Synthesis of histone messenger RNA of HeLa cells during the cell cycle

Melli, Marialuisa; Spinelli, Giovanni; Arnold, Eva

doi:10.1016/0092-8674(77)90194-5

Cited by 76 publications

(22 citation statements)

References 20 publications

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“…Experiments described in this paper show that P mRNA decays with an approximate half-life of30 min within 1 hr after it appears and that degradation is a process requiring ongoing protein synthesis. Whether the increased levels of/3 mRNA in the absence ofprotein synthesis can be explained entirely by the increase in the half-life of the /3 mRNA (5) or whether in the presence of cycloheximide the rate of transcription is altered as well (28) (29,30). It is interesting to note, but may only be coincidental, that both interferon and histone mRNAs belong to the rare class of unspliced mRNAs (31)(32)(33).…”

Section: Resultsmentioning

confidence: 99%

Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.

Raj¹,

Pitha²

1981

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

135

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The levels of interferon mRNA as a function of interferon induction by poly(rI)-poly(rC) in human fibroblast cells were determined by RNA hybridization using a cloned 13 interferon cDNA and by translation in Xenopus oocytes. Whereas previous studies analyzed mixtures of interferons, the availability of the cloned 13 interferon cDNA and the antiserum to purified 13 interferon enabled us to focus on the expression of only one class (13) of interferon genes. The induction of interferon synthesis depends primarily on the accumulation of interferon 13 mRNA in the cells, and the interferon 13 mRNA rapidly disappears several hours after its appearance in the cytoplasm. No detectable interferon 13 mRNA sequences are present in uninduced cells. The degradation ofinterferon 13 mRNA in the induced cells requires ongoing protein synthesis; accumulation of interferon 13 mRNA was observed in the continuous presence of cycloheximide. The interferon 13 mRNA detected at the early stages of induction is 1100 nucleotides long and its size progressively decreases with time. By both the hybridization and the translational assay in Xenopus oocytes, only one size of interferon 13 mRNA and one species of 13 interferon could be identified.

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Section: Resultsmentioning

confidence: 99%

Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.

Raj¹,

Pitha²

1981

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

135

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“…However, other studies with HeLa cells suggested that transcription of histone genes occurs throughout the cell cycle. Using cloned sea urchin histone DNA as a hybridization probe, Melli et al (19) found equal amounts of high-molecular-weight hybridizable RNA in HeLa cells at various times after release from a thymidine block as well as in cells treated with a DNA synthesis inhibitor. Still other, more recent work has suggested that post-translational controls may be important in regulating the deposition of newly synthesized histones in chromatin.…”

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confidence: 99%

Cell cycle regulation of mouse H3 histone mRNA metabolism.

Alterman

Ganguly²,

Schulze³

et al. 1984

Mol. Cell. Biol.

175

108

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The mechanisms responsible for the periodic accumulation and decay of histone mRNA in the mammalian cell cycle were investigated in mouse erythroleukemia cells, using a cloned mouse H3 histone gene probe that hybridizes with most or all H3 transcripts. Exponentially growing cells were fractionated into cell cycle-specific stages by centrifugal elutriation, a method for purifying cells at each stage of the cycle without the use of treatments that arrest growth. Measurements of H3 histone mRNA content throughout the cell cycle show that the mRNA accumulates gradually during S phase, achieving its highest value in mid-S phase when DNA synthesis is maximal. The mRNA content then decreases as cells approach G2. These results demonstrate that the periodic synthesis of histones during S phase is due to changes in the steady-state level of histone mRNA. They are consistent with the conventional view in which histone synthesis is regulated coordinately with DNA synthesis in the cell cycle. The periodic accumulation and decay of H3 histone mRNA appear to be controlled primarily by changes in the rate of appearance of newly synthesized mRNA in the cytoplasm, determined by pulse-labeling whole cells with [3HJuridine. Measurements of H3 mRNA turnover by pulse-chase experiments with cells in S and G2 did not provide evidence for changes in the cytoplasmic stability of the mRNA during the period of its decay in late S and G2. Furthermore, transcription measurements carried out by brief pulse-labeling in vivo and by in vitro transcription in isolated nuclei indicate that the rate of H3 gene transcription changes to a much smaller extent than the steady-state levels of the mRNA or the appearance of newly synthesized mRNA in the cytoplasm. The results suggest that post-transcriptional processes make an important contribution to the periodic accumulation and decay of histone mRNA and that these processes may operate within the nucleus.The biosynthesis of histones is generally thought to occur periodically in the cell cycle and to be tightly coupled to DNA replication. Early studies utilizing synchronized HeLa cells showed that newly synthesized histones could be found associated with chromatin only in S-phase cells (2,14,27). These cells contained an abundance of small polyribosomes with nascent polypeptides that comigrated with histones in gel electrophoresis; these small polysomes were not apparent in G1 cells (2). When cells undergoing DNA replication are treated with inhibitors of DNA synthesis there is a rapid loss of histone production (2, 4). Gallwitz and Mueller (8) showed that histone proteins were not synthesized in vitro on microsomes isolated from such cells, and Borun et al. (1) confirmed these results by a direct mRNA translation assay.Despite extensive investigations into the mechanisms responsible for the temporal pattern of histone synthesis in the cell cycle, there is still considerable disagreement concerning the level(s) at which histone protein synthesis is regulated. A number of studies support the view ...

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“…The level of cytoplasmic tubulin mRNA in colchicine-treated cells is regulated at the post-transcriptional level (6), as is the histone mRNA level in HeLa cells (30). The growth-dependent dihydrofolate reductase mRNA level is probably also determined by post-transcriptional events since the relative level of dihydrofolate reductase mRNA in growing cells is approximately 10-fold that in stationary cells in contrast to the 2-fold change in the relative transcription rate of the dihydrofolate reductase gene (22).…”

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confidence: 99%

Post-transcriptional regulation of the abundance of mRNAs encoding alpha-tubulin and a 94,000-dalton protein in teratocarcinoma-derived stem cells versus differentiated cells.

Howe¹,

Lugg²,

Overton³

1984

Mol. Cell. Biol.

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Changes in the expression of the genes encoding a-tubulin and a 94,000-dalton protein (p94) specified by a cDNA clone, p4-30, were examined in a differentiated teratocarcinoma-derived parietal endoderm cell line, PYS-2, and an undifferentiated teratocarcinoma stem cell line, F9. Relative to other proteins or mRNA species, the synthesis rate of the a-tubulins and of p94, as well as the levels of their corresponding cytoplasmic mRNAs, were lower in PYS-2 than in F9 cells. The decrease was greater for the relative abundance of cytoplasmic a-tubulin mRNA than for p94 mRNA. Similarly, induction of differentiation of F9 cells by simultaneous exposure to retinoic acid (RA) and dibutyryl cyclic AMP resulted in reduced relative levels of the cytoplasmic mRNAs for these proteins. The reduction in abundance of the two RNA species was not due to a decrease in growth rate since the differentiated cells, PYS-2, RA-treated F9, and RA plus dibutyryl cyclic AMP-treated F9 cells, grew at a rate similar to that of undifferentiated F9 cells. However, induction of differentiation of F9 cells by treatment with RA alone did not cause down-regulation of the two RNA species. The relative levels of total cellular RNA encoding ca-tubulin and p94 in PYS-2 cells were also lower than those in F9 cells to an extent comparable to the decrease in the cytoplasmic RNAs. Since the apparent relative rates of RNA transcription were similar in both cell types, we conclude that the reduction in relative levels of the a-tubulin and p94 RNAs in the cell depends largely on the relative stability of the two RNAs and not on the relative rates of transcription. The faster disappearance of the two RNA species relative to other cellular RNAs from actinomycin D-treated PYS-2 compared with F9 cells is consistent with this interpretation.Microtubules consist of two proteins, a-and ,B-tubulin, each shown in human, chicken, and Drosophila melanogaster to contain several distinct genes (7,8,10,20,37,46). In D. melanogaster, members of the a-and P-tubulin multigene families are differentially expressed during embryonic development and in different adult tissues (21,23,31,35). However, little is known about the regulation of synthesis of these proteins during murine embryogenesis, though changes in protein synthesis have been demonstrated (17) to occur during early embryonic development. A recent study (9) showed that treatment of Chinese hamster ovary cells with the microtubule-depolymerizing drug colchicine resulted in the specific and rapid loss of tubulin mRNA from the cytoplasm. It was suggested that this loss of tubulin mRNA was probably not achieved through a transcriptionally regulated mechanism since the relative rates of tubulin RNA transcription are essentially unchanged in isolated nuclei derived from colchicine-treated and untreated control cells (6). In contrast, expression of globin genes in a hemintreated human erythroid cell line (5) and of a-fetoprotein and albumin genes in liver from late prenatal to 1-month-postpartum mice (43) is regulated primar...

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Synthesis of histone messenger RNA of HeLa cells during the cell cycle

Cited by 76 publications

References 20 publications

Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.

Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.

Cell cycle regulation of mouse H3 histone mRNA metabolism.

Post-transcriptional regulation of the abundance of mRNAs encoding alpha-tubulin and a 94,000-dalton protein in teratocarcinoma-derived stem cells versus differentiated cells.

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