Distinctive signatures of histone methylation in transcribed coding and noncoding human β-globin sequences

Molecular and Cellular Biology

Volumn 27, Issue 4, 2007, Pages 1271-1279

  Kim, AeRi ^a   Kiefer, Christine M ^b   Dean, Ann ^b,c  

^a Pusan National University   (South Korea)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c MSC 8028 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; HISTONE; INSULATOR FACTOR; PROTEIN CTCF; PROTEIN H3K36ME3; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN STRUCTURE; CHROMOSOME 11; ENZYME MECHANISM; EPIGENETICS; GENE LOCUS; HUMAN; HUMAN CELL; METHYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MODIFICATION; TRANSCRIPTION REGULATION;

ACETYLATION; BASE SEQUENCE; CHROMATIN; DEOXYRIBONUCLEASE I; DNA, INTERGENIC; EPIGENESIS, GENETIC; GLOBINS; HISTONES; HUMANS; K562 CELLS; LYSINE; METHYLATION; OPEN READING FRAMES; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 33846905189     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01684-06     Document Type: Article

References (68)

1. Ashe, H. L., J. Monks, M. Wijgerde, P. Fraser, and N. J. Proudfoot. 1997. Intergenic transcription and transinduction of the human β-globin locus. Genes Dev. 11:2494-2509.
2. Bannister, A. J., R. Schneider, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2005. Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280:17732-17736.
3. 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.
4. Bender, M. A., R. Byron, T. Ragoczy, A. Telling, M. Bulger, and M. Groudine. 2006. Flanking HS-62.5 and 3′ HS1, and regions upstream of the LCR, are not required for beta-globin transcription. Blood 108:1395-1401.
5. Berger, S. L. 2002. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12:142-148.
6. Bernstein, B. E., E. L. Humphrey, R. L. Erlich, R. Schneider, P. Bouman, J. S. Liu, T. Kouzarides, and S. L. Schreiber. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. USA 99:8695-8700.
7. Brinkman, A. B., T. Roelofsen, S. W. Pennings, J. H. Martens, T. Jenuwein, and H. G. Stunnenberg. 2006. Histone modification patterns associated with the human X chromosome. EMBO Rep. 7:628-634.
8. Bulger, M., D. Schubeler, M. A. Bender, J. Hamilton, C. M. Farrell, R. C. Hardison, and M. Groudine. 2003. A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse β-globin locus. Mol. Cell. Biol. 23:5234-5244.
9. Bulger, M., J. H. van Doorninck, N. Saitoh, A. Telling, C. Farrell, M. A. Bender, G. Felsenfeld, R. Axel, M. Groudine, and J. H. von Doorninck. 1999. Conservation of sequence and structure flanking the mouse and human β-globin loci: the β-globin genes are embedded within an array of odorant receptor genes. Proc. Natl. Acad. Sci. USA 96:5129-5134. (Erratum, 96:8307.)
10. Carrozza, M. J., B. Li, L. Florens, T. Suganuma, S. K. Swanson, K. K. Lee, W. J. Shia, S. Anderson, J. Yates, M. P. Washburn, and J. L. Workman. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581-592.
11. Cheng, C., and P. A. Sharp. 2003. RNA polymerase II accumulation in the promoter-proximal region of the dihydrofolate reductase and γ-actin genes. Mol. Cell. Biol. 23:1961-1967.
12. Chung, J. H., A. C. Bell, and G. Felsenfeld. 1997. Characterization of the chicken β-globin insulator. Proc. Natl. Acad. Sci. USA 94:575-580.
13. Dean, A. 2006. On a chromosome far, far away: LCRs and gene regulation. Trends Genet. 22:38-45.
14. Dou, Y., T. A. Milne, A. J. Ruthenburg, S. Lee, J. W. Lee, G. L. Verdine, C. D. Allis, and R. G. Roeder. 2006. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 13:713-719.
15. Edmondson, D. G., J. K. Davie, J. Zhou, B. Mirnikjoo, K. Tatchell, and S. Y. Dent. 2002. Site-specific loss of acetylation upon phosphorylation of histone H3. J. Biol. Chem. 277:29496-29502.
16. Farrell, C. M., A. G. West, and G. Felsenfeld. 2002. Conserved CTCF insulator elements flank the mouse and human β-globin loci. Mol. Cell. Biol. 22:3820-3831.
17. Fischle, W., Y. Wang, and C. D. Allis. 2003. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15:172-183.
18. Forsberg, E. C., K. M. Downs, H. M. Christensen, H. Im, P. A. Nuzzi, and E. H. Bresnick. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 97:14494-14499.
19. Gong, Q. H., J. C. McDowell, and A. Dean. 1996. Essential role of NF-E2 in remodeling of chromatin structure and transcriptional activation of the ε-globin gene in vivo by 5′ hypersensitive site 2 of the β-globin locus control region. Mol. Cell. Biol. 16:6055-6064.
20. Gribnau, J., K. Diderich, S. Pruzina, R. Calzolari, and P. Fraser. 2000. Intergenic transcription and developmental remodeling of chromatin subdomains in the human β-globin locus. Mol. Cell 5:377-386.
21. Haussecker, D., and N. J. Proudfoot. 2005. Dicer-dependent turnover of intergenic transcripts from the human β-globin gene cluster. Mol. Cell. Biol. 25:9724-9733.
22. Hebbes, T. R., A. L. Clayton, A. W. Thorne, and C. Crane-Robinson. 1994. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken β-globin chromosomal domain. EMBO J. 13:1823-1830.
23. Ho, Y., F. Elefant, S. A. Liebhaber, and N. E. Cooke. 2006. Locus control region transcription plays an active role in long-range gene activation. Mol. Cell 23:365-375.
24. Johnson, K. D., and E. H. Bresnick. 2002. Dissecting long-range transcriptional mechanisms by chromatin immunoprecipitation. Methods 26:27-36.
25. Johnson, K. D., H. M. Christensen, B. Zhao, and E. H. Bresnick. 2001. Distinct mechanisms control RNA polymerase II recruitment to a tissue-specific locus control region and a downstream promoter. Mol. Cell 8:465-471.
26. Johnson, K. D., J. A. Grass, C. Park, H. Im, K. Choi, and E. H. Bresnick. 2003. Highly restricted localization of RNA polymerase II within a locus control region of a tissue-specific chromatin domain. Mol. Cell. Biol. 23:6484-6493.
27. Joshi, A. A., and K. Struhl. 2005. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20:971-978.
28. Keogh, M. C., S. K. Kurdistani, S. A. Morris, S. H. Ahn, V. Podolny, S. R. Collins, M. Schuldiner, K. Chin, T. Punna, N. J. Thompson, C. Boone, A. Emili, J. S. Weissman, T. R. Hughes, B. D. Strahl, M. Grunstein, J. F. Greenblatt, S. Buratowski, and N. J. Krogan. 2005. Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593-605.
29. Kim, A., and A. Dean. 2004. Developmental stage differences in chromatin sub-domains of the β-globin locus. Proc. Natl. Acad. Sci. USA 101:7028-7033.
30. Kouzarides, T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:198-209.
31. Krogan, N. J., J. Dover, A. Wood, J. Schneider, J. Heidt, M. A. Boateng, K. Dean, O. W. Ryan, A. Golshani, M. Johnston, J. F. Greenblatt, and A. Shilatifard. 2003. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11:721-729.
32. Krogan, N. J., M. Kim, A. Tong, A. Golshani, G. Cagney, V. Canadien, D. P. Richards, B. K. Beattie, A. Emili, C. Boone, A. Shilatifard, S. Buratowski, and J. Greenblatt. 2003. Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23:4207-4218.
33. Lachner, M., R. J. O'Sullivan, and T. Jenuwein. 2003. An epigenetic road map for histone lysine methylation. J. Cell Sci. 116:2117-2124.
34. Landry, J., A. Sutton, T. Hesman, J. Min, R. M. Xu, M. Johnston, and R. Sternglanz. 2003. Set2-catalyzed methylation of histone H3 represses basal expression of GAL4 in Saccharomyces cerevisiae. Mol. Cell. Biol. 23:5972-5978.
35. Lefevre, P., C. Lacroix, H. Tagoh, M. Hoogenkamp, S. Melnik, R. Ingram, and C. Bonifer. 2005. Differentiation-dependent alterations in histone methylation and chromatin architecture at the inducible chicken lysozyme gene. J. Biol. Chem. 280:27552-27560.
36. Li, B., L. Howe, S. Anderson, J. R. Yates III, and J. L. Workman. 2003. The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278:8897-8903.
37. Litt, M. D., M. Simpson, M. Gaszner, C. D. Allis, and G. Felsenfeld. 2001. Correlation between histone lysine methylation and developmental changes at the chicken β-globin locus. Science 293:2453-2455.
38. Litt, M. D., M. Simpson, F. Recillas-Targa, M. N. Prioleau, and G. Felsenfeld. 2001. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20:2224-2235.
39. Martin, C., and Y. Zhang. 2005. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6:838-849.
40. Masternak, K., N. Peyraud, M. Krawczyk, E. Barras, and W. Reith. 2003. Chromatin remodeling and extragenic transcription at the MHC class II locus control region. Nat. Immunol. 4:132-137.
41. McArthur, M., S. Gerum, and G. Stamatoyannopoulos. 2001. Quantification of DNaseI-sensitivity by real-time PCR: quantitative analysis of DNaseI-hypersensitivity of the mouse beta-globin LCR. J. Mol. Biol. 313:27-34.
42. Morillon, A., N. Karabetsou, A. Nair, and J. Mellor. 2005. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol. Cell 18:723-734.
43. Morris, D. P., G. A. Michelotti, and D. A. Schwinn. 2005. Evidence that phosphorylation of the RNA polymerase II carboxyl-terminal repeats is similar in yeast and humans. J. Biol. Chem. 280:31368-31377.
44. Ng, H. H., F. Robert, R. A. Young, and K. Struhl. 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11:709-719.
45. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
46. Palstra, R. J., B. Tolhuis, E. Splinter, R. Nijmeijer, F. Grosveld, and W. de Laat. 2003. The β-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35:190-194.
47. Plant, K. E., S. J. Routledge, and N. J. Proudfoot. 2001. Intergenic transcription in the human β-globin gene cluster. Mol. Cell. Biol. 21:6507-6514.
48. Rao, B., Y. Shibata, B. D. Strahl, and J. D. Lieb. 2005. Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide. Mol. Cell. Biol. 25:9447-9459.
49. Routledge, S. J., and N. J. Proudfoot. 2002. Definition of transcriptional promoters in the human β-globin locus control region. J. Mol. Biol. 323:601-611.
50. Saitoh, N., A. C. Bell, F. Recillas-Targa, A. G. West, M. Simpson, M. Pikaart, and G. Felsenfeld. 2000. Structural and functional conservation at the boundaries of the chicken β-globin domain. EMBO J. 19:2315-2322.
51. Santos-Rosa, H., R. Schneider, A. J. Bannister, J. Sherriff, B. E. Bernstein, N. C. Emre, S. L. Schreiber, J. Mellor, and T. Kouzarides. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419:407-411.
52. Sawado, T., J. Halow, M. A. Bender, and M. Groudine. 2003. The β-globin locus control region (LCR) functions primarily by enhancing the transition from transcription initiation to elongation. Genes Dev. 17:1009-1018.
53. Schäbeler, D., D. M. MacAlpine, D. Scalzo, C. Wirbelauer, C. Kooperberg, F. van Leeuwen, D. E. Gottschling, L. P. O'Neill, B. M. Turner, J. Delrow, S. P. Bell, and M. Groudine. 2004. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18:1263-1271.
54. Schneider, R., A. J. Bannister, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6:73-77.
55. Sims, R. J., III, K. Nishioka, and D. Reinberg. 2003. Histone lysine methylation: a signature for chromatin function. Trends Genet. 19:629-639.
56. Splinter, E., H. Heath, J. Kooren, R. J. Palstra, P. Klous, F. Grosveld, N. Galjart, and W. de Laat. 2006. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 20:2349-2354.
57. Stamatoyannopoulos, G. 2005. Control of globin gene expression during development and erythroid differentiation. Exp. Hematol. 33:259-271.
58. Stopka, T., D. F. Amanatullah, M. Papetti, and A. I. Skoultchi. 2005. PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J. 24:3712-3723.
59. Strahl, B. D., P. A. Grant, S. D. Briggs, Z. W. Sun, J. R. Bone, J. A. Caldwell, S. Mollah, R. G. Cook, J. Shabanowitz, D. F. Hunt, and C. D. Allis. 2002. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22:1298-1306.
60. Sun, X. J., J. Wei, X. Y. Wu, M. Hu, L. Wang, H. H. Wang, Q. H. Zhang, S. J. Chen, Q. H. Huang, and Z. Chen. 2005. Identification and characterization of a novel human histone H3 lysine 36-specific methyltransferase. J. Biol. Chem. 280:35261-35271.
61. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell 10:1453-1465.
62. Turner, B. M. 2002. Cellular memory and the histone code. Cell 111:285-291.
63. Vakoc, C. R., S. A. Mandat, B. A. Olenchock, and G. A. Blobel. 2005. Histone H3 lysine 9 methylation and HP1γ are associated with transcription elongation through mammalian chromatin. Mol. Cell 19:381-391.
64. Vakoc, C. R., M. M. Sachdeva, H. Wang, and G. A. Blobel. 2006. A profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol. 26:9185-9195.
65. West, A. G., and P. Fraser. 2005. Remote control of gene transcription. Hum. Mol. Genet. 14:R101-R111.
66. Xiao, T., H. Hall, K. O. Kizer, Y. Shibata, M. C. Hall, C. H. Borchers, and B. D. Strahl. 2003. Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17:654-663.
67. 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.
68. Zhao, H., and A. Dean. 2005. Organizing the genome: enhancers and insulators. Biochem. Cell Biol. 83:516-524.