The expression of histone genes during Drosophila melanogaster oogenesis

Walker, J. Ross; Bownes, Mary

doi:10.1007/s004270050144

Cited by 10 publications

(12 citation statements)

References 20 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…During this time, the canonical histones are present in a complex with histone chaperones (N1–N2 for H3–H4 and nucleoplasmin for H2A–H2B)83, which are histone storage proteins. The mRNA used to synthesize these embryonic histone proteins is synthesized by the nurse cells in a small window of time at the end of oogenesis84,85 following the final round of endoreplication. As suggested earlier, the large numbers of copies of the D. melanogaster canonical histone genes may be necessary at this stage to produce sufficient amounts of protein.…”

Section: Regulation During Early Developmentmentioning

confidence: 99%

Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail

2008

View full text Add to dashboard Cite

The canonical histone proteins are encoded by replication-dependent genes and must rapidly reach high levels of expression during S phase. In metazoans the genes that encode these proteins produce mRNAs that, instead of being polyadenylated, contain a unique 3' end structure. By contrast, the synthesis of the variant, replication-independent histones, which are encoded by polyadenylated mRNAs, persists outside of S phase. Accurate positioning of both histone types in chromatin is essential for proper transcriptional regulation, the demarcation of heterochromatic boundaries and the epigenetic inheritance of gene expression patterns. Recent results suggest that the coordinated synthesis of replication-dependent and variant histone mRNAs is achieved by signals that affect formation of the 3' end of the replication-dependent histone mRNAs.Histones are the primary protein component of chromatin. Although they were initially thought to be mainly involved in chromosomal DNA packaging in eukaryotes, it is now recognized that they also have a crucial role in regulating gene expression. Histones can be extensively modified after translation and these modifications play an important part in regulating gene expression. They are constantly being shifted, modified, evicted and re-deposited as chromatin is continually remodelled (reviewed in REF. 1 ). Thus, the cell must carefully coordinate the replication of DNA, the synthesis of an estimated 10 8 molecules of each histone type in mammalian cells and the rapid deposition of new and old histones to reform chromatin during each relatively short S phase 2,3 .In metazoans the bulk of the histone proteins, defined here as the canonical histone proteins, are encoded by a family of replication-dependent histone genes. Their mRNAs are the only known cellular non-polyadenylated mRNAs in eukaryotes 4 . These genes encode all four core histones -H2A, H2B, H3 and H4 -which make up the nucleosome, and the linker H1 histones, which are found between nucleosomes. In place of a poly(A) tail, replicationdependent histone mRNAs end in a 3′ stem-loop sequence that is crucial in their regulation (FIG. 1a), and is formed by endonu-cleolytic cleavage of the pre-mRNA (FIG. 1b). This novel 3′ end results in the requirement for a distinct set of factors for metabolism and regulation of these histone mRNAs. These mRNAs must be expressed rapidly at the beginning of S phase and must persist at high levels throughout S phase to coincide with the replication of DNA. They are destroyed at the conclusion of S phase or rapidly during S phase if DNA replication is halted.In addition to the canonical histones, there are several variant histones whose synthesis is not cell-cycle-regulated and whose mRNAs are polyadenylated and expressed throughout the cell cycle (replication-independent histone mRNAs). These histones include the H3.3 and Correspondence to W.F.M.

show abstract

Section: Regulation During Early Developmentmentioning

confidence: 99%

Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail

2008

View full text Add to dashboard Cite

show abstract

“…The Drosophila egg contains high levels of maternally deposited histones incorporated into chromatin during the rapid cell cycles in the early embryo. It is therefore not surprising that some of these pre-deposition histones are modified (Walker and Bownes 1998).…”

Section: Pre-deposition Mono-and Trimethylated H4-k20mentioning

confidence: 99%

Free and chromatin-associated mono-, di-, and trimethylation of histone H4-lysine 20 during development and cell cycle progression

Karachentsev

Druzhinina

Steward

2007

Developmental Biology

View full text Add to dashboard Cite

Methylation of specific amino acids in histone tails is responsible for packaging DNA into condensed, repressed chromatin, and into open chromatin that is accessible to the transcription machinery. Monomethylation and trimethylation of histone H4-lysine 20 (H4-K20) control the formation of repressed chromatin. Using antibodies that specifically recognize the three methyl marks of histone H4-K20, we characterized their regulation during the cell cycle and throughout development. We find free mono- and trimethylated histone H4-K20 in unfertilized Drosophila eggs and in S2 tissue culture cells. Soluble mono-. di-, and trimethylated H4-K20 are also found in HeLa cells. These soluble modified histones may represent a pool of free histones that can rapidly be incorporated into chromatin. The three methyl marks are each regulated differentially during development and their detection on western blots does not overlap with their detection on chromosomes. Monomethylated H4-K20 is detected on condensed chromosomes throughout development, while di- and trimethylated H4-K20 are detected on metaphase chromosomes at specific stages. Our results suggest that the detection of methylated H4-K20 on chromosomes may reveal chromatin packaging rather than the distribution of the methyl marks.

show abstract

“…Histone mRNA accumulation during endocycles correlates with S phase (Sullivan et al 2001). Because the cells do not replicate in synchrony, this appears as a mosaic in situ hybridization staining pattern in both nurse cells and follicle cells using a histone H3 coding probe (Ambrosio and Schedl 1985;Ruddell and JacobsLorena 1985;Walker and Bownes 1998; Fig. 7A).…”

Section: Loss Of U7 and Slbp Affects Drosophila Development Differentlymentioning

confidence: 99%

“…The first is replication dependent and results in the accumulation of histone mRNA specifically during S phase. The second is a burst of replication-independent nurse cell expression late in oogenesis that generates the maternal mRNAs that are transported to the oocyte (Ambrosio and Schedl 1985;Ruddell and Jacobs-Lorena 1985;Walker and Bownes 1998). Both modes of expression are affected by mutation of Slbp.…”

Section: U7 and Slbp Are Required During Oogenesismentioning

confidence: 99%

U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis

Godfrey

Kupsco²,

Burch³

et al. 2006

RNA

View full text Add to dashboard Cite

Metazoan replication-dependent histone mRNAs are not polyadenylated, and instead terminate in a conserved stem-loop structure generated by an endonucleolytic cleavage involving the U7 snRNP, which interacts with histone pre-mRNAs through base-pairing between U7 snRNA and a purine-rich sequence in the pre-mRNA located downstream of the cleavage site. Here we generate null mutations of the single Drosophila U7 gene and demonstrate that U7 snRNA is required in vivo for processing all replication-associated histone pre-mRNAs. Mutation of U7 results in the production of poly A + histone mRNA in both proliferating and endocycling cells because of read-through to cryptic polyadenylation sites found downstream of each Drosophila histone gene. A similar molecular phenotype also results from mutation of Slbp, which encodes the protein that binds the histone mRNA 3¢ stem-loop. U7 null mutants develop into sterile males and females, and these females display defects during oogenesis similar to germ line clones of Slbp null cells. In contrast to U7 mutants, Slbp null mutations cause lethality. This may reflect a later onset of the histone pre-mRNA processing defect in U7 mutants compared to Slbp mutants, due to maternal stores of U7 snRNA. A double mutant combination of a viable, hypomorphic Slbp allele and a viable U7 null allele is lethal, and these double mutants express polyadenylated histone mRNAs earlier in development than either single mutant. These data suggest that SLBP and U7 snRNP cooperate in the production of histone mRNA in vivo, and that disruption of histone pre-mRNA processing is detrimental to development.

show abstract

The expression of histone genes during Drosophila melanogaster oogenesis

Cited by 10 publications

References 20 publications

Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail

Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail

Free and chromatin-associated mono-, di-, and trimethylation of histone H4-lysine 20 during development and cell cycle progression

U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis

Contact Info

Product

Resources

About