Abstract
We have examined the effects of protein synthesis inhibition on histone gene expression during the HeLa cell cycle. Histone mRNAs, which normally are rapidly degraded in the absence of DNA synthesis, persist and increase in concentration when translation is inhibited before DNA replication is halted. This is not a function of polysomal shielding of these mRNAs from active degradation mechanisms since inhibitors of translation initiation alone effect stabilization and induction. The superinduction of histone mRNAs by protein synthesis inhibition is effective at the G1/S border, and in the S-phase and non-S-phase periods of the cell cycle. However, the relative increase in histone mRNA is greater when cells not synthesizing DNA are treated with a protein synthesis inhibitor than when S-phase cells are so treated. Non-histone mRNAs examined are not superinduced by translation inhibition. Transcription rates from both histone and non-histone genes increase after protein synthesis inhibition. Although the decrease in histone gene transcription associated with DNA synthesis inhibition is prevented and reversed by protein synthesis inhibition, we have no evidence that histone gene-specific transcriptional regulation is dependent on protein synthesis. Transcriptional increases may contribute to the superinduction effect but cannot explain its differential extent during the cell cycle, since these increases are similar when replicating or nonreplicating cells are treated with a protein synthesis inhibitor. We believe that changes in histone mRNA stability can account for much of the differential superinduction effect. Our results indicate a requirement for continuing protein synthesis in the cell cycle regulation of histone mRNAs.
MeSH Terms
Aphidicolin
Cycloheximide/pharmacology
DNA-Directed RNA Polymerases/metabolism
Diterpenes/pharmacology
Gene Expression Regulation
HeLa Cells
Histones/genetics
Humans
Polyribosomes/metabolism
Protein Biosynthesis
RNA, Messenger/metabolism
Transcription, Genetic
Chemicals
Diterpenes
Histones
RNA, Messenger
Aphidicolin
Cycloheximide
DNA-Directed RNA Polymerases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sive H L
Heintz N
Roeder R G
References (23)
23 references, click to expand
-
Inhibition of protein synthesis in reticulocytes by antibiotics. I. Effects on polysomes.
Biochim Biophys Acta. 1966 Apr 18;119(1):109-19
PMID: 5960399
-
Mechanism of cycloheximide inhibition of protein synthesis in a cell-free system prepared from rat liver.
J Biol Chem. 1969 Aug 25;244(16):4480-9
PMID: 5806588
-
Histone synthesis in vitro on HeLa cell microsomes. The nature of the coupling to deoxyribonucleic acid synthesis.
J Biol Chem. 1969 Nov 10;244(21):5947-52
PMID: 5350949
-
Control of histone synthesis in HeLa cells.
Biochim Biophys Acta. 1973 Feb 4;294(1):481-96
PMID: 4705997
-
Fate of histone messenger RNA in synchronized HeLa cells in the absence of initiation of protein synthesis.
Eur J Biochem. 1977 Jan;72(2):385-92
PMID: 837922
-
Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes.
Cell. 1980 May;20(1):95-105
PMID: 6893015
-
Synchronization of HeLa cell cultures by inhibition of DNA polymerase alpha with aphidicolin.
Nucleic Acids Res. 1980 Jan 25;8(2):377-87
PMID: 6775308
-
Cell-cycle regulation of yeast histone mRNA.
Cell. 1981 May;24(2):367-75
PMID: 7016339
-
Mechanism of activation of early viral transcription by the adenovirus E1A gene product.
Cell. 1981 Oct;26(2 Pt 2):213-20
PMID: 7332929
-
Separation of basal histone synthesis from S-phase histone synthesis in dividing cells.
Cell. 1981 Dec;27(2 Pt 1):321-30
PMID: 7199388
-
Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.
Proc Natl Acad Sci U S A. 1981 Dec;78(12):7426-30
PMID: 6174973
-
Cycloheximide stimulates early adenovirus transcription if early gene expression is allowed before treatment.
J Virol. 1983 Feb;45(2):683-92
PMID: 6834470
-
Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation.
Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849-53
PMID: 6572946
-
Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle.
Mol Cell Biol. 1983 Apr;3(4):539-50
PMID: 6406835
-
Increased histone mRNA levels during inhibition of protein synthesis.
Biochem Biophys Res Commun. 1983 Jul 18;114(1):131-7
PMID: 6882419
-
Effect of adenovirus on metabolism of specific host mRNAs: transport control and specific translational discrimination.
Mol Cell Biol. 1983 Jul;3(7):1212-21
PMID: 6688459
-
Changes in liver-specific compared to common gene transcription during primary culture of mouse hepatocytes.
Mol Cell Biol. 1983 Sep;3(9):1552-61
PMID: 6633533
-
The primary structure and expression of four cloned human histone genes.
Nucleic Acids Res. 1983 Nov 11;11(21):7409-25
PMID: 6647026
-
Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor.
Cell. 1983 Dec;35(3 Pt 2):603-10
PMID: 6606489
-
Transcriptional activation and subsequent control of the human heat shock gene during adenovirus infection.
Mol Cell Biol. 1983 Nov;3(11):2058-65
PMID: 6689197
-
Rapid reversible changes in the rate of histone gene transcription and histone mRNA levels in mouse myeloma cells.
Mol Cell Biol. 1984 Feb;4(2):351-7
PMID: 6700595
-
Requirement of protein synthesis for the coupling of histone mRNA levels and DNA replication.
FEBS Lett. 1984 Mar 12;168(1):65-9
PMID: 6705922
-
Control of biologically active interleukin 2 messenger RNA formation in induced human lymphocytes.
Proc Natl Acad Sci U S A. 1984 May;81(9):2601-5
PMID: 6609365