Differential expression of early and late embryonic histone genes in adult tissues of the sea urchin Strongylocentrotus purpuratus

Halsell, Susan R.; Ito, Masamichi; Maxson, Rob

doi:10.1016/0012-1606(87)90228-4

Cited by 16 publications

(6 citation statements)

References 20 publications

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“…pSpL-1 is a genomic segment containing the late H4 and late H2b histone genes inserted in pBR322 (27) Figure 2 shows the results of a primer extension analysis of the early and late H2b transcription products. Oocytes that had received the early H2b genes contained an RNA species whose extension product comigrated with a product previously shown to be that of the early H2b mRNA (17 (Fig. 5A, lane 6; Fig.…”

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confidence: 60%

Differential stimulation of sea urchin early and late H2B histone gene expression by a gastrula nuclear extract after injection into Xenopus laevis oocytes.

Maxson¹,

Ito²,

Balcells³

et al. 1988

Mol. Cell. Biol.

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Sea urchin early histone genes are active in preblastula embryos; late histone genes are maximafly expressed during subsequent stages of embryogenesis. We used the Xenopus laevis oocyte to assay for trans-acting factors involved in this differential regulation. Sea urchin nuclear proteins were prepared by extracting gastrula-stage chromatin successively with 0.45, 1, and 2 M NaCl. We injected three fractions into oocytes along with plasmids bearing sea urchin early and late H2b histone genes. While neither the 0 to 0.45 M nor the 1 to 2 M salt fraction affected H2b gene expression, the 0.45 to 1 M salt fraction stimulated early and late H2b mRNA levels significantly. Late H2b gene expression was stimulated preferentially when the early and late genes were coinjected into the same oocytes. This extract did not stimulate the accumulation of transcripts of injected herpesvirus thymidine kinase genes or of the sea urchin Spec 1 gene, suggesting that the stimulatory activity is not a general transcription factor. We localized the DNA sequence required for the stimulatory effect to a region of the late H2b gene located between -43 and +62 relative to the transcription start site. A component of the 0.45 to 1 M salt wash fraction specifically bound to the 105-base-pair late gene DNA sequence and to the corresponding early gene fragment. The abundance of this binding activity decreased on a per genome basis during early development of the sea urchin.The sea urchin synthesizes several distinct sets of histone proteins during early embryogenesis (7, 32). These include early isotypes, synthesized from fertilization to the blastula stage, and late isotypes, synthesized from the blastula stage onward. Each set of proteins is encoded by a distinct class of genes. Early histone genes are repeated several hundredfold in the genome and are organized in tandem quintets, each comprising genes for the five major histone types. In contrast, late histone genes are present in only 6 to 12 copies per genome and are arranged in irregular clusters (6,21,22,27). The developmental switches in the synthesis of early and late histone isotypes are caused largely by changes in rates of transcription of the two gene sets (23,28,35).The Xenopus laevis oocyte has proven highly useful in the analysis of transcriptional processes (9, 10). A variety of genes, including histone genes, are accurately transcribed after microinjection into oocyte nuclei, and the injection of genes with mutated promoter regions has enabled the identification of elements required for transcription in the oocyte (16). The Xenopus oocyte system has also been used to identify a trans-acting factor involved in the processing of sea urchin histone mRNAs (34) and, more recently, to identify a factor capable of stimulating sea urchin early H2b gene transcription (30).We used the Xenopus oocyte to examine the mechanisms underlying the differential expression of sea urchin early and late histone genes. We found that an extract of sea urchin gastrula-stage chromatin stimulated the ...

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confidence: 60%

Differential stimulation of sea urchin early and late H2B histone gene expression by a gastrula nuclear extract after injection into Xenopus laevis oocytes.

Maxson¹,

Ito²,

Balcells³

et al. 1988

Mol. Cell. Biol.

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“…In contrast to the early genes, the late genes might be expected to have gene-specific cis-acting elements. The timing of expression of the different late genes coding for a particular histone type is not coordinate (2,26,(29)(30)(31)49), and in some cases there is specificity of expression of subtypes in particular adult tissues (19,30,40). The promoters of such genes would be expected to be complex, and it is not surprising that the promoter of the one late gene analyzed in detail thus far, the Hi-p gene of S. purpuratus, contains a variety of 5' elements essential for maximal activity (39), one of which appears to be a stage-specific enhancer (38).…”

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confidence: 99%

UHF-1, a factor required for maximal transcription of early and late sea urchin histone H4 genes: analysis of promoter-binding sites.

Lee¹,

Tung²,

Bumcrot³

et al. 1991

Mol. Cell. Biol.

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A protein, denoted UHF-1, was found to bind upstream of the transcriptional start site of both the early and late H4 (EH4 and LH4) histone genes of the sea urchin Strongylocentrotus purpuratus. A nuclear extract from hatching blastulae contained proteins that bind to EH4 and LH4 promoter fragments in a band shift assay and produced sharp DNase I footprints upstream of the EH4 gene (from -133 to -106) and the LH4 gene (from -94 to -66). DNase I footprinting performed in the presence of EH4 and LH4 promoter competitor DNAs indicated that UHF-1 binds more strongly to the EH4 site. A sequence match of 11 of 13 nucleotides was found within the two footprinted regions: AGGGGGCGCACTC. Methylation interference and footprinting experiments showed that UHF-1 bound to the two sites somewhat differently. DNA-protein UV cross-linking studies indicated that UHF-1 has an electrophoretic mobility on sodium dodecyl sulfate-acrylamide gels of approximately 85 kDa and suggested that additional proteins, specific to each promoter, bind to each site. In vitro and in vivo assays were used to demonstrate that the UHF-1-binding site is essential for maximal transcription of the H4 genes. Deletion of the EH4 footprinted region resulted in a 3-fold decrease in transcription in a nuclear extract and a 2.6-fold decrease in expression in morulae from templates that had been injected into eggs. In the latter case, deletion of the binding site did not grossly disrupt the temporal program of expression from the injected EH4 genes. LH4 templates containing a 10-bp deletion in the consensus region or base substitutions in the footprinted region were transcribed at 14 to 58% of the level of the wild-type LH4 template. UHF-1 is therefore essential for maximal expression of the early and late H4 genes.The sea urchin genome contains several histone gene sets which are differentially regulated during development (reviewed in references 23 and 43). The early embryonic genes, organized as a unit containing a gene for each of the five histones, are reiterated several hundred-fold per haploid genome in a tandem array. The late gene set of each haploid genome is composed of 5 to 12 genes for each nucleosomal histone (4,29,30,42) and at least two Hi genes (32,33,37), organized in small irregular clusters or found as single genes. The amount of early RNA increases approximately 10-fold from the 16-cell stage to early blastula and then decreases rapidly so that little early histone mRNA remains by the gastrula stage (41,46,67). Late gene transcripts are found at low levels in the egg and, depending on the particular gene, increase to maximum levels at the mid-blastula and later stages (2,3,18,24,29,31,32,37,42,49). Nuclear run-on assays indicate that the basis of these changes in mRNA levels is predominantly transcriptional; during blastulation, early gene template activity decreases and late gene transcription increases (31,62,70). Measurements of histone RNA synthesis rate and turnover in intact embryos are consistent with changes in the level of transcrip...

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“…The somatic late histone genes are expressed in all adult tissues, whereas the expression of other late histone genes appears to be restricted to embryonic and larval development (Kemler and Busslinger 1986;Lieber et al 1986;Halsell et al 1987). The tissue-specific class of late histone genes so far consists of two nonallelic pairs of late H2A and H2B genes that we have isolated previously on two different cosmid clones from the sea urchin Psammechinus miliaris (Kemler and Busslinger 1986;Fig.…”

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confidence: 99%

Developmental and tissue-specific regulation of a novel transcription factor of the sea urchin.

Barberis

Superti‐Furga²,

Vitelli³

et al. 1989

Genes Dev.

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We have identified a novel transcription factor that interacts with the promoter of four tissue-specific late histone H2A-2 and H2B-2 genes of the sea urchin by DNase I footprint, mobility shift, and methylation interference analyses. The binding site for this factor is required for efficient transcription of the H2B-2.1 gene both in vitro in nuclear extracts of gastrula embryos and in vivo in microinjected sea urchin embryos. This factor binds with equal affinity to the recognition sequences of all four histone genes in cross-competition assays. Moreover, the binding site of the H2B-2.2 promoter can functionally substitute for that of the H2B-2.1 gene in in vivo expression experiments. Nevertheless, all four binding sites share little sequence homology with each other. This transcription factor increases in abundance during embryogenesis and has been detected in the adult sea urchin only in the tube feet, where the late H2A-2 and H2B-2 genes are expressed specifically. Therefore, we refer to this factor as tissue-specific activator protein (TSAP). The close correlation between the presence of TSAP and the expression pattern of the late H2A-2 and H2B-2 genes suggests that this transcription factor is directly responsible for the developmental and tissue-specific regulation of these genes.

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Differential expression of early and late embryonic histone genes in adult tissues of the sea urchin Strongylocentrotus purpuratus

Cited by 16 publications

References 20 publications

Differential stimulation of sea urchin early and late H2B histone gene expression by a gastrula nuclear extract after injection into Xenopus laevis oocytes.

Differential stimulation of sea urchin early and late H2B histone gene expression by a gastrula nuclear extract after injection into Xenopus laevis oocytes.

UHF-1, a factor required for maximal transcription of early and late sea urchin histone H4 genes: analysis of promoter-binding sites.

Developmental and tissue-specific regulation of a novel transcription factor of the sea urchin.

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