A molecular model of chromatin organisation and transcription: How a multi-RNA polymerase II machine transcribes and remodels the β-globin locus during development

BioEssays

Volumn 31, Issue 12, 2009, Pages 1357-1366

  Wong, Hua ^a,b   Winn, Peter J ^c   Mozziconacci, Julien ^b,d  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

globin; Chromatin; Development; Locus control region; Transcription

Indexed keywords

BETA GLOBIN; DNA; RNA POLYMERASE II;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; DEVELOPMENTAL GENETICS; DNA SUPERCOILING; GENE CONTROL; GENE LOCUS; GENETIC TRANSCRIPTION; MOLECULAR MODEL; PROMOTER REGION;

ANIMALS; BETA-GLOBINS; CHROMATIN; DNA PACKAGING; EMBRYONIC DEVELOPMENT; GENETIC LOCI; HUMANS; MODELS, MOLECULAR; RNA POLYMERASE II; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 73149089231     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200900062     Document Type: Article

References (88)

1. Reik A, Telling A, Zitnik G, et al. 1998. The locus control region is necessary for gene expression in the human β-globin locus but not the maintenance of an open chromatin structure in erythroid cells. Mol Cell Biol 18: 5992-6000.
2. Epner E, Reik A, Cimbora D, et al. 1998. The β-globin LCR is not necessary for an open chromatin structure or developmentally regulated transcription of the native mouse β-globin locus. Mol Cell 2: 447-455.
3. Tolhuis B, Palstra RJ, Splinter E, et al. 2002. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol Cell 10: 1453-1465.
4. Palstra RJ, Tolhuis B, Splinter E, et al. 2003. The β-globin nuclear compartment in development and erythroid differentiation. Nat Genet 35: 190-194.
5. Eltsov M, Maclellan KM, Maeshima K, et al. 2008. Analysis of cryoelectron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc Natl Acad Sci U S A 105: 19732-19737.
6. McDowall AW, Smith JM, Dubochet J. 1986. Cryo-electron microscopy of vitrified chromosomes in situ. EMBO J 5: 1395-1402.
7. Woodcock CL. 1994. Chromatin fibers observed in situ in frozen hydrated sections. Native fiber diameter is not correlated with nucleosome repeat length. J Cell Biol 125: 11-19.
8. Ghirlando R, Felsenfeld G. 2008. Hydrodynamic studies on defined heterochromatin fragments support a 30-nm fiber having six nucleosomes per turn. J Mol Biol 376: 1417-1425.
9. Brown JM, Green J, das Neves RP, et al. 2008. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J Cell Biol 182: 1083-1097.
10. Sapojnikova N, Thorne A, Myers F, et al. 2009. The chromatin of active genes is not in a permanently open conformation. J Mol Biol 386: 290-299.
11. Wong H, Victor JM, Mozziconacci J. 2007. An all-atom model of the chromatin fiber containing linker histones reveals a versatile structure tuned by the nucleosomal repeat length. PLoS One 2: e877.
12. Robinson PJ, Fairall L, Huynh VA, et al. 2006. EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci U S A 103: 6506-6511.
13. Benezra R, Cantor CR, Axel R. 1986. Nucleosomes are phased along the mouse b-major globin gene in erythroid and nonerythroid cells. Cell 44: 697-704.
14. Johnson KD, Grass JA, Park C, et al. 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.
15. Cho Y, Song SH, Lee JJ, et al. 2008. The role of transcriptional activator GATA-1 at human β-globin HS2. Nucleic Acids Res 36: 4521-4528.
16. Layon ME, Ackley CJ, West RJ, et al. 2007. Expression of GATA-1 in a non-hematopoietic cell line induces β-globin locus control region chromatin structure remodeling and an erythroid pattern of gene expression. J Mol Biol 366: 737-744.
17. Stamatoyannopoulos JA, Goodwin A, Joyce T, et al. 1995. NF-E2 and GATA binding motifs are required for the formation of DNase I hypersensitive site 4 of the human β-globin locus control region. EMBO J 14: 106-116.
18. Kornberg R. 2007. The molecular basis of eukaryotic transcription (Nobel Lecture). Angew Chem, Int Ed Engl 46: 6956-6965.
19. Forrester WC, Novak U, Gelinas R, et al. 1989. Molecular analysis of the human β-globin locus activation region. Proc Natl Acad Sci U S A 86: 5439-5443.
20. Epshtein V, Toulme F, Rahmouni AR, et al. 2003. Transcription through the roadblocks: the role of RNA polymerase cooperation. EMBO J 22: 4719-4727.
21. Darzacq X, Shav-Tal Y, de Turris V, et al. 2007. In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 14: 796-806.
22. Epshtein V, Nudler E. 2003. Cooperation between RNA polymerase molecules in transcription elongation. Science 300: 801-805.
23. Cook PR. 1999. The organization of replication and transcription. Science 284: 1790-1795.
24. Lavelle C. 2007. Transcription elongation through a chromatin template. Biochimie 89: 516-527.
25. Bancaud A, Wagner G, Conde ESN, et al. 2007. Nucleosome chiral transition under positive torsional stress in single chromatin fibers. Mol Cell 27: 135-147.
26. Lavelle C. 2009. Forces and torques in the nucleus: chromatin under mechanical constraints. Biochem Cell Biol 87: 307-322.
27. Ito T, Ikehara T, Nakagawa T, et al. 2000. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev 14: 1899-1907.
28. Reinberg D, Sims RJ, III. 2006. de FACTo nucleosome dynamics. J Biol Chem 281: 23297-23301.
29. Collins I, Weber A, Levens D. 2001. Transcriptional consequences of topoisomerase inhibition. Mol Cell Biol 21: 8437-8451.
30. Kouzine F, Sanford S, Elisha-Feil Z, et al. 2008. The functional response of upstream DNA to dynamic supercoiling in vivo. Nat Struct Mol Biol 15: 146-154.
31. Salceda J, Fernandez X, Roca J. 2006. Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J 25: 2575-2583.
32. Preker P, Nielsen J, Schierup MH, et al. 2009. RNA polymerase plays both sides: vivid and bidirectional transcription around and upstream of active promoters. Cell Cycle 8.
33. Kapranov P, Willingham AT, Gingeras TR. 2007. Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 8: 413-423.
34. Li LC, Okino ST, Zhao H, et al. 2006. Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci U S A 103: 17337-17342.
35. Mao Q, Li Y, Zheng X, et al. 2008. Up-regulation of E-cadherin by small activating RNA inhibits cell invasion and migration in 5637 human bladder cancer cells. Biochem Biophys Res Commun 375: 566-570.
36. Wu L, Belasco JG. 2008. Let me count the ways: mechanisms of gene regulation by miRNAs and siRNAs. Mol Cell 29: 1-7.
37. Borunova VV, Yudinkova ES, Razin SV. 2003. Mapping of the boundary of the erythroid-specific transcriptional unit in the 5(-terminal region of the domain of chicken α-globin genes. Dokl Biochem Biophys 393: 301-303.
38. Chekanova JA, Gregory BD, Reverdatto SV, et al. 2007. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340-1353.
39. Xu Z, Wei W, Gagneur J, et al. 2009. Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033-1037.
40. West S, Gromak N, Norbury CJ, et al. 2006. Adenylation and exosomemediated degradation of cotranscriptionally cleaved pre-messenger RNA in human cells. Mol Cell 21: 437-443.
41. Carter D, Chakalova L, Osborne CS, et al. 2002. Long-range chromatin regulatory interactions in vivo. Nat Genet 32: 623-626.
42. Brand M, Ranish JA, Kummer NT, et al. 2004. Dynamic changes in transcription factor complexes during erythroid differentiation revealed by quantitative proteomics. Nat Struct Mol Biol 11: 73-80.
43. Gribnau J, Diderich K, Pruzina S, et al. 2000. Intergenic transcription and developmental remodeling of chromatin subdomains in the human bglobin locus. Mol Cell 5: 377-386.
44. Zhu X, Ling J, Zhang L, et al. 2007. A facilitated tracking and transcription mechanism of long-range enhancer function. Nucleic Acids Res 35: 5532-5544.
45. Bulger M, Groudine M. 1999. Looping versus linking: toward a model for long-distance gene activation. Genes Dev 13: 2465-2477.
46. Wang Q, Carroll JS, Brown M. 2005. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell 19: 631-642.
47. Hatzis P, Talianidis I. 2002. Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol Cell 10: 1467-1477.
48. Wijgerde M, Grosveld F, Fraser P. 1995. Transcription complex stability and chromatin dynamics in vivo. Nature 377: 209-213.
49. Chakalova L, Debrand E, Mitchell JA, et al. 2005. Replication and transcription: shaping the landscape of the genome. Nat Rev Genet 6: 669-677.
50. Miles J, Mitchell JA, Chakalova L, et al. 2007. Intergenic transcription, cell-cycle and the developmentally regulated epigenetic profile of the human β-globin locus. PLoS One 2: e630.
51. Wang L, Di LJ, Lv X, et al. 2009. Inter-MAR association contributes to transcriptionally active looping events in human β-globin gene cluster. PLoS One 4: e4629.
52. Wen J, Huang S, Rogers H, et al. 2005. SATB1 family protein expressed during early erythroid differentiation modifies globin gene expression. Blood 105: 3330-3339.
53. Workman JL. 2006. Nucleosome displacement in transcription. Genes Dev 20: 2009-2017.
54. Filippova GN. 2008. Genetics and epigenetics of the multifunctional protein CTCF. Curr Top Dev Biol 80: 337-360.
55. Wallace JA, Felsenfeld G. 2007. We gather together: insulators and genome organization. Curr Opin Genet Dev 17: 400-407.
56. Splinter E, Heath H, Kooren J, et al. 2006. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev 20: 2349-2354.
57. Bender MA, Byron R, Ragoczy T, et al. 2006. Flanking HS-62.5 and 3′ HS1, and regions upstream of the LCR, are not required for β-globin transcription. Blood 108: 1395-1401.
58. Rubio ED, Reiss DJ, Welcsh PL, et al. 2008. CTCF physically links cohesin to chromatin. Proc Natl Acad Sci U S A 105: 8309-8314.
59. Wendt KS, Yoshida K, Itoh T, et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
60. Richard P, Manley JL. 2009. Transcription termination by nuclear RNA polymerases. Genes Dev 23: 1247-1269.
61. Hirota K, Miyoshi T, Kugou K, et al. 2008. Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature 456: 130-134.
62. de Laat W, Grosveld F. 2003. Spatial organization of gene expression: The active chromatin hub. Chromosome Res 11: 447-459.
63. Demers C, Chaturvedi CP, Ranish JA, et al. 2007. Activator-mediated recruitment of the MLL2 methyltransferase complex to the β-globin locus. Mol Cell 27: 573-584.
64. Kim A, Song SH, Brand M, et al. 2007. Nucleosome and transcription activator antagonism at human β-globin locus control region DNase I hypersensitive sites. Nucleic Acids Res 35: 5831-5838.
65. Birney E, Stamatoyannopoulos JA, Dutta A, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
66. Hongay CF, Grisafi PL, Galitski T, et al. 2006. Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 127: 735-745.
67. Rinn JL, Kertesz M, Wang JK, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
68. Bottardi S, Ross J, Bourgoin V, et al. 2009. Ikaros and GATA-1 combinatorial effect is required for silencing of human gamma-globin genes. Mol Cell Biol 29: 1526-1537.
69. Kim SI, Bultman SJ, Kiefer CM, et al. 2009. BRG1 requirement for longrange interaction of a locus control region with a downstream promoter. Proc Natl Acad Sci USA 106: 2259-2264.
70. Forsberg EC, Downs KM, Christensen HM, et al. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc Natl Acad Sci U S A 97: 14494-14499.
71. Chadick JZ, Asturias FJ. 2005. Structure of eukaryotic Mediator complexes. Trends Biochem Sci 30: 264-271.
72. Chen HT, Warfield L, Hahn S. 2007. The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat Struct Mol Biol 14: 696-703.
73. Schultz P, Fribourg S, Poterszman A, et al. 2000. Molecular structure of human TFIIH. Cell 102: 599-607.
74. Swinburne IA, Meyer CA, Liu XS, et al. 2006. Genomic localization of RNA binding proteins reveals links between pre-mRNA processing and transcription. Genome Res 16: 912-921.
75. Asturias FJ, Chung WH, Kornberg RD, et al. 2002. Structural analysis of the RSC chromatin-remodeling complex. Proc Natl Acad Sci U S A 99: 13477-13480.
76. Davey CA, Sargent DF, Luger K, et al. 2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319: 1097-1113.
77. Andel F, III, Ladurner AG, Inouye C, et al. 1999. Three-dimensional structure of the human TFIID-IIA-IIB complex. Science 286: 2153-2156.
78. Azubel M, Wolf SG, Sperling J, et al. 2004. Three-dimensional structure of the native spliceosome by cryo-electron microscopy. Mol Cell 15: 833-839.
79. Gnatt AL, Cramer P, Fu J, et al. 2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution. Science 292: 1876-1882.
80. Haering CH, Schoffnegger D, Nishino T, et al. 2004. Structure and stability of cohesin's Smc1-kleisin interaction. Mol Cell 15: 951-964.
81. Keys JR, Tallack MR, Zhan Y, et al. 2008. A mechanism for Ikaros regulation of human globin gene switching. Br J Haematol 141: 398-406.
82. Kooren J, Palstra RJ, Klous P, et al. 2007. β-globin active chromatin Hub formation in differentiating erythroid cells and in p45 NF-E2 knock-out mice. J Biol Chem 282: 16544-16552.
83. Vakoc CR, Letting DL, Gheldof N, et al. 2005. Proximity among distant regulatory elements at the β-globin locus requires GATA-1 and FOG-1. Mol Cell 17: 453-462.
84. Song SH, Hou C, Dean A. 2007. A positive role for NLI/Ldb1 in long-range β-globin locus control region function. Mol Cell 28: 810-822.
85. Du MJ, Lv X, Hao DL, et al. 2008. MafK/NF-E2 p18 is required for β-globin genes activation by mediating the proximity of LCR and active β-globin genes in MEL cell line. Int J Biochem Cell Biol 40: 1481-1493.
86. Drissen R, Palstra RJ, Gillemans N, et al. 2004. The active spatial organization of the β-globin locus requires the transcription factor EKLF. Genes Dev 18: 2485-2490.
87. Nuez B, Michalovich D, Bygrave A, et al. 1995. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375: 316-318.
88. Perkins AC, Sharpe AH, Orkin SH. 1995. Lethal b-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375: 318-322.