Exploring cellular memory molecules marking competent and active transcriptions

Springer Science and Business Media LLC - 2007
Li X1, Guangming Zhou1, Wei Song1, Xuesong Wu1, Gong‐Hong Wei1, Dejun Hao1, Xiang Lv1, De-Pei Liu1, Chih‐Chuan Liang1
1From National Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100005, PR China

Tóm tắt

Abstract Background Development in higher eukaryotes involves programmed gene expression. Cell type-specific gene expression is established during this process and is inherited in succeeding cell cycles. Higher eukaryotes have evolved elegant mechanisms by which committed gene-expression states are transmitted through numerous cell divisions. Previous studies have shown that both DNase I-sensitive sites and the basal transcription factor TFIID remain on silenced mitotic chromosomes, suggesting that certain trans-factors might act as bookmarks, maintaining the information and transmitting it to the next generation. Results We used the mouse globin gene clusters as a model system to examine the retention of active information on M-phase chromosomes and its contribution to the persistence of transcriptional competence of these gene clusters in murine erythroleukemia cells. In cells arrested in mitosis, the erythroid-specific activator NF-E2p45 remained associated with its binding sites on the globin gene loci, while the other major erythroid factor, GATA-1, was removed from chromosome. Moreover, despite mitotic chromatin condensation, the distant regulatory regions and promoters of transcriptionally competent globin gene loci are marked by a preserved histone code consisting in active histone modifications such as H3 acetylation, H3-K4 dimethylation and K79 dimethylation. Further analysis showed that other active genes are also locally marked by the preserved active histone code throughout mitotic inactivation of transcription. Conclusion Our results imply that certain kinds of specific protein factors and active histone modifications function as cellular memory markers for both competent and active genes during mitosis, and serve as a reactivated core for the resumption of transcription when the cells exit mitosis.

Từ khóa


Tài liệu tham khảo

Gottesfeld JM, Forbes DJ: Mitotic repression of the transcriptional machinery. Trends Biochem Sci. 1997, 22 (6): 197-202. 10.1016/S0968-0004(97)01045-1

Kerem BS, Goitein R, Diamond G, Cedar H, Marcus M: Mapping of DNAase I sensitive regions on mitotic chromosomes. Cell. 1984, 38 (2): 493-499. 10.1016/0092-8674(84)90504-X

Michelotti EF, Sanford S, Levens D: Marking of active genes on mitotic chromosomes. Nature. 1997, 388 (6645): 895-899. 10.1038/42282

John S, Workman JL: Bookmarking genes for activation in condensed mitotic chromosomes. Bioessays. 1998, 20 (4): 275-279. 10.1002/(SICI)1521-1878(199804)20:4<275::AID-BIES1>3.0.CO;2-P

Chen D, Hinkley CS, Henry RW, Huang S: TBP dynamics in living human cells: constitutive association of TBP with mitotic chromosomes. Mol Biol Cell. 2002, 13 (1): 276-284. 10.1091/mbc.01-10-0523

Christova R, Oelgeschlager T: Association of human TFIID-promoter complexes with silenced mitotic chromatin in vivo. Nat Cell Biol. 2002, 4 (1): 79-82. 10.1038/ncb733

Nobrega MA, Ovcharenko I, Afzal V, Rubin EM: Scanning human gene deserts for long-range enhancers. Science. 2003, 302 (5644): 413- 10.1126/science.1088328

Spitz F, Gonzalez F, Duboule D: A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell. 2003, 113 (3): 405-417. 10.1016/S0092-8674(03)00310-6

Palstra RJ, Tolhuis B, Splinter E, Nijmeijer R, Grosveld F, de Laat W: The beta-globin nuclear compartment in development and erythroid differentiation. Nat Genet. 2003, 35 (2): 190-194. 10.1038/ng1244

Groudine M, Weintraub H: Propagation of globin DNAase I-hypersensitive sites in absence of factors required for induction: a possible mechanism for determination. Cell. 1982, 30 (1): 131-139. 10.1016/0092-8674(82)90019-8

Jenuwein T, Allis CD: Translating the histone code. Science. 2001, 293 (5532): 1074-1080. 10.1126/science.1063127

Turner BM: Cellular memory and the histone code. Cell. 2002, 111 (3): 285-291. 10.1016/S0092-8674(02)01080-2

Kouskouti A, Talianidis I: Histone modifications defining active genes persist after transcriptional and mitotic inactivation. Embo J. 2005, 24 (2): 347-357. 10.1038/sj.emboj.7600516

Sawado T, Igarashi K, Groudine M: Activation of beta-major globin gene transcription is associated with recruitment of NF-E2 to the beta-globin LCR and gene promoter. Proc Natl Acad Sci U S A. 2001, 98 (18): 10226-10231. 10.1073/pnas.181344198

Anguita E, Hughes J, Heyworth C, Blobel GA, Wood WG, Higgs DR: Globin gene activation during haemopoiesis is driven by protein complexes nucleated by GATA-1 and GATA-2. Embo J. 2004, 23 (14): 2841-2852. 10.1038/sj.emboj.7600274

Kruhlak MJ, Hendzel MJ, Fischle W, Bertos NR, Hameed S, Yang XJ, Verdin E, Bazett-Jones DP: Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J Biol Chem. 2001, 276 (41): 38307-38319.

Boyes J, Byfield P, Nakatani Y, Ogryzko V: Regulation of activity of the transcription factor GATA-1 by acetylation. Nature. 1998, 396 (6711): 594-598. 10.1038/25166

Collavin L, Gostissa M, Avolio F, Secco P, Ronchi A, Santoro C, Del Sal G: Modification of the erythroid transcription factor GATA-1 by SUMO-1. Proc Natl Acad Sci U S A. 2004, 101 (24): 8870-8875. 10.1073/pnas.0308605101

Partington GA, Patient RK: Phosphorylation of GATA-1 increases its DNA-binding affinity and is correlated with induction of human K562 erythroleukaemia cells. Nucleic Acids Res. 1999, 27 (4): 1168-1175. 10.1093/nar/27.4.1168

Francastel C, Magis W, Groudine M: Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci U S A. 2001, 98 (21): 12120-12125. 10.1073/pnas.211444898

Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M: The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004, 18 (11): 1263-1271. 10.1101/gad.1198204

Ahmad K, Henikoff S: The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell. 2002, 9 (6): 1191-1200. 10.1016/S1097-2765(02)00542-7

McKittrick E, Gafken PR, Ahmad K, Henikoff S: Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A. 2004, 101 (6): 1525-1530. 10.1073/pnas.0308092100

Schwartz BE, Ahmad K: Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 2005, 19 (7): 804-814. 10.1101/gad.1259805

Chow CM, Georgiou A, Szutorisz H, Maia e Silva A, Pombo A, Barahona I, Dargelos E, Canzonetta C, Dillon N: Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep. 2005, 6 (4): 354-360. 10.1038/sj.embor.7400366

Trimborn T, Gribnau J, Grosveld F, Fraser P: Mechanisms of developmental control of transcription in the murine alpha- and beta-globin loci. Genes Dev. 1999, 13: 112-124.

Wijgerde M, Grosveld F, Fraser P: Transcription complex stability and chromatin dynamics in vivo. Nature. 1995, 377: 209-213. 10.1038/377209a0

de Krom M, van de Corput M, von Lindern M, Grosveld F, Strouboulis J: Stochastic patterns in globin gene expression are established prior to transcriptional activation and are clonally inherited. Mol Cell. 2002, 9: 1319-1326. 10.1016/S1097-2765(02)00558-0

Thông tin
Thông tin xuất bản

Springer Science and Business Media LLC

Thông tin tác giả