Nucleosome exclusion from the interspecies-conserved central AT-rich region of the Ars insulator

Journal of Biochemistry

Volumn 151, Issue 1, 2012, Pages 75-87

  Takagi, Haruna ^a   Inai, Yuta ^a   Watanabe, Shun Ichiro ^a   Tatemoto, Sayuri ^a   Yajima, Mamiko ^b   Akasaka, Koji ^c   Yamamoto, Takashi ^a   Sakamoto, Naoaki ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

insulator; nuclease hypersensitive site; nucleosome; sea urchin development

Indexed keywords

ARYLSULFATASE; ARYLSULFATASE INSULATOR; DIETHYL PYROCARBONATE; MICROCOCCAL NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; AT RICH SEQUENCE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA STRUCTURE; EMBRYO; ENZYME ACTIVE SITE; GENETIC CONSERVATION; HYPERSENSITIVITY; MOLECULAR MECHANICS; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; SEA URCHIN; SPECIES COMPARISON; STRONGYLOCENTROTUS;

ANIMALS; ARYLSULFATASES; AT RICH SEQUENCE; BASE SEQUENCE; BINDING SITES; CELL NUCLEUS; CHROMATIN; CONSERVED SEQUENCE; DEOXYRIBONUCLEASES; DNA; DNA-DIRECTED DNA POLYMERASE; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMICENTROTUS; HISTONES; INSULATOR ELEMENTS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; STRONGYLOCENTROTUS PURPURATUS;

ECHINOIDEA; HEMICENTROTUS PULCHERRIMUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 84855245511     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr118     Document Type: Article

References (59)

1. West, A.G., Gaszner, M., and Felsenfeld, G. (2002) Insulators: many functions, many mechanisms. Genes Dev. 16, 271-288 (Pubitemid 34111407)
2. Geyer, P.K. and Clark, I. (2002) Protecting against promiscuity: the regulatory role of insulators. Cell. Mol. Life Sci. 59, 2112-2127 (Pubitemid 36140284)
3. Valenzuela, L. and Kamakaka, R.T. (2006) Chromatin insulators. Annu. Rev. Genet. 40, 107-138 (Pubitemid 44956781)
4. Chung, J.H., Whiteley, M., and Felsenfeld, G. (1993) A 50 element of the chicken b-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74, 505-514 (Pubitemid 23244616)
5. West, A.G., Huang, S., Gaszner, M., Litt, M.D., and Felsenfeld, G. (2004) Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16, 453-463 (Pubitemid 39504798)
6. 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 (Pubitemid 29380573)
7. Gdula, D.A., Gerasimova, T.I., and Corces, V.G. (1996) Genetic and molecular analysis of the gypsy chromatin insulator of Drosophila. Proc. Natl Acad. Sci. USA 93, 9378-9383 (Pubitemid 26296615)
8. Spana, C. and Corces, V.G. (1990) DNA bending is a determinant of binding specificity for a Drosophila zinc finger protein. Genes Dev. 4, 1505-1515
9. Dorn, R., Krauss, V., Reuter, G., and Saumweber, H. (1993) The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc. Natl Acad. Sci. USA 90, 11376-11380 (Pubitemid 23354432)
10. Gerasimova, T.I., Gdula, D.A., Gerasimov, D.V., Simonova, O., and Corces, V.G. (1995) A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 82, 587-597
11. Pai, C.Y., Lei, E.P., Ghosh, D., and Corces, V.G. (2004) The Centrosomal Protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell 16, 737-748 (Pubitemid 39586532)
12. Chen, S. and Corces, V.G. (2001) The gypsy insulator of Drosophila affects chromatin structure in a directional manner. Genetics 159, 1649-1658 (Pubitemid 34087604)
13. Gaszner, M., Vazquez, J., and Schedl, P. (1999) The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev. 13, 2098-2107 (Pubitemid 29407350)
14. Zhao, K., Hart, C.M., and Laemmli, U.K. (1995) Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81, 879-889
15. Hart, C.M., Zhao, K., and Laemmli, U.K. (1997) The scs' boundary element: characterization of boundary element-associated factors. Mol. Cell. Biol. 17, 999-1009 (Pubitemid 27044398)
16. Cuvier, O., Hart, C.M., and Laemmli, U.K. (1998) Identification of a class of chromatin boundary elements. Mol. Cell. Biol. 18, 7478-7486 (Pubitemid 28533066)
17. Cuvier, O., Hart, C.M., Kas, E., and Laemmli, U.K. (2002) Identification of a multicopy chromatin boundary element at the borders of silenced chromosomal domains. Chromosoma 110, 519-531 (Pubitemid 34192937)
18. Udvardy, A. and Schedl, P. (1993) The dynamics of chromatin condensation: redistribution of topoisomerase II in the 87A7 heat shock locus during induction and recovery. Mol. Cell. Biol. 13, 7522-7530 (Pubitemid 23354277)
19. Kanduri, M., Kanduri, C., Mariano, P., Vostrov, A.A., Quitschke, W., Lobanenkov, V., and Ohlsson, R. (2002) Multiple nucleosome positioning sites regulate the CTCF-mediated insulator function of the H19 imprinting control region. Mol. Cell. Biol. 22, 3339-3344 (Pubitemid 34453975)
20. Sasaki, H., Yamada, K., Akasaka, K., Kawasaki, H., Suzuki, K., Saito, A., Sato, M., and Shimada, H. (1988) cDNA cloning, nucleotide sequence and expression of the gene for arylsulfatase in the sea urchin (Hemicentrotus pulcherrimus) embryo. Eur. J. Biochem. 177, 9-13
21. Akasaka, K., Ueda, T., Higashinakagawa, T., Yamada, K., and Shimada, H. (1990) Spatial patterns of arylsulfatase mRNA expression in sea urchin embryo. Dev. Growth Differ. 32, 9-13 (Pubitemid 20166903)
22. Akasaka, K., Nishimura, A., Takata, K., Mitsunaga, K., Mibuka, F., Ueda, H., Hirose, S., Tsutsui, K., and Shimada, H. (1999) Upstream element of the sea urchin arylsulfatase gene serves as an insulator. Cell. Mol. Biol. (Noisy-le-grand) 45, 555-565
23. Yajima, M., Kiyomoto, M., and Akasaka, K. (2007) Ars insulator protects transgenes from long-term silencing in sea urchin larva. Dev. Genes Evol. 217, 331-336 (Pubitemid 46510909)
24. Nagaya, S., Yoshida, K., Kato, K., Akasaka, K., and Shinmyo, A. (2001) An insulator element from the sea urchin Hemicentrotus pulcherrimus suppresses variation in transgene expression in cultured tobacco cells. Mol. Genet. Genomics 265, 405-413
25. Hino, S., Fan, J., Taguwa, S., Akasaka, K., and Matsuoka, M. (2004) Sea urchin insulator protects lentiviral vector from silencing by maintaining active chromatin structure. Gene Ther. 11, 819-828 (Pubitemid 38714585)
26. Moritani, K., Tagashira, H., Shimotori, T., Sakamoto, N., Tanaka, S., Takata, K., Mitsunaga-Nakatsubo, K., Bojiiwa, Y., Yamamoto, T., Shimada, H., and Akasaka, K. (2004) A new G-stretch-DNA-binding protein, Unichrom, displays cell-cycle-dependent expression in sea urchin embryos. Dev. Growth Differ. 46, 335-341 (Pubitemid 39215134)
27. Tagashira, H., Shimotori, T., Sakamoto, N., Katahira, M., Miyanoiri, Y., Yamamoto, T., Mitsunaga-Nakatsubo, K., Shimada, H., Kusunoki, S., and Akasaka, K. (2006) Unichrom, a novel nuclear matrix protein, binds to the Ars insulator and canonical MARs. Zoolog. Sci. 23, 9-21 (Pubitemid 43726650)
28. Tung, L., Morris, G.F., Yager, L.N., and Weinberg, E.S. (1989) Sea urchin early and late H4 histone genes bind a specific transcription factor in a stable preinitiation complex. Mol. Cell. Biol. 9, 1476-1487 (Pubitemid 19095187)
29. Fronk, J., Tank, G.A., and Langmore, J.P. (1990) Chromatin structure of the developmentally regulated early histone genes of the sea urchin Strongylocentrotus purpuratus. Nucleic Acids Res. 18, 5255-5263
30. Tanaka, Y., Tawaramoto-Sasanuma, M., Kawaguchi, S., Ohta, T., Yoda, K., Kurumizaka, H., and Yokoyama, S. (2004) Expression and purification of recombinant human histones. Methods 33, 3-11 (Pubitemid 38369085)
31. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. 3rd edn, pp. 5.23-5.25, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
32. Sakamoto, N., Akasaka, K., Yamamoto, T., and Shimada, H. (1996) A triplex DNA structure of the polypyrimidine: polypurine stretch in the 5' flanking region of the sea urchin arylsulfatase gene. Zoolog. Sci. 13, 105-109 (Pubitemid 126409784)
33. Brown, C.T., Rust, A.G., Clarke, P.J., Pan, Z., Schilstra, M.J., De Buysscher, T., Griffin, G., Wold, B.J., Cameron, R.A., Davidson, E.H., and Bolouri, H. (2002) New computational approaches for analysis of cis-regulatory networks. Dev. Biol. 246, 86-102 (Pubitemid 34625977)
34. Akasaka, K., Nishimura, A., Hijikata, K., Iuchi, Y., Morokuma, J., Takahashi, M., Morikawa, H., and Shimada, H. (1995) Introduction of DNA into sea urchin eggs by particle gun. Mol. Mar. Biol. Biotechnol. 4, 255-261
35. Anderson, O.D., Yu, M., and Wilt, F. (1986) Site and stage specific action of endogenous nuclease and micrococcal nuclease on the histone genes of sea urchin embryos. Dev. Biol. 117, 109-113
36. Simpson, R.T. and Stafford, D.W. (1983) Structural features of a phased nucleosome core particle. Proc. Natl Acad. Sci. USA 80, 51-55
37. Simpson, R.T. and Kü nzler, P. (1979) Chromatin and core particles formed from the inner histones and synthetic polydeoxyribonucleotides of defined sequence. Nucleic Acids Res. 6, 1387-1415
38. Garner, M.M. and Felsenfeld, G. (1987) Effect of Z-DNA on nucleosome placement. J. Mol. Biol. 196, 581-590
39. Ausio, J., Zhou, G., and van Holde, K. (1987) A reexamination of the reported B ! Z DNA transition in nucleosomes reconstituted with poly(dG-m5dC)-poly(dG-m5dC). Biochemistry 26, 5595-5599
40. Casasnovas, J.M. and Azorín, F. (1987) Supercoiled induced transition to the Z-DNA conformation affects the ability of a d(CG/GC)12 sequence to be organized into nucleosome-cores. Nucleic Acids Res. 15, 8899-8918
41. Dayn, A., Samadashwily, G.M., and Mirkin, S.M. (1992) Intramolecular DNA triplexes: unusual sequence requirements and influence on DNA polymerization. Proc. Natl Acad. Sci. USA 89, 11406-11410
42. Yuh, C.H., Brown, C.T., Livi, C.B., Rowen, L., Clarke, P.J., and Davidson, E.H. (2002) Patchy interspecific sequence similarities efficiently identify positive cis-regulatory elements in the sea urchin. Dev. Biol. 246, 148-161 (Pubitemid 34625981)
43. Ochiai, H., Sakamoto, N., Momiyama, A., Akasaka, K., and Yamamoto, T. (2008) Analysis of cis-regulatory elements controlling spatio-temporal expression of T-brain gene in sea urchin, Hemicentrotus pulcherrimus. Mech. Dev. 125, 2-17 (Pubitemid 50009077)
44. Litt, M.D., Simpson, M., Gaszner, M., Allis, C.D., and Felsenfeld, G. (2001) Correlation between histone lysine methylation and developmental changes at the chicken b-globin locus. Science 293, 2453-2455 (Pubitemid 32917326)
45. Litt, M.D., Simpson, M., Recillas-Targa, F., Prioleau, M.N., and Felsenfeld, G. (2001) Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20, 2224-2235 (Pubitemid 32410592)
46. Recillas-Targa, F., Pikaart, M.J., Burgess-Beusse, B., Bell, A.C., Litt, M.D., West, A.G., Gaszner, M., and Felsenfeld, G. (2002) Position-effect protection and enhancer blocking by the chicken b-globin insulator are separable activities. Proc. Natl Acad. Sci. USA 99, 6883-6888 (Pubitemid 34526227)
47. Bode, J., Kohwi, Y., Dickinson, L., Joh, T., Klehr, D., Mielke, C., and Kohwi-Shigematsu, T. (1992) Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science 255, 195-197
48. Nickol, J., Behe, M., and Felsenfel, G. (1982) Effect of the B-Z transition in poly(dG-m5dC)-poly(dG-m5dC) on nucleosome formation. Proc. Natl Acad. Sci. USA 79, 1771-1775 (Pubitemid 12088509)
49. Westin, L., Blomquist, P., Milligan, J.F., and Wrange, O. (1995) Triple helix DNA alters nucleosomal histone-DNA interactions and acts as a nucleosome barrier. Nucleic Acids Res. 23, 2184-2191
50. Espinas, M.L., Jimenez-Garcia, E., Martinez-Balbas, A., and Azorin, F. (1996) Formation of triple-stranded DNA at d(GA-TC)n sequences prevents nucleosome assembly and is hindered by nucleosomes. J. Biol. Chem. 271, 31807-31812 (Pubitemid 26422199)
51. Shimizu, M., Mori, T., Sakurai, T., and Shindo, H. (2000) Destabilization of nucleosomes by an unusual DNA conformation adopted by poly(dA)-poly(dT) tracts in vivo. EMBO J. 19, 3358-3365 (Pubitemid 30428213)
52. Bi, X., Yu, Q., Sandmeier, J.J., and Zou, Y. (2004) Formation of boundaries of transcriptionally silent chromatin by nucleosome-excluding structures. Mol. Cell. Biol. 24, 2118-2131 (Pubitemid 38248950)
53. Cohen, L.H., Newrock, K.M., and Zweidler, A. (1975) Stage-specific switches in histone synthesis during embryogenesis of the sea urchin. Science 190, 994-997
54. Maxson, R., Cohn, R., Kedes, L., and Mohun, T. (1983) Expression and organization of histone genes. Annu. Rev. Genet. 17, 239-277
55. Chambers, S.A., Vaughn, J.P., and Shaw, B.R. (1983) Shortest nucleosomal repeat lengths during sea urchin development are found in two-cell embryos. Biochemistry 22, 5626-5631
56. Clark, S.P., Lewis, C.D., and Felsenfeld, G. (1990) Properties of BGP1, a poly(dG)-binding protein from chicken erythrocytes. Nucleic Acids Res. 18, 5119-5126
57. Fu, Y., Sinha, M., Peterson, C.L., and Weng, Z. (2008) The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet. 4, e1000138
58. Kohwi-Shigematsu, T. and Kohwi, Y. (1991) Detection of triple-helix related structures adopted by poly(dG)-poly(dC) sequences in supercoiled plasmid DNA. Nucleic Acids Res. 19, 4267-4271 (Pubitemid 21912804)
59. Kohwi, Y., Malkhosyan, S.R., and Kohwi-Shigematsu, T. (1992) Intramolecular dG-dG-dC triplex detected in Escherichia coli cells. J. Mol. Biol. 223, 817-822