Chromatin position in human HepG2 cells: although being non-random, significantly changed in daughter cells
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
Wellcome Trust - United Kingdom
075834/04/Z
Wellcome Trust - United Kingdom
PubMed
19056497
PubMed Central
PMC2658736
DOI
10.1016/j.jsb.2008.10.007
PII: S1047-8477(08)00253-0
Knihovny.cz E-zdroje
- MeSH
- buněčné jadérko metabolismus MeSH
- buněčné jádro metabolismus MeSH
- buněčné linie MeSH
- časové faktory MeSH
- chromatin chemie metabolismus MeSH
- chromozomy ultrastruktura MeSH
- fibroblasty metabolismus MeSH
- fluorescenční mikroskopie metody MeSH
- histony metabolismus MeSH
- lidé MeSH
- počítačové zpracování obrazu MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chromatin MeSH
- histony MeSH
Mammalian chromosomes occupy chromosome territories within nuclear space the positions of which are generally accepted as non-random. However, it is still controversial whether position of chromosome territories/chromatin is maintained in daughter cells. We addressed this issue and investigated maintenance of various chromatin regions of unknown composition as well as nucleolus-associated chromatin, a significant part of which is composed of nucleolus organizer region-bearing chromosomes. The photoconvertible histone H4-Dendra2 was used to label such regions in transfected HepG2 cells, and its position was followed up to next interphase. The distribution of labeled chromatin in daughter cells exhibited a non-random character. However, its distribution in a vast majority of daughter cells extensively differed from the original ones and the labeled nucleolus-associated chromatin differently located into the vicinity of different nucleoli. Therefore, our results were not consistent with a concept of preservation chromatin position. This conclusion was supported by the finding that the numbers of nucleoli significantly differed between the two daughter cells. Our results support a view that while the transfected daughter HepG2 cells maintain some features of the parental cell chromosome organization, there is also a significant stochastic component associated with reassortment of chromosome territories/chromatin that results in their positional rearrangements.
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Belmont A.S., Dietzel S., Nye A.C., Strukov Y.G., Tumbar T. Large-scale chromatin structure and function. Curr. Opin. Cell Biol. 1999;11:307–311. PubMed
Berr A., Schubert I. Interphase chromosome arrangement in Arabidopsis thaliana is similar in differentiated and meristematic tissues and shows a transient mirror symmetry after nuclear division. Genetics. 2007;176:853–863. PubMed PMC
Bickmore W.A., Chubb J.R. Dispatch. Chromosome position: now, where was I? Curr. Biol. 2003;13:R357–R359. PubMed
Boisvert F.M., van Koningsbruggen S., Navascues J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007;8:574–585. PubMed
Bolzer A., Kreth G., Solovei I., Koehler D., Saracoglu K., Fauth C., Müller S., Eils R., Cremer C., Speicher M.R., Cremer T. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 2005;3:e157. PubMed PMC
Boyle S., Gilchrist S., Bridger J.M., Mahy N.L., Ellis J.A., Bickmore W.A. The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet. 2001;10:211–219. PubMed
Branco M.R., Pombo A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 2006;4:e138. PubMed PMC
Cavalli G. Chromosome kissing. Curr. Opin. Genet. Dev. 2007;17:443–450. PubMed
Chuang C.H., Belmont A.S. Moving chromatin within the interphase nucleus-controlled transitions? Semin. Cell Dev. Biol. 2007;18:698–706. PubMed PMC
Clemson C.M., Hall L.L., Byron M., McNeil J., Lawrence J.B. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc. Natl. Acad. Sci. USA. 2006;103:7688–7693. PubMed PMC
Cremer T., Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2001;2:292–301. PubMed
Essers J., van Cappellen W.A., Theil A.F., van Drunen E., Jaspers N.G., Hoeijmakers J.H., Wyman C., Vermeulen W., Kanaar R. Dynamics of relative chromosome position during the cell cycle. Mol. Biol. Cell. 2005;16:769–775. PubMed PMC
Federico C., Cantarella C.D., Di Mare P., Tosi S., Saccone S. The radial arrangement of the human chromosome 7 in the lymphocyte cell nucleus is associated with chromosomal band gene density. Chromosoma. 2008;117:399–410. PubMed
Fraser P., Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature. 2007;447:413–417. PubMed
Frey M.R., Bailey A.D., Weiner A.M., Matera A.G. Association of snRNA genes with coiled bodies is mediated by nascent snRNA transcripts. Curr. Biol. 1999;9:126–135. PubMed
Gerlich D., Beaudouin J., Kalbfuss B., Daigle N., Eils R., Ellenberg J. Global chromosome positions are transmitted through mitosis in mammalian cells. Cell. 2003;112:751–764. PubMed
Gerlich D., Ellenberg J. Dynamics of chromosome positioning during the cell cycle. Curr. Opin. Cell Biol. 2003;15:664–671. PubMed
Gonda K., Fowler J., Katoku-Kikyo N., Haroldson J., Wudel J., Kikyo N. Reversible disassembly of somatic nucleoli by the germ cell proteins FRGY2a and FRGY2b. Nat. Cell Biol. 2003;5:205–210. PubMed
Gurskaya N.G., Verkhusha V.V., Shcheglov A.S., Staroverov D.B., Chepurnykh T.V., Fradkov A.F., Lukyanov S., Lukyanov K.A. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 2006;24:461–465. PubMed
Kalmarova M., Smirnov E., Kovacik L., Popov A., Raska I. Positioning of the NOR-bearing chromosomes in relation to nucleoli in daughter cells after mitosis. Physiol. Res. 2008;57:421–425. PubMed PMC
Kalmarova M., Smirnov E., Masata M., Koberna K., Ligasova A., Popov A., Raska I. Positioning of NORs and NOR-bearing chromosomes in relation to nucleoli. J. Struct. Biol. 2007;160:49–56. PubMed PMC
Kimura H., Cook P.R. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 2001;153:1341–1353. PubMed PMC
Kumaran R.I., Spector D.L. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 2008;180:51–65. PubMed PMC
Kumaran R.I., Thakar R., Spector D.L. Chromatin dynamics and gene positioning. Cell. 2008;132:929–934. PubMed PMC
Kupper K., Kolbl A., Biener D., Dittrich S., von Hase J., Thormeyer T., Fiegler H., Carter N.P., Speicher M.R., Cremer T., Cremer M. Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma. 2007;116:285–306. PubMed PMC
Kurakin A. Self-organization versus Watchmaker: ambiguity of molecular recognition and design charts of cellular circuitry. J. Mol. Recognit. 2007;20:205–214. PubMed
Lanctot C., Cheutin T., Cremer M., Cavalli G., Cremer T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 2007;8:104–115. PubMed
Leger I., Guillaud M., Krief B., Brugal G. Interactive computer-assisted analysis of chromosome 1 colocalization with nucleoli. Cytometry. 1994;16:313–323. PubMed
Manuelidis L., Borden J. Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma. 1988;96:397–410. PubMed
Meaburn K.J., Misteli T., Soutoglou E. Spatial genome organization in the formation of chromosomal translocations. Semin. Cancer. Biol. 2007;17:80–90. PubMed PMC
Misteli T. Beyond the sequence: cellular organization of genome function. Cell. 2007;128:787–800. PubMed
Nagele R.G., Freeman T., McMorrow L., Thomson Z., Kitson-Wind K., Lee H. Chromosomes exhibit preferential positioning in nuclei of quiescent human cells. J. Cell Sci. 1999;112:525–535. PubMed
Nunez E., Kwon Y.S., Hutt K.R., Hu Q., Cardamone M.D., Ohgi K.A., Garcia-Bassets I., Rose D.W., Glass C.K., Rosenfeld M.G. Nuclear receptor-enhanced transcription requires motor- and LSD1-dependent gene networking in interchromatin granules. Cell. 2008;132:996–1010. PubMed
Nunez E., Kwon Y.S., Hutt K.R., Hu Q., Cardamone M.D., Ohgi K.A., Garcia-Bassets I., Rose D.W., Glass C.K., Rosenfeld M.G. Retracted: nuclear receptor-enhanced transcription requires motor- and LSD1-dependent gene networking in interchromatin granules. Cell. 2008;134:189. PubMed
Parada L., Misteli T. Chromosome positioning in the interphase nucleus. Trends Cell Biol. 2002;12:425–432. PubMed
Parada L.A., McQueen P.G., Misteli T. Tissue-specific spatial organization of genomes. Genome Biol. 2004;5:R44. PubMed PMC
Parada L.A., Roix J.J., Misteli T. An uncertainty principle in chromosome positioning. Trends Cell Biol. 2003;13:393–396. PubMed
Peng J.C., Karpen G.H. H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat. Cell Biol. 2007;9:25–35. PubMed PMC
Raska I., Shaw P.J., Cmarko D. New insights into nucleolar architecture and activity. Int. Rev. Cytol. 2006;255:177–235. PubMed
Roix J.J., McQueen P.G., Munson P.J., Parada L.A., Misteli T. Spatial proximity of translocation-prone gene loci in human lymphomas. Nat. Genet. 2003;34:287–291. PubMed
Schul W., van Der Kraan I., Matera A.G., van Driel R., de Jong L. Nuclear domains enriched in RNA 3′-processing factors associate with coiled bodies and histone genes in a cell cycle-dependent manner. Mol. Biol. Cell. 1999;10:3815–3824. PubMed PMC
Smirnov E., Kalmarova M., Koberna K., Zemanova Z., Malinsky J., Masata M., Cvackova Z., Michalova K., Raska I. NORs and their transcription competence during the cell cycle. Folia Biol. (Praha) 2006;52:59–70. PubMed PMC
Thomson I., Gilchrist S., Bickmore W.A., Chubb J.R. The radial positioning of chromatin is not inherited through mitosis but is established de novo in early G1. Curr. Biol. 2004;14:166–172. PubMed
Volpi E.V., Chevret E., Jones T., Vatcheva R., Williamson J., Beck S., Campbell R.D., Goldsworthy M., Powis S.H., Ragoussis J. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J. Cell Sci. 2000;113:1565–1576. PubMed
Walter J., Schermelleh L., Cremer M., Tashiro S., Cremer T. Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J. Cell Biol. 2003;160:685–697. PubMed PMC
Wiesmeijer K., Krouwels I.M., Tanke H.J., Dirks R.W. Chromatin movement visualized with photoactivable GFP-labeled histone H4. Differentiation. 2008;76:83–90. PubMed
Williams R.R., Broad S., Sheer D., Ragoussis J. Subchromosomal positioning of the epidermal differentiation complex (EDC) in keratinocyte and lymphoblast interphase nuclei. Exp. Cell Res. 2002;272:163–175. PubMed
Williams R.R., Fisher A.G. Chromosomes, positions please! Nat. Cell Biol. 2003;5:388–390. PubMed