLS; HUMANS; HYBRID CELLS; INSULIN-LIKE GROWTH FACTOR II; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA, UNTRANSLATED; TRANSFECTION;

EID: 76749171311     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00827-09     Document Type: Article

References (93)

1. Affar, E. B., P. J. Duriez, R. G. Shah, E. Winstall, M. Germain, C. Boucher, S. Bourassa, J. B. Kirkland, and G. G. Poirier. 1999. Immunological determination and size characterization of poly(ADP-ribose) synthesized in vitro and in vivo. Biochim. Biophys. Acta 1428:137-146.
2. Aguilar-Quesada, R., J. A. Munoz-Gamez, D. Martin-Oliva, A. Peralta-Leal, R. Quiles-Perez, J. M. Rodriguez-Vargas, M. R. de Almodovar, C. Conde, A. Ruiz-Extremera, and F. J. Oliver. 2007. Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr. Med. Chem. 14:1179-1187.
3. Althaus, F. R., and C. Richter. 1987. ADP-ribosylation of proteins. Enzymology and biological significance. Mol. Biol. Biochem. Biophys. 37:1-237.
4. Altmeyer, M., S. Messner, P. O. Hassa, M. Fey, and M. O. Hottiger. 2009. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res. 37:3723-3738.
5. Alvarez-Gonzalez, R., and F. R. Althaus. 1989. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat. Res. 218:67-74.
6. Ame, J. C., C. Spenlehauer, and G. de Murcia. 2004. The PARP superfamily. Bioessays 26:882-893.
7. Awad, T. A., J. Bigler, J. E. Ulmer, Y. J. Hu, J. M. Moore, M. Lutz, P. E. Neiman, S. J. Collins, R. Renkawitz, V. V. Lobanenkov, and G. N. Filippova. 1999. Negative transcriptional regulation mediated by thyroid hormone response element 144 requires binding of the multivalent factor CTCF to a novel target DNA sequence. J. Biol. Chem. 274:27092-27098.
8. Bakondi, E., P. Bai, E. E. Szabo, J. Hunyadi, P. Gergely, C. Szabo, and L. Virag. 2002. Detection of poly(ADP-ribose) polymerase activation in oxidatively stressed cells and tissues using biotinylated NAD substrate. J. Histochem. Cytochem. 50:91-98.
9. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837.
10. Bell, A. C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485.
11. Bell, A. C., A. G. West, and G. Felsenfeld. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387-396.
12. Bergstrom, R., J. Whitehead, S. Kurukuti, and R. Ohlsson. 2007. CTCF regulates asynchronous replication of the imprinted H19/Igf2 domain. Cell Cycle 6:450-454.
13. Birney, E., J. A. Stamatoyannopoulos, A. Dutta, R. Guigo, T. R. Gingeras, E. H. Margulies, Z. Weng, M. Snyder, E. T. Dermitzakis, R. E. Thurman, M. S. Kuehn, C. M. Taylor, S. Neph, C. M. Koch, S. Asthana, A. Malhotra, I. Adzhubei, J. A. Greenbaum, R. M. Andrews, P. Flicek, P. J. Boyle, H. Cao, N. P. Carter, G. K. Clelland, S. Davis, N. Day, P. Dhami, S. C. Dillon, M. O. Dorschner, H. Fiegler, P. G. Giresi, J. Goldy, M. Hawrylycz, A. Haydock, R. Humbert, K. D. James, B. E. Johnson, E. M. Johnson, T. T. Frum, E. R. Rosenzweig, N. Karnani, K. Lee, G. C. Lefebvre, P. A. Navas, F. Neri, S. C. Parker, P. J. Sabo, R. Sandstrom, A. Shafer, D. Vetrie, M. Weaver, S. Wilcox, M. Yu, F. S. Collins, J. Dekker, J. D. Lieb, T. D. Tullius, G. E. Crawford, S. Sunyaev, W. S. Noble, I. Dunham, F. Denoeud, A. Reymond, P. Kapranov, J. Rozowsky, D. Zheng, R. Castelo, A. Frankish, J. Harrow, S. Ghosh, A. Sandelin, I. L. Hofacker, R. Baertsch, D. Keefe, S. Dike, J. Cheng, H. A. Hirsch, E. A. Sekinger, J. Lagarde, J. F. Abril, A. Shahab, C. Flamm, C. Fried, J. Hackermuller, J. Hertel, M. Lindemeyer, K. Missal, A. Tanzer, S. Washietl, J. Korbel, O. Emanuelsson, J. S. Pedersen, N. Holroyd, R. Taylor, D. Swarbreck, N. Matthews, M. C. Dickson, D. J. Thomas, M. T. Weirauch, J. Gilbert, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799-816.
14. Bonicalzi, M. E., J. F. Haince, A. Droit, and G. G. Poirier. 2005. Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when? Cell. Mol. Life Sci. 62:739-750.
15. Braun, S. A., P. L. Panzeter, M. A. Collinge, and F. R. Althaus. 1994. Endoglycosidic cleavage of branched polymers by poly(ADP-ribose) glycohydrolase. Eur. J. Biochem. 220:369-375.
16. Burcin, M., R. Arnold, M. Lutz, B. Kaiser, D. Runge, F. Lottspeich, G. N. Filippova, V. V. Lobanenkov, and R. Renkawitz. 1997. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol. Cell. Biol. 17:1281-1288.
17. Butcher, D. T., and D. I. Rodenhiser. 2007. Epigenetic inactivation of BRCA1 is associated with aberrant expression of CTCF and DNA methyltransferase (DNMT3B) in some sporadic breast tumours. Eur. J. Cancer 43:210-219.
18. Caiafa, P., and J. Zlatanova. 2009. CCCTC-binding factor meets poly(ADPribose) polymerase-1. J. Cell. Physiol. 219:265-270.
19. Chernukhin, I., S. Shamsuddin, S. Y. Kang, R. Bergstrom, Y. W. Kwon, W. Yu, J. Whitehead, R. Mukhopadhyay, F. Docquier, D. Farrar, I. Morrison, M. Vigneron, S. Y. Wu, C. M. Chiang, D. Loukinov, V. Lobanenkov, R. Ohlsson, and E. Klenova. 2007. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol. Cell. Biol. 27:1631-1648.
20. Chernukhin, I. V., S. Shamsuddin, A. F. Robinson, A. F. Carne, A. Paul, A. I. El-Kady, V. V. Lobanenkov, and E. M. Klenova. 2000. Physical and functional interaction between two pluripotent proteins, the Y-box DNA/RNAbinding factor, YB-1, and the multivalent zinc finger factor, CTCF. J. Biol. Chem. 275:29915-29921.
21. Chiarugi, A. 2002. Poly(ADP-ribose) polymerase: killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol. Sci. 23:122-129.
22. Cuddapah, S., R. Jothi, D. E. Schones, T. Y. Roh, K. Cui, and K. Zhao. 2009. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 19:24-32.
23. D'Amours, D., S. Desnoyers, I. D'Silva, and G. G. Poirier. 1999. Poly(ADPribosyl) ation reactions in the regulation of nuclear functions. Biochem. J. 342(Pt. 2):249-268.
24. De La Rosa-Velazquez, I. A., H. Rincon-Arano, L. Benitez-Bribiesca, and F. Recillas-Targa. 2007. Epigenetic regulation of the human retinoblastoma tumor suppressor gene promoter by CTCF. Cancer Res. 67:2577-2585.
25. de Murcia, G., and S. Shall. 2000. From DNA damage and stress signalling to cell death: poly ADP-ribosylation reactions. Oxford University Press, Oxford, United Kingdom.
26. Docquier, F., D. Farrar, V. D'Arcy, I. Chernukhin, A. F. Robinson, D. Loukinov, S. Vatolin, S. Pack, A. Mackay, R. A. Harris, H. Dorricott, M. J. O'Hare, V. Lobanenkov, and E. Klenova. 2005. Heightened expression of CTCF in breast cancer cells is associated with resistance to apoptosis. Cancer Res. 65:5112-5122.
27. Docquier, F., G. X. Kita, D. Farrar, P. Jat, M. O'Hare, I. Chernukhin, S. Gretton, A. Mandal, L. Alldridge, and E. Klenova. 2009. Decreased poly-(ADP-ribosyl)ation of CTCF, a transcription factor, is associated with breast cancer phenotype and cell proliferation. Clin. Cancer Res. 15:5762-5771.
28. Dunn, K. L., and J. R. Davie. 2003. The many roles of the transcriptional regulator CTCF. Biochem. Cell Biol. 81:161-167.
29. El-Kady, A., and E. Klenova. 2005. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett. 579:1424-1434.
30. Faraone-Mennella, M. R. 2005. Chromatin architecture and functions: the role(s) of poly(ADP-RIBOSE) polymerase and poly(ADPribosyl)ation of nuclear proteins. Biochem. Cell Biol. 83:396-404.
31. Filippova, G. N. 2008. Genetics and epigenetics of the multifunctional protein CTCF. Curr. Top. Dev. Biol. 80:337-360.
32. Filippova, G. N., S. Fagerlie, E. M. Klenova, C. Myers, Y. Dehner, G. Goodwin, P. E. Neiman, S. J. Collins, and V. V. Lobanenkov. 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16:2802-2813.
33. Filippova, G. N., C. F. Qi, J. E. Ulmer, J. M. Moore, M. D. Ward, Y. J. Hu, D. I. Loukinov, E. M. Pugacheva, E. M. Klenova, P. E. Grundy, A. P. Feinberg, A. M. Cleton-Jansen, E. W. Moerland, C. J. Cornelisse, H. Suzuki, A. Komiya, A. Lindblom, F. Dorion-Bonnet, P. E. Neiman, H. C. Morse III, S. J. Collins, and V. V. Lobanenkov. 2002. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter tts DNA-binding specificity. Cancer Res. 62:48-52.
34. Fredriksson, S., M. Gullberg, J. Jarvius, C. Olsson, K. Pietras, S. M. Gustafsdottir, A. Ostman, and U. Landegren. 2002. Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20:473-477.
35. Gage, F. H. 2000. Mammalian neural stem cells. Science 287:1433-1438.
36. Gagne, J. P., M. E. Bonicalzi, P. Gagne, M. E. Ouellet, M. J. Hendzel, and G. G. Poirier. 2005. Poly(ADP-ribose) glycohydrolase is a component of the FMRP-associated messenger ribonucleoparticles. Biochem. J. 392:499-509.
37. Gagne, J. P., M. J. Hendzel, A. Droit, and G. G. Poirier. 2006. The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr. Opin. Cell Biol. 18:145-151.
38. Gause, M., C. A. Schaaf, and D. Dorsett. 2008. Cohesin and CTCF: cooperating to control chromosome conformation? Bioessays 30:715-718.
39. Gondor, A., and R. Ohlsson. 2008. Chromatin insulators and cohesins. EMBO Rep. 9:327-329.
40. Guastafierro, T., B. Cecchinelli, M. Zampieri, A. Reale, G. Riggio, O. Sthandier, G. Zupi, L. Calabrese, and P. Caiafa. 2008. CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. J. Biol. Chem. 283:21873-21880.
41. Haince, J. F., S. Kozlov, V. L. Dawson, T. M. Dawson, M. J. Hendzel, M. F. Lavin, and G. G. Poirier. 2007. Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J. Biol. Chem. 282: 16441-16453.
42. Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancerblocking activity at the H19/Igf2 locus. Nature 405:486-489.
43. Hassa, P. O., S. S. Haenni, M. Elser, and M. O. Hottiger. 2006. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol. Mol. Biol. Rev. 70:789-829.
44. Hassa, P. O., and M. O. Hottiger. 2008. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci. 13:3046-3082.
45. Kanai, M., K. Hanashiro, S. H. Kim, S. Hanai, A. H. Boulares, M. Miwa, and K. Fukasawa. 2007. Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nat. Cell Biol. 9:1175-1183.
46. Kanduri, C., V. Pant, D. Loukinov, E. Pugacheva, C. F. Qi, A. Wolffe, R. Ohlsson, and V. V. Lobanenkov. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10:853-856.
47. Kawamitsu, H., H. Hoshino, H. Okada, M. Miwa, H. Momoi, and T. Sugimura. 1984. Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry 23:3771-3777.
48. Keil, C., T. Grobe, and S. L. Oei. 2006. MNNG-induced cell death is controlled by interactions between PARP-1, poly(ADP-ribose) glycohydrolase, and XRCC1. J. Biol. Chem. 281:34394-34405.
49. Kim, J. H., T. Ebersole, N. Kouprina, V. N. Noskov, J. I. Ohzeki, H. Masumoto, B. Mravinac, B. A. Sullivan, A. Pavlicek, S. Dovat, S. D. Pack, Y. W. Kwon, P. T. Flanagan, D. Loukinov, V. Lobanenkov, and V. Larionov. 2009. Human gamma-satellite DNA maintains open chromatin structure and protects a transgene from epigenetic silencing. Genome Res. 19:533-544.
50. Kim, T. H., Z. K. Abdullaev, A. D. Smith, K. A. Ching, D. I. Loukinov, R. D. Green, M. Q. Zhang, V. V. Lobanenkov, and B. Ren. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128:1231-1245.
51. Kleine, H., E. Poreba, K. Lesniewicz, P. O. Hassa, M. O. Hottiger, D. W. Litchfield, B. H. Shilton, and B. Luscher. 2008. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol. Cell 32:57-69.
52. Klenova, E., and R. Ohlsson. 2005. Poly(ADP-ribosyl)ation and epigenetics. Is CTCF PARt of the plot? Cell Cycle 4:96-101.
53. Klenova, E. M., I. V. Chernukhin, A. El-Kady, R. E. Lee, E. M. Pugacheva, D. I. Loukinov, G. H. Goodwin, D. Delgado, G. N. Filippova, J. Leon, H. C. Morse III, P. E. Neiman, and V. V. Lobanenkov. 2001. Functional phosphorylation sites in the C-terminal region of the multivalent multifunctional transcriptional factor CTCF. Mol. Cell. Biol. 21:2221-2234.
54. Klenova, E. M., H. C. Morse III, R. Ohlsson, and V. V. Lobanenkov. 2002. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol. 12:399-414.
55. Klenova, E. M., R. H. Nicolas, H. F. Paterson, A. F. Carne, C. M. Heath, G. H. Goodwin, P. E. Neiman, and V. V. Lobanenkov. 1993. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol. Cell. Biol. 13:7612-7624.
56. Koesters, C., B. Unger, I. Bilic, U. Schmidt, S. Bluml, B. Lichtenberger, M. Schreiber, J. Stockl, and W. Ellmeier. 2007. Regulation of dendritic cell differentiation and subset distribution by the zinc finger protein CTCF. Immunol. Lett. 109:165-174.
57. Kraus, W. L. 2008. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol. 20:294-302.
58. Kraus, W. L., and J. T. Lis. 2003. PARP goes transcription. Cell 113:677-683.
59. Krishnakumar, R., M. J. Gamble, K. M. Frizzell, J. G. Berrocal, M. Kininis, and W. L. Kraus. 2008. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319:819-821.
60. Lautier, D., J. Lagueux, J. Thibodeau, L. Menard, and G. G. Poirier. 1993. Molecular and biochemical features of poly(ADP-ribose) metabolism. Mol. Cell. Biochem. 122:171-193.
61. Li, T., and L. Lu. 2005. Epidermal growth factor-induced proliferation requires down-regulation of Pax6 in corneal epithelial cells. J. Biol. Chem. 280:12988-12995.
62. Lobanenkov, V. V., R. H. Nicolas, V. V. Adler, H. Paterson, E. M. Klenova, A. V. Polotskaja, and G. H. Goodwin. 1990. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5′-flanking sequence of the chicken c-myc gene. Oncogene 5:1743-1753.
63. Lutz, M., L. J. Burke, P. LeFevre, F. A. Myers, A. W. Thorne, C. Crane-Robinson, C. Bonifer, G. N. Filippova, V. Lobanenkov, and R. Renkawitz. 2003. Thyroid hormone-regulated enhancer blocking: cooperation of CTCF and thyroid hormone receptor. EMBO J. 22:1579-1587.
64. MacPherson, M. J., L. G. Beatty, W. Zhou, M. Du, and P. D. Sadowski. 2009. The CTCF insulator protein is posttranslationally modified by SUMO. Mol. Cell. Biol. 29:714-725.
65. Manders, M. M., P. J. Verbeek, and J. A. Aten. 1993. Measurement of co-localization of objects in dual colour confocal images. J. Microsc. 169: 375-382.
66. Miller, F. 1972. Glycopeptides of human immunoglobulins. 3. The use and preparation of specific glycosidases. Immunochemistry 9:217-228.
67. Mitsuya, K., M. Meguro, H. Sui, T. C. Schulz, H. Kugoh, H. Hamada, and M. Oshimura. 1998. Epigenetic reprogramming of the human H19 gene in mouse embryonic cells does not erase the primary parental imprint. Genes Cells 3:245-255.
68. Miwa, M., and M. Masutani. 2007. PolyADP-ribosylation and cancer. Cancer Sci. 98:1528-1535.
69. Miwa, M., N. Saikawa, Z. Yamaizumi, S. Nishimura, and T. Sugimura. 1979. Structure of poly(adenosine diphosphate ribose): identification of 2′-[1″-ribosyl-2″-(or 3″-)(1‴-ribosyl)]adenosine- 5′,5″,5‴-tris(phosphate) as a branch linkage. Proc. Natl. Acad. Sci. U. S. A. 76:595-599.
70. Monaco, L., U. Kolthur-Seetharam, R. Loury, J. M. Murcia, G. de Murcia, and P. Sassone-Corsi. 2005. Inhibition of Aurora-B kinase activity by poly-(ADP-ribosyl)ation in response to DNA damage. Proc. Natl. Acad. Sci. U. S. A. 102:14244-14248.
71. Mukhopadhyay, R., W. Yu, J. Whitehead, J. Xu, M. Lezcano, S. Pack, C. Kanduri, M. Kanduri, V. Ginjala, A. Vostrov, W. Quitschke, I. Chernukhin, E. Klenova, V. Lobanenkov, and R. Ohlsson. 2004. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genome-wide. Genome Res. 14:1594-1602.
72. Ohlsson, R., R. Renkawitz, and V. Lobanenkov. 2001. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 17:520-527.
73. Okazaki, I. J., and J. Moss. 1996. Mono-ADP-ribosylation: a reversible posttranslational modification of proteins. Adv. Pharmacol. 35:247-280.
74. Phillips, J. E., and V. G. Corces. 2009. CTCF: master weaver of the genome. Cell 137:1194-1211.
75. Pugacheva, E. M., V. K. Tiwari, Z. Abdullaev, A. A. Vostrov, P. T. Flanagan, W. W. Quitschke, D. I. Loukinov, R. Ohlsson, and V. V. Lobanenkov. 2005. Familial cases of point mutations in the XIST promoter reveal a correlation between CTCF binding and pre-emptive choices of X chromosome inactivation. Hum. Mol. Genet. 14:953-965.
76. Qi, C. F., A. Martensson, M. Mattioli, R. Dalla-Favera, V. V. Lobanenkov, and H. C. Morse III. 2003. CTCF functions as a critical regulator of cell-cycle arrest and death after ligation of the B cell receptor on immature B cells. Proc. Natl. Acad. Sci. U. S. A. 100:633-638.
77. Rasko, J. E., E. M. Klenova, J. Leon, G. N. Filippova, D. I. Loukinov, S. Vatolin, A. F. Robinson, Y. J. Hu, J. Ulmer, M. D. Ward, E. M. Pugacheva, P. E. Neiman, H. C. Morse III, S. J. Collins, and V. V. Lobanenkov. 2001. Cell growth inhibition by the multifunctional multivalent zinc-finger factor CTCF. Cancer Res. 61:6002-6007.
78. Recillas-Targa, F., I. A. De La Rosa-Velazquez, E. Soto-Reyes, and L. Benitez-Bribiesca. 2006. Epigenetic boundaries of tumour suppressor gene promoters: the CTCF connection and its role in carcinogenesis. J. Cell. Mol. Med. 10:554-568.
79. Rossi, L., M. Denegri, M. Torti, G. G. Poirier, and A. Ivana Scovassi. 2002. Poly(ADP-ribose) degradation by post-nuclear extracts from human cells. Biochimie 84:1229-1235.
80. Schreiber, V., F. Dantzer, J. C. Ame, and G. de Murcia. 2006. Poly(ADPribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7:517-528.
81. Simbulan-Rosenthal, C. M., D. S. Rosenthal, R. B. Luo, R. Samara, M. Jung, A. Dritschilo, A. Spoonde, and M. E. Smulson. 2001. Poly(ADP-ribosyl)ation of p53 in vitro and in vivo modulates binding to its DNA consensus sequence. Neoplasia 3:179-188.
82. Szabo, P., S. H. Tang, A. Rentsendorj, G. P. Pfeifer, and J. R. Mann. 2000. Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function. Curr. Biol. 10:607-610.
83. Torrano, V., I. Chernukhin, F. Docquier, V. D'Arcy, J. Leon, E. Klenova, and M. D. Delgado. 2005. CTCF regulates growth and erythroid differentiation of human myeloid leukemia cells. J. Biol. Chem. 280:28152-28161.
84. Torrano, V., J. Navascues, F. Docquier, R. Zhang, L. J. Burke, I. Chernukhin, D. Farrar, J. Leon, M. T. Berciano, R. Renkawitz, E. Klenova, M. Lafarga, and M. D. Delgado. 2006. Targeting of CTCF to the nucleolus inhibits nucleolar transcription through a poly(ADP-ribosyl)ation-dependent mechanism. J. Cell Sci. 119:1746-1759.
85. Virag, L., and C. Szabo. 2002. The therapeutic potential of poly(ADPribose) polymerase inhibitors. Pharmacol. Rev. 54:375-429.
86. Vostrov, A. A., and W. W. Quitschke. 1997. The zinc finger protein CTCF binds to the APBβ domain of the amyloid beta-protein precursor promoter. Evidence for a role in transcriptional activation. J. Biol. Chem. 272:33353-33359.
87. Wacker, D. A., K. M. Frizzell, T. Zhang, and W. L. Kraus. 2007. Regulation of chromatin structure and chromatin-dependent transcription by poly-(ADP-ribose) polymerase-1: possible targets for drug-based therapies. Subcell. Biochem. 41:45-69.
88. Wallace, J. A., and G. Felsenfeld. 2007. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17:400-407.
89. Wesierska-Gadek, J., and G. Schmid. 2001. Poly(ADP-ribose) polymerase-1 regulates the stability of the wild-type p53 protein. Cell. Mol. Biol. Lett. 6:117-140.
90. Wielckens, K., R. Bredehorst, P. Adamietz, and H. Hilz. 1982. Mono ADP-ribosylation and poly ADP-ribosylation of proteins in normal and malignant tissues. Adv. Enzyme Regul. 20:23-37.
91. Witcher, M., and B. M. Emerson. 2009. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol. Cell 34:271-284.
92. Yu, W., V. Ginjala, V. Pant, I. Chernukhin, J. Whitehead, F. Docquier, D. Farrar, G. Tavoosidana, R. Mukhopadhyay, C. Kanduri, M. Oshimura, A. P. Feinberg, V. Lobanenkov, E. Klenova, and R. Ohlsson. 2004. Poly(ADP-ribosyl) ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 36:1105-1110.
93. Yusufzai, T. M., H. Tagami, Y. Nakatani, and G. Felsenfeld. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13:291-298.