Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts - PubMed (original) (raw)
Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts
P K Geyer et al. Mol Cell Biol. 1982 Jun.
Abstract
When resting (G0) mouse 3T6 fibroblasts are serum stimulated to reenter the cell cycle, the rates of synthesis of rRNA and ribosomal proteins increase, resulting in an increase in ribosome content beginning about 6 h after stimulation. In this study, we monitored the content, metabolism, and translation of ribosomal protein mRNA (rp mRNA) in resting, exponentially growing, and serum-stimulated 3T6 cells. Cloned cDNAs for seven rp mRNAs were used in DNA-excess filter hybridization studies to assay rp mRNA. We found that about 85% of rp mRNA is polyadenylated under all growth conditions. The rate of labeling of rp mRNA relative to total polyadenylated mRNA changed very little after stimulation. The half-life of rp mRNA was about 11 h in resting cells and about 8 h in exponentially growing cells, values which are similar to the half-lives of total mRNA in resting and growing cells (about 9 h). The content of rp mRNA relative to total mRNA was about the same in resting and growing 3T6 cells. Furthermore, the total amount of rp mRNA did not begin to increase until about 6 h after stimulation. Since an increase in rp mRNA content did not appear to be responsible for the increase in ribosomal protein synthesis, we determined the efficiency of translation of rp mRNA under different conditions. We found that about 85% of pulse-labeled rp mRNA was associated with polysomes in exponentially growing cells. In resting cells, however, only about half was associated with polysomes, and about 30% was found in the monosomal fraction. The distribution shifted to that found in growing cells within 3 h after serum stimulation. Similar results were obtained when cells were labeled for 10.5 h. About 70% of total polyadenylated mRNA was in the polysome fraction in all growth states regardless of labeling time, indicating that the shift in mRNA distribution was species specific. These results indicate that the content and metabolism of rp mRNA do not change significantly after growth stimulation. The rate of ribosomal protein synthesis appears to be controlled during the resting-growing transition by an alteration of the efficiency of translation of rp mRNA, possibly at the level of protein synthesis initiation.
Similar articles
- Absence of control of poly(A)(+) messenger RNA translation in growth-stimulated mouse 3T6 fibroblasts.
Pratt RE, Johnson LF. Pratt RE, et al. Biochim Biophys Acta. 1980 Jul 29;608(2):332-43. doi: 10.1016/0005-2787(80)90179-3. Biochim Biophys Acta. 1980. PMID: 7397189 - Oral administration of leucine stimulates ribosomal protein mRNA translation but not global rates of protein synthesis in the liver of rats.
Anthony TG, Anthony JC, Yoshizawa F, Kimball SR, Jefferson LS. Anthony TG, et al. J Nutr. 2001 Apr;131(4):1171-6. doi: 10.1093/jn/131.4.1171. J Nutr. 2001. PMID: 11285321 - In vitro and in vivo analysis of the control of dihydrofolate reductase gene transcription in serum-stimulated mouse fibroblasts.
Santiago C, Collins M, Johnson LF. Santiago C, et al. J Cell Physiol. 1984 Jan;118(1):79-86. doi: 10.1002/jcp.1041180114. J Cell Physiol. 1984. PMID: 6690454 - TOPs and their regulation.
Hamilton TL, Stoneley M, Spriggs KA, Bushell M. Hamilton TL, et al. Biochem Soc Trans. 2006 Feb;34(Pt 1):12-6. doi: 10.1042/BST20060012. Biochem Soc Trans. 2006. PMID: 16246169 Review. - Translational control of ribosomal protein production in mammalian cells.
Perry RP, Meyuhas O. Perry RP, et al. Enzyme. 1990;44(1-4):83-92. doi: 10.1159/000468749. Enzyme. 1990. PMID: 2133661 Review.
Cited by
- LARP1 senses free ribosomes to coordinate supply and demand of ribosomal proteins.
Saba JA, Huang Z, Schole KL, Ye X, Bhatt SD, Li Y, Timp W, Cheng J, Green R. Saba JA, et al. bioRxiv [Preprint]. 2023 Nov 2:2023.11.01.565189. doi: 10.1101/2023.11.01.565189. bioRxiv. 2023. PMID: 37961604 Free PMC article. Preprint. - RIOK2 phosphorylation by RSK promotes synthesis of the human small ribosomal subunit.
Cerezo EL, Houles T, Lié O, Sarthou MK, Audoynaud C, Lavoie G, Halladjian M, Cantaloube S, Froment C, Burlet-Schiltz O, Henry Y, Roux PP, Henras AK, Romeo Y. Cerezo EL, et al. PLoS Genet. 2021 Jun 14;17(6):e1009583. doi: 10.1371/journal.pgen.1009583. eCollection 2021 Jun. PLoS Genet. 2021. PMID: 34125833 Free PMC article. - The mTOR regulated RNA-binding protein LARP1 requires PABPC1 for guided mRNA interaction.
Smith EM, Benbahouche NEH, Morris K, Wilczynska A, Gillen S, Schmidt T, Meijer HA, Jukes-Jones R, Cain K, Jones C, Stoneley M, Waldron JA, Bell C, Fonseca BD, Blagden S, Willis AE, Bushell M. Smith EM, et al. Nucleic Acids Res. 2021 Jan 11;49(1):458-478. doi: 10.1093/nar/gkaa1189. Nucleic Acids Res. 2021. PMID: 33332560 Free PMC article. - The Exon Junction Complex Undergoes a Compositional Switch that Alters mRNP Structure and Nonsense-Mediated mRNA Decay Activity.
Mabin JW, Woodward LA, Patton RD, Yi Z, Jia M, Wysocki VH, Bundschuh R, Singh G. Mabin JW, et al. Cell Rep. 2018 Nov 27;25(9):2431-2446.e7. doi: 10.1016/j.celrep.2018.11.046. Epub 2018 Nov 19. Cell Rep. 2018. PMID: 30466796 Free PMC article. - LARP1 on TOP of ribosome production.
Fonseca BD, Lahr RM, Damgaard CK, Alain T, Berman AJ. Fonseca BD, et al. Wiley Interdiscip Rev RNA. 2018 Sep;9(5):e1480. doi: 10.1002/wrna.1480. Epub 2018 May 2. Wiley Interdiscip Rev RNA. 2018. PMID: 29722158 Free PMC article. Review.
References
- Nature. 1974 Oct 4;251(5474):385-8 - PubMed
- Proc Natl Acad Sci U S A. 1973 Oct;70(10):2819-22 - PubMed
- Eur J Biochem. 1980 Jun;107(2):323-9 - PubMed
- Cell. 1980 Sep;21(2):523-35 - PubMed
- Proc Natl Acad Sci U S A. 1980 Sep;77(9):5140-4 - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources