Identification and characterization of ToRC, a novel ISWI-containing ATP-dependent chromatin assembly complex

Emelyanov, Alexander; Vershilova, Elena; Ignatyeva, Maria; Pokrovsky, Daniil; Lu, Xingwu; Konev, Alexander Y.; Fyodorov, Dmitry V.

doi:10.1101/gad.180604.111

Cited by 28 publications

(23 citation statements)

References 65 publications

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“…This is a somewhat paradoxical result, since up-regulation of ribosome biogenesis is a feature of most cancers. The Drosophila ortholog of TIP5, Toutatis, is also involved in the regulation of genes transcribed by Pol II (Emelyanov et al 2012). …”

Section: The Pol I Transcription Machinerymentioning

confidence: 99%

Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination

2016

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Nucleoli form around tandem arrays of a ribosomal gene repeat, termed nucleolar organizer regions (NORs). During metaphase, active NORs adopt a characteristic undercondensed morphology. Recent evidence indicates that the HMG-box-containing DNA-binding protein UBF (upstream binding factor) is directly responsible for this morphology and provides a mitotic bookmark to ensure rapid nucleolar formation beginning in telophase in human cells. This is likely to be a widely employed strategy, as UBF is present throughout metazoans. In higher eukaryotes, NORs are typically located within regions of chromosomes that form perinucleolar heterochromatin during interphase. Typically, the genomic architecture of NORs and the chromosomal regions within which they lie is very poorly described, yet recent evidence points to a role for context in their function. In Arabidopsis, NOR silencing appears to be controlled by sequences outside the rDNA (ribosomal DNA) array. Translocations reveal a role for context in the expression of the NOR on the X chromosome in Drosophila. Recent work has begun on characterizing the genomic architecture of human NORs. A role for distal sequences located in perinucleolar heterochromatin has been inferred, as they exhibit a complex transcriptionally active chromatin structure. Links between rDNA genomic stability and aging in Saccharomyces cerevisiae are now well established, and indications are emerging that this is important in aging and replicative senescence in higher eukaryotes. This, combined with the fact that rDNA arrays are recombinational hot spots in cancer cells, has focused attention on DNA damage responses in NORs. The introduction of DNA double-strand breaks into rDNA arrays leads to a dramatic reorganization of nucleolar structure. Damaged rDNA repeats move from the nucleolar interior to form caps at the nucleolar periphery, presumably to facilitate repair, suggesting that the chromosomal context of human NORs contributes to their genomic stability. The inclusion of NORs and their surrounding chromosomal environments in future genome drafts now becomes a priority.The relationship between nucleolar organizer regions (NORs) and nucleoli was first established in the 1930s (Heitz 1931;McClintock 1934), but, for decades, the content of the former and the role of the latter remained mysterious. The era of molecular and cellular biology revealed that NORs contain tandem arrays of ribosomal gene (rDNA) repeats and that nucleoli are the sites of ribosome biogenesis. Biochemistry has revealed the inner workings of the nucleolus and the complexity of ribosome biogenesis (for review, see Pederson 2010). However, the genomic architecture of NORs and the chromosomal context in which they lie remains undetermined for most eukaryotes. The resulting void has placed limitations on our understanding of the fundamental mechanisms by which NORs orchestrate formation of the largest structure in the nucleus. In this review, I discuss recent findings regarding the morphology of active NORs and how they seed r...

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Section: The Pol I Transcription Machinerymentioning

confidence: 99%

Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination

2016

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“…The homologous protein in flies, toutatis, also interacts with ISWI (Vanolst et al 2005). NoRC interacts with CtBP to form ToRC, which is involved in transcription regulation and nucleosome assembly outside of the nucleolus (Emelyanov et al 2012). In mammals, additional complexes are known (Bao and Shen 2011;Kasten et al 2011;Sims and Wade 2011;Yadon and Tsukiyama 2011) and it is likely that further assemblies will be discovered in flies as well.…”

Section: The Discovery Of Nucleosome Remodeling: a Historical Perspecmentioning

confidence: 99%

Nucleosome Remodeling and Epigenetics

Becker

Workman

2013

Cold Spring Harbor Perspectives in Biology

270

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“…For instance, Drosophila ACF/CHRAC can mediate chromatin assembly in conjunction with histone chaperone NAP-1 (Varga-Weisz et al 1997;Ito et al 1999). Other known ATP-dependent chromatin assembly factors include RSF, CHD1, ATRX, and ToRC/NoRC (LeRoy et al 1998(LeRoy et al , 2000Lusser et al 2005; Lewis et al 2010;Emelyanov et al 2012).…”

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confidence: 99%

Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization

et al. 2014

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Nuclear DNA in the male gamete of sexually reproducing animals is organized as sperm chromatin compacted primarily by sperm-specific protamines. Fertilization leads to sperm chromatin remodeling, during which protamines are expelled and replaced by histones. Despite our increased understanding of the factors that mediate nucleosome assembly in the nascent male pronucleus, the machinery for protamine removal remains largely unknown. Here we identify four Drosophila protamine chaperones that mediate the dissociation of protamine-DNA complexes: NAP-1, NLP, and nucleophosmin are previously characterized histone chaperones, and TAP/p32 has no known function in chromatin metabolism. We show that TAP/p32 is required for the removal of Drosophila protamine B in vitro, whereas NAP-1, NLP, and Nph share roles in the removal of protamine A. Embryos from P32-null females show defective formation of the male pronucleus in vivo. TAP/p32, similar to NAP-1, NLP, and Nph, facilitates nucleosome assembly in vitro and is therefore a histone chaperone. Furthermore, mutants of P32, Nlp, and Nph exhibit synthetic-lethal genetic interactions. In summary, we identified factors mediating protamine removal from DNA and reconstituted in a defined system the process of sperm chromatin remodeling that exchanges protamines for histones to form the nucleosome-based chromatin characteristic of somatic cells.

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Identification and characterization of ToRC, a novel ISWI-containing ATP-dependent chromatin assembly complex

Cited by 28 publications

References 65 publications

Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination

Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination

Nucleosome Remodeling and Epigenetics

Drosophila TAP/p32 is a core histone chaperone that cooperates with NAP-1, NLP, and nucleophosmin in sperm chromatin remodeling during fertilization

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