The fourth chromosome of
            <i>Drosophila melanogaster</i>
            : Interspersed euchromatic and heterochromatic domains

Sun, Fang-Lin; Cuaycong, Matthew H.; Craig, Charles P.; Wallrath, Lori L.; Locke, John; Elgin, Sarah C. R.

doi:10.1073/pnas.090530797

Cited by 124 publications

(110 citation statements)

References 47 publications

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“…3A, panels 1 to 3). One of them is the base of the fourth chromosome (33), which is mostly heterochromatic. Staining with an anti-male-specific lethal 1 (anti-MSL-1) antibody (Fig.…”

Section: Resultsmentioning

confidence: 99%

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The Drosophila DAXX-Like Protein (DLP) Cooperates with ASF1 for H3.3 Deposition and Heterochromatin Formation

Fromental-Ramain

Ramain

Hamiche

2017

Molecular and Cellular Biology

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Histone variants are nonallelic isoforms of canonical histones, and they are deposited, in contrast to canonical histones, in a replication-independent (RI) manner. RI deposition of H3.3, a histone variant from the H3.3 family, is mediated in mammals by distinct pathways involving either the histone regulator A (HIRA) complex or the death-associated protein (DAXX)/␣-thalassemia X-linked mental retardation protein (ATRX) complex. Here, we investigated the function of the Drosophila DAXX-like protein (DLP) by using both fly genetic approaches and protein biochemistry. DLP specifically interacts with H3.3 and shows a prominent localization on the base of the X chromosome, where it appears to act in concert with XNP, the Drosophila homolog of ATRX, in heterochromatin assembly and maintenance. The functional association between DLP and XNP is further supported by a series of experiments that illustrate genetic interactions and the DLP-XNP-dependent localization of specific chromosomal proteins. In addition, DLP both participates in the RI deposition of H3.3 and associates with anti-silencing factor 1 (ASF1). We suggest, in agreement with a recently proposed model, that DLP and ASF1 are part of a predeposition complex, which is recruited by XNP and is necessary to prevent DNA exposure in the nucleus.KEYWORDS DLP, heterochromatin, histone variant, H3.3, XNP, ASF1 I n the nucleus, DNA is packaged under the form of chromatin. The basic repeating unit of chromatin is the nucleosome, and the nucleosome core particle consists of approximately 146 bp of DNA wrapped around a histone octamer composed of two copies of each of the histones H2A, H2B, H3, and H4. (1, 2). Gene-rich domains are packaged into euchromatin, which is decondensed in interphase nuclei and is enriched for histone modifications characteristic of transcriptionally active regions. Moreover, euchromatin often exhibits high DNA accessibility. In contrast, gene-poor domains and repetitive sequences are packaged into condensed heterochromatin that carries histone modifications associated with transcriptional repression.In addition to the canonical core histones, cells express nonallelic-isoform histone variants (3). Histone variants have emerged as essential contributors to the regulation of chromatin structure, and they are involved in multiple processes, including chromatin stability, DNA repair, and transcriptional regulation. Canonical histones are almost exclusively expressed during the S phase of the cell cycle and are incorporated into chromatin in a DNA replication-dependent fashion, whereas replication-independent (RI) histone variants are expressed throughout the cell cycle.One of the best-studied histone variants is H3.3, which can replace the major species H3 (4). H3.3 is expressed and incorporated at all phases of the cell cycle (5). The available data suggest that H3.3 is a marker of active chromatin and associated with the

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“…3A, panels 1 to 3). One of them is the base of the fourth chromosome (33), which is mostly heterochromatic. Staining with an anti-male-specific lethal 1 (anti-MSL-1) antibody (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…MSL-2 is expressed only in males (39) and induces the assembly of the MSL complex on chromatin and a 2-fold upregulation of the single X chromosome to reach the level of the two X chromosomes in females (33). We then investigated the consequences of overexpressed dlp for male viability when msl-2 function is reduced (Fig.…”

Section: Resultsmentioning

confidence: 99%

The Drosophila DAXX-Like Protein (DLP) Cooperates with ASF1 for H3.3 Deposition and Heterochromatin Formation

Fromental-Ramain

Ramain

Hamiche

2017

Molecular and Cellular Biology

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“…This transposon was introduced into flies that carried a deletion of the endogenous yellow gene, and eight homozygousviable transgenic lines were established (Table 1). Six lines had insertions within the euchromatic portion of the chromosomal arms (5B, 18C, 47A, 84A, 90F, and 92A), one line had an insertion close to a telomere (100F), and one line had an insertion on the fourth chromosome (102B), which contains interspersed euchromatic and heterochromatic domains (42). Flies from all lines displayed near wild-type levels of cuticular pigmentation, with scores of 5 in both wing and body ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Enhancer action in trans is permitted throughout the Drosophila genome

Chen

Huisinga

Viering

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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Interactions between paired homologous genes can lead to changes in gene expression. Such trans-regulatory effects exemplify transvection and are displayed by many genes in Drosophila, in which homologous chromosomes are paired somatically. Transvection involving the yellow cuticle pigmentation gene can occur by at least two mechanisms, one involving the trans-action of enhancers on a paired promoter and a second involving pairingmediated bypass of a chromatin insulator. A system was developed to evaluate whether the action of the yellow enhancers in trans could be reconstituted outside of the natural near telomeric location of the yellow gene. To this end, transgenic flies were generated that carried a yellow gene modified by the inclusion of strategically placed recognition sites for the Cre and FLP recombinases. Independent action of the recombinases produced a pair of derivative alleles, one enhancerless and the other promoterless, at each transgene location. Transvection between the derivatives was assessed by the degree of interallelic complementation. Complementation was observed at all eight sites tested. These studies demonstrate that yellow transvection can occur at multiple genomic locations and indicate that the Drosophila genome generally is permissive to enhancer action in trans. G ene expression is controlled by regulatory elements that modulate transcription in appropriate temporal and spatial patterns. In eukaryotes, these control elements often reside in large, complex regions, requiring action over long distances to elicit changes in transcription of a target promoter. In some cases, the control elements of paired homologous genes can interact in trans to alter gene expression. Such trans-regulatory effects illustrate processes known as transvection. Transvection was described first in Drosophila (1), which has homologous chromosomes that are paired somatically. Transvection and related processes have been reported in many organisms besides Drosophila (for example, refs. 2-7, and reviewed in refs. 8-11). These observations suggest that transvection may be generally possible for eukaryotic control regions and that these processes may be important for the normal regulation of some genes. For example, chromosomal pairing is proposed to play a role in gene silencing associated with imprinting and X chromosome inactivation (4, 12).In Drosophila, interactions between homologous chromosomes can have either a positive or negative effect on transcription. Examples of negative effects include repression of white gene expression by certain alleles of zeste, trans silencing conferred by the insertion of a block of heterochromatin near the brown gene, and pairing-dependent silencing, as exemplified by the effects of Polycomb response elements (reviewed in refs. 8-11, 13, and 14). Examples of positive effects include events at the Ultrabithorax, Abdominal B, decapentaplegic, yellow, and eyes absent genes (1,(15)(16)(17)(18)(19)(20)(21)(22)(23)(24).A useful system for studying the mechanisms involved in posi...

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“…The small fourth chromosome of Drosophila melanogaster, interspersed with heterochromatic domains, shows a banded pattern of HP1 localization (7,15). Consistent with HP1 having a packaging function at these locations, transgenes inserted along the fourth chromosome exhibit PEV that is suppressed by Su(var)2-5 mutations (15,16).…”

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confidence: 98%

Does heterochromatin protein 1 always follow code?

Kirschmann

Wallrath

2002

Proc. Natl. Acad. Sci. U.S.A.

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Heterochromatin protein 1 (HP1) is a conserved chromosomal protein that participates in chromatin packaging and gene silencing. A loss of HP1 leads to lethality in Drosophila and correlates with metastasis in human breast cancer cells. On Drosophila polytene chromosomes HP1 is localized to centric regions, telomeric regions, in a banded pattern along the fourth chromosome, and at many sites scattered throughout the euchromatic arms. Recently, one mechanism of HP1 chromosome association was revealed; the amino-terminal chromo domain of HP1 interacts with methylated lysine nine of histone H3, consistent with the histone code hypothesis. Compelling data support this mechanism of HP1 association at centric regions. Is this the only mechanism by which HP1 associates with chromosomes? Interest is now shifting toward the role of HP1 within euchromatic domains. Accumulating evidence in Drosophila and mammals suggests that HP1 associates with chromosomes through interactions with nonhistone chromosomal proteins at locations other than centric heterochromatin. Does HP1 play a similar role in chromatin packaging and gene regulation at these sites as it does in centric heterochromatin? Does HP1 associate with the same proteins at these sites as it does in centric heterochromatin? A first step toward answering these questions is the identification of sequences associated with HP1 within euchromatic domains. Such sequences are likely to include HP1 ''target genes'' whose discovery will aid in our understanding of HP1 lethality in Drosophila and metastasis of breast cancer cells.

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The fourth chromosome of Drosophila melanogaster : Interspersed euchromatic and heterochromatic domains

Cited by 124 publications

References 47 publications

The Drosophila DAXX-Like Protein (DLP) Cooperates with ASF1 for H3.3 Deposition and Heterochromatin Formation

The Drosophila DAXX-Like Protein (DLP) Cooperates with ASF1 for H3.3 Deposition and Heterochromatin Formation

Enhancer action in trans is permitted throughout the Drosophila genome

Does heterochromatin protein 1 always follow code?

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