Identification of CTCF as a master regulator of the clustered protocadherin genes

Nucleic Acids Research

Volumn 40, Issue 8, 2012, Pages 3378-3391

  Golan Mashiach, Michal ^a   Grunspan, Moshe ^a   Emmanuel, Rafi ^a   Gibbs Bar, Liron ^a   Dikstein, Rivka ^a   Shapiro, Ehud ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CCTC BINDING FACTOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONSERVED SEQUENCE ELEMENT; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; HUMAN; HUMAN CELL; NERVE CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PURIFICATION; PROTOCADHERIN GENE; SPECIFIC SEQUENCE ELEMENT; TRANSCRIPTION INITIATION;

BASE SEQUENCE; CADHERINS; CELL LINE; CONSERVED SEQUENCE; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84860376812     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1260     Document Type: Article

References (64)

1. Lomvardas, S., Barnea, G., Pisapia, D., Mendelsohn, M., Kirkland, J. and Axel, R. (2006) Interchromosomal interactions and olfactory receptor choice. Cell, 126, 403-413.
2. Schmucker, D., Clemens, J., Shu, H., Worby, C., Xiao, J., Muda, M., Dixon, J. and Zipursky, S. (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell, 101, 671-684.
3. Wojtowicz, W.M., Flanagan, J.J., Millard, S.S., Zipursky, S.L. and Clemens, J.C. (2004) Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell, 118, 619-633.
4. Hattori, D., Demir, E., Kim, H., Viragh, E., Zipursky, S. and Dickson, B. (2007) Dscam diversity is essential for neuronal wiring and self-recognition. Nature, 449, 223-227.
5. Hamada, S. and Yagi, T. (2001) The cadherin-related neuronal receptor family: a novel diversified cadherin family at the synapse. Neurosci. Res., 41, 207-215.
6. Shapiro, L. and Colman, D.R. (1999) The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron, 23, 427-430.
7. Serafini, T. (1999) Finding a partner in a crowd: neuronal diversity and synaptogenesis. Cell, 98, 133-136.
8. Yagi, T. and Takeichi, M. (2000) Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev., 14, 1169-1180.
9. Emond, M. and Jontes, J. (2008) Inhibition of protocadherin-alpha function results in neuronal death in the developing zebrafish. Dev. Biol., 321, 175-187.
10. Phillips, G.R., Tanaka, H., Frank, M., Elste, A., Fidler, L., Benson, D.L. and Colman, D.R. (2003) Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J. Neurosci., 23, 5096-5104.
11. Weiner, J., Wang, X., Tapia, J. and Sanes, J. (2005) Gamma protocadherins are required for synaptic development in the spinal cord. Proc. Natl Acad. Sci. USA, 102, 8-14.
12. Kohmura, N., Senzaki, K., Hamada, S., Kai, N., Yasuda, R., Watanabe, M., Ishii, H., Yasuda, M., Mishina, M. and Yagi, T. (1998) Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron, 20, 1137-1151.
13. Wu, Q. and Maniatis, T. (1999) A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell, 97, 779-790.
14. Wang, X., Weiner, J.A., Levi, S., Craig, A.M., Bradley, A. and Sanes, J.R. (2002) Gamma protocadherins are required for survival of spinal interneurons. Neuron, 36, 843-854.
15. Blank, M., Triana-Baltzer, G., Richards, C. and Berg, D. (2004) Alpha-protocadherins are presynaptic and axonal in nicotinic pathways. Mol. Cell. Neurosci., 26, 530-543.
16. Frank, M., Ebert, M., Shan, W., Phillips, G.R., Arndt, K., Colman, D.R. and Kemler, R. (2005) Differential expression of individual gamma-protocadherins during mouse brain development. Mol. Cell. Neurosci., 29, 603-616.
17. Zou, C., Huang, W., Ying, G. and Wu, Q. (2007) Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires. Neuroscience, 144, 579-603.
18. Fukuda, E., Hamada, S., Hasegawa, S., Katori, S., Sanbo, M., Miyakawa, T., Yamamoto, T., Yamamoto, H., Hirabayashi, T. and Yagi, T. (2008) Down-regulation of protocadherin-alpha A isoforms in mice changes contextual fear conditioning and spatial working memory. Eur. J. Neurosci., 28, 1362-1376.
19. Katori, S., Hamada, S., Noguchi, Y., Fukuda, E., Yamamoto, T., Yamamoto, H., Hasegawa, S. and Yagi, T. (2009) Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. J. Neurosci., 29, 9137-9147.
20. Sugino, H., Hamada, S., Yasuda, R., Tuji, A., Matsuda, Y., Fujita, M. and Yagi, T. (2000) Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics, 63, 75-87.
21. Wu, Q., Zhang, T., Cheng, J., Kim, Y., Grimwood, J., Schmutz, J., Dickson, M., Noonan, J., Zhang, M., Myers, R. et al. (2001) Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Res., 11, 389-404.
22. Esumi, S., Kakazu, N., Taguchi, Y., Hirayama, T., Sasaki, A., Hirabayashi, T., Koide, T., Kitsukawa, T., Hamada, S. and Yagi, T. (2005) Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nat. Genet., 37, 171-176.
23. Kaneko, R., Kato, H., Kawamura, Y., Esumi, S., Hirayama, T., Hirabayashi, T. and Yagi, T. (2006) Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. J. Biol. Chem., 281, 30551-30560.
24. Zhang, T., Haws, P. and Wu, Q. (2004) Multiple variable first exons: a mechanism for cell-and tissue-specific gene regulation. Genome Res., 14, 79-89.
25. Wu, Q. and Maniatis, T. (2000) Large exons encoding multiple ectodomains are a characteristic feature of protocadherin genes. Proc. Natl Acad. Sci. USA, 97, 3124-3129.
26. Tasic, B., Nabholz, C.E., Baldwin, K.K., Kim, Y., Rueckert, E.H., Ribich, S.A., Cramer, P., Wu, Q., Axel, R. and Maniatis, T. (2002) Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol. Cell, 10, 21-33.
27. Wang, X., Su, H. and Bradley, A. (2002) Molecular mechanisms governing Pcdh-gamma gene expression: evidence for a multiple promoter and cis-alternative splicing model. Genes Dev., 16, 1890-1905.
28. Ribich, S., Tasic, B. and Maniatis, T. (2006) Identification of long-range regulatory elements in the protocadherin-alpha gene cluster. Proc. Natl Acad. Sci. USA, 103, 19719-19724.
29. Kawaguchi, M., Toyama, T., Kaneko, R., Hirayama, T., Kawamura, Y. and Yagi, T. (2008) Relationship between DNA methylation states and transcription of individual isoforms encoded by the protocadherin-alpha gene cluster. J. Biol. Chem., 283, 12064-12075.
30. Murata, Y., Hamada, S., Morishita, H., Mutoh, T. and Yagi, T. (2004) Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha. J. Biol. Chem., 279, 49508-49516.
31. Amir-Zilberstein, L., Ainbinder, E., Toube, L., Yamaguchi, Y., Handa, H. and Dikstein, R. (2007) Differential regulation of NF-kappaB by elongation factors is determined by core promoter type. Mol. Cell Biol., 27, 5246-5259.
32. Amir-Zilberstein, L. and Dikstein, R. (2008) Interplay between E-box and NF-kappaB in regulation of A20 gene by DRB sensitivity-inducing factor (DSIF). J. Biol. Chem., 283, 1317-1323.
33. Kurukuti, S., Tiwari, V.K., Tavoosidana, G., Pugacheva, E., Murrell, A., Zhao, Z., Lobanenkov, V., Reik, W. and Ohlsson, R. (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc. Natl Acad. Sci. USA, 103, 10684-10689.
34. Hancock, A.L., Brown, K.W., Moorwood, K., Moon, H., Holmgren, C., Mardikar, S.H., Dallosso, A.R., Klenova, E., Loukinov, D., Ohlsson, R. et al. (2007) A CTCF-binding silencer regulates the imprinted genes AWT1 and WT1-AS and exhibits sequential epigenetic defects during Wilms' tumourigenesis. Hum. Mol. Genet., 16, 343-354.
35. Noonan, J.P., Li, J., Nguyen, L., Caoile, C., Dickson, M., Grimwood, J., Schmutz, J., Feldman, M.W. and Myers, R.M. (2003) Extensive linkage disequilibrium, a common 16.7-kilobase deletion, and evidence of balancing selection in the human protocadherin alpha cluster. Am. J. Hum. Genet., 72, 621-635.
36. Noonan, J.P., Grimwood, J., Schmutz, J., Dickson, M. and Myers, R.M. (2004) Gene conversion and the evolution of protocadherin gene cluster diversity. Genome Res., 14, 354-366.
37. Sakamoto, S., Kabe, Y., Hatakeyama, M., Yamaguchi, Y. and Handa, H. (2009) Development and application of high-performance affinity beads: toward chemical biology and drug discovery. Chem. Rec., 9, 66-85.
38. Handoko, L., Xu, H., Li, G., Ngan, C.Y., Chew, E., Schnapp, M., Lee, C.W., Ye, C., Ping, J.L., Mulawadi, F. et al. (2011) CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet., 43, 630-638.
39. Filippova, G.N., Fagerlie, S., Klenova, E.M., Myers, C., Dehner, Y., Goodwin, G., Neiman, P.E., Collins, S.J. and Lobanenkov, V.V. (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.
40. Kosaka-Suzuki, N., Suzuki, T., Pugacheva, E.M., Vostrov, A.A., Morse, H.C., Loukinov, D. and Lobanenkov, V. (2011) Transcription factor BORIS (Brother of the Regulator of Imprinted Sites) directly induces expression of a cancer-testis antigen, TSP50, through regulated binding of BORIS to the promoter. J. Biol. Chem., 286, 27378-27388.
41. Renaud, S., Pugacheva, E.M., Delgado, M.D., Braunschweig, R., Abdullaev, Z., Loukinov, D., Benhattar, J. and Lobanenkov, V. (2007) Expression of the CTCF-paralogous cancer-testis gene, brother of the regulator of imprinted sites (BORIS), is regulated by three alternative promoters modulated by CpG methylation and by CTCF and p53 transcription factors. Nucleic Acids Res., 35, 7372-7388.
42. Ohlsson, R., Renkawitz, R. and Lobanenkov, V. (2001) CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet., 17, 520-527.
43. Gaszner, M. and Felsenfeld, G. (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet., 7, 703-713.
44. Filippova, G.N. (2008) Genetics and epigenetics of the multifunctional protein CTCF. Curr. Top. Dev. Biol., 80, 337-360.
45. Klenova, E.M., Morse, H.C., Ohlsson, R. and Lobanenkov, V.V. (2002) The novel BORIS+CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol., 12, 399-414.
46. Shu, W., Chen, H., Bo, X. and Wang, S. (2011) Genome-wide analysis of the relationships between DNaseI HS, histone modifications and gene expression reveals distinct modes of chromatin domains. Nucleic Acids Res., 39, 7428-7443.
47. Bell, A.C., West, A.G. and Felsenfeld, G. (1999) The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell, 98, 387-396.
48. Liu, Z., Scannell, D.R., Eisen, M.B. and Tjian, R. (2011) Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell, 146, 720-731.
49. 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. (2008) CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J., 27, 2839-2850.
50. Splinter, E., Heath, H., Kooren, J., Palstra, R.J., Klous, P., Grosveld, F., Galjart, N. and de Laat, W. (2006) CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev., 20, 2349-2354.
51. Soshnikova, N., Montavon, T., Leleu, M., Galjart, N. and Duboule, D. (2010) Functional analysis of CTCF during mammalian limb development. Dev. Cell, 19, 819-830.
52. Donohoe, M.E., Zhang, L.F., Xu, N., Shi, Y. and Lee, J.T. (2007) Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol. Cell, 25, 43-56.
53. Tempera, I., Wiedmer, A., Dheekollu, J. and Lieberman, P.M. (2010) CTCF prevents the epigenetic drift of EBV latency promoter Qp. PLoS Pathog., 6, e1001048.
54. Weth, O. and Renkawitz, R. (2011) CTCF function is modulated by neighboring DNA binding factors. Biochem Cell Biol., 89, 459-468.
55. Gordon, S., Akopyan, G., Garban, H. and Bonavida, B. (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene, 25, 1125-1142.
56. Kim, T.H., Abdullaev, Z.K., Smith, A.D., Ching, K.A., Loukinov, D.I., Green, R.D., Zhang, M.Q., Lobanenkov, V.V. and Ren, B. (2007) Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell, 128, 1231-1245.
57. Kehayova, P., Monahan, K., Chen, W. and Maniatis, T. (2011) Regulatory elements required for the activation and repression of the protocadherin-alpha gene cluster. Proc. Natl Acad. Sci. USA, 108, 17195-17200.
58. Yokota, S., Hirayama, T., Hirano, K., Kaneko, R., Toyoda, S., Kawamura, Y., Hirabayashi, M., Hirabayashi, T. and Yagi, T. (2011) Identification of the cluster control region for the protocadherin-{beta} genes located beyond the protocadherin-{gamma} cluster. J. Biol. Chem., 286, 31885-31895.
59. Ohlsson, R., Lobanenkov, V. and Klenova, E. (2010) Does CTCF mediate between nuclear organization and gene expression? Bioessays, 32, 37-50.
60. Phillips, J.E. and Corces, V.G. (2009) CTCF: master weaver of the genome. Cell, 137, 1194-1211.
61. Morrow, E., Yoo, S., Flavell, S., Kim, T., Lin, Y., Hill, R., Mukaddes, N., Balkhy, S., Gascon, G., Hashmi, A. et al. (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science, 321, 218-223.
62. Pedrosa, E., Stefanescu, R., Margolis, B., Petruolo, O., Lo, Y., Nolan, K., Novak, T., Stopkova, P. and Lachman, H. (2008) Analysis of protocadherin alpha gene enhancer polymorphism in bipolar disorder and schizophrenia. Schizophr. Res., 102, 210-219.
63. Zheng, Q., Yu, H., Washington.J.L. 3rd, Kisley, L., Kikkawa, Y., Pawlowski, K., Wright, C. and Alagramam, K. (2006) A new spontaneous mutation in the mouse protocadherin 15 gene. Hear Res., 219, 110-120.
64. Dallosso, A., Hancock, A., Szemes, M., Moorwood, K., Chilukamarri, L., Tsai, H., Sarkar, A., Barasch, J., Vuononvirta, R., Jones, C. et al. (2009) Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Genet., 5, e1000745.