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Homeostasis in the Central Dogma of molecular biology: the importance of mRNA instability

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Pages 1659-1666 | Received 04 Apr 2019, Accepted 04 Aug 2019, Published online: 02 Sep 2019

References

  • Marguerat S, Schmidt A, Codlin S, et al. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell. 2012;151(3):671–683.
  • Neurohr GE, Terry RL, Lengefeld J, et al. Excessive cell growth causes cytoplasm dilution and contributes to senescence. Cell. 2019;176(5):1083–1097.e18.
  • Crick FH. On protein synthesis. Symp Soc Exp Biol. 1958;12:138–163.
  • Liebermeister W, Noor E, Flamholz A, et al. Visual account of protein investment in cellular functions. Proc Natl Acad Sci U S A. 2014;111(23):8488–8493.
  • Milo R, Phillips R. Cell biology by the numbers. 1sted. New York: Garland Science; 2015. ISBN 9780815345374.
  • Benet M, Miguel A, Carrasco F, et al. Modulation of protein synthesis and degradation maintains proteostasis during yeast growth at different temperatures. Biochim Biophys Acta Gene Regul Mech. 2017;1860(7):794–802.
  • Pérez-Ortín JE, Alepuz P, Chávez S, et al. Eukaryotic mRNA decay: methodologies, pathways, and links to other stages of gene expression. J Mol Biol. 2013;425(20):3750–3775.
  • García-Martínez J, Delgado-Ramos L, Ayala G, et al. The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons. Nucleic Acids Res. 2016;44(8):3643–3658.
  • Haimovich G, Medina DA, Causse SZ, et al. Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell. 2013;153(5):1000–1111.
  • Mena A, Medina DA, García-Martínez J, et al. Asymmetric cell division requires specific mechanisms for adjusting global transcription. Nucleic Acids Res. 2017;45(21):12401–12412.
  • Hausser J, Mayo A, Keren L, et al. Central dogma rates and the trade-off between precision and economy in gene expression. Nat Commun. 2019;10(1):68.
  • Raser JM, O’Shea EK. Noise in gene expression: origins, consequences, and control. Science. 2005;309(5743):2010–2013.
  • Warner JR. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci. 1999;24(11):437–440.
  • Waldron C, Lacroute F. Effect of growth rate on the amounts of ribosomal and transfer ribonucleic acids in yeast. J Bacteriol. 1975;122(3):855–865.
  • Pelechano V, Chávez S, Pérez-Ortín JE. A complete set of nascent transcription rates for yeast genes. PLoS One. 2010;5(11):e15442.
  • Dujon B. The yeast genome project: what did we learn? Trends Genet. 1996;12(7):263–270.
  • Milo R. What is the total number of protein molecules per cell volume? A call to rethink some published values. Bioessays. 2013;35(12):1050–1055.
  • Milo R, Jorgensen P, Moran U, et al. BioNumbers–the database of key numbers in molecular and cell biology. Nucleic Acids Res. 2010;38:D750–3. (Database issue). .
  • Lange HC, Heijnen JJ. Statistical reconciliation of the elemental and molecular biomass composition of Saccharomyces cerevisiae. Biotechnol Bioeng. 2001;75(3):334–344.
  • Schönheit P, Buckel W, Martin WF. On the origin of heterotrophy. Trends Microbiol. 2016;24(1):12–25.
  • Swanson M, Reguera G, Schaechter M, et al. Microbe. Washington (DC): ASM Press; 2016. ISBN-10: 1555819125.
  • Lodish H. Molecular cell biology. 5th. New York: W. H. Freeman & Co Ltd; 2003. ISBN-10: 0716743663.
  • Neymotin B, Athanasiadou R, Gresham D. Determination of in vivo RNA kinetics using RATE-seq . RNA. 2014;20(10):1645–1652.
  • von der Haar T. A quantitative estimation of the global translational activity in logarithmically growing yeast cells. BMC Syst Biol. 2008;2:87.
  • Wagner A. Energy constraints on the evolution of gene expression. Mol Biol Evol. 2005;22(6):1365–1374.
  • Tani H, Akimitsu N. Genome-wide technology for determining RNA stability in mammalian cells: historical perspective and recent advantages based on modified nucleotide labeling. RNA Biol. 2012;9(10):1233–1238.
  • Yang E. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res. 2003;13(8):1863–1872.
  • Chávez S, García-Martínez J, Delgado-Ramos L, et al. The importance of controlling mRNA turnover during cell proliferation. Curr Genet. 2016;62(4):701–710.
  • Christiano R, Nagaraj N, Fröhlich F, et al. Global proteome turnover analyses of the Yeasts S. cerevisiae and S. pombe. Cell Rep. 2014;9(5):1959–1965.
  • Wiechecki K, Manohar S, Silva G, et al. Integrative meta-analysis reveals that most yeast proteins are very stable. bioRxiv. 2017;165290. DOI:10.1101/165290.
  • Zhang T, Wolfe C, Pierle A, et al. Proteome-wide modulation of degradation dynamics in response to growth arrest. Proc Natl Acad Sci U S A. 2017;114(48):E10329–E10338.
  • Li JJ, Biggin MD. Gene expression. Statistics requantitates the central dogma. Science. 2015;347(6226):1066–1067.
  • Arava Y, Wang Y, Storey JD, et al. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2003;100(7):3889–3894.
  • Brandt F, Etchells SA, Ortiz JO, et al. The native 3D organization of bacterial polysomes. Cell. 2009;136(2):261–271.
  • Chu D, von der Haar T. The architecture of eukaryotic translation. Nucleic Acids Res. 2012;40(20):10098–10106.
  • Shah P, Ding Y, Niemczyk M, et al. Rate-limiting steps in yeast protein translation. Cell. 2013;153(7):1589–1601.
  • Tarrant D, von der Haar T. Synonymous codons, ribosome speed, and eukaryotic gene expression regulation. Cell Mol Life Sci. 2014;71(21):4195–4206.
  • Kafri M, Metzl-Raz E, Jona G, et al. The cost of protein production. Cell Rep. 2016;14(1):22–31.
  • Metzl-Raz E, Kafri M, Yaakov G, et al. Principles of cellular resource allocation revealed by condition-dependent proteome profiling. Elife. 2017;6:e28034.
  • Radonjic M, Andrau JC, Lijnzaad P, et al. Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol Cell. 2005;18(2):171–183.
  • Metzl-Raz E, Kafri M, Yaakov G, et al. Gene transcription as a limiting factor in protein production and cell growth. BioRxiv. 2019. DOI:10.1101/626242
  • Newman JR, Ghaemmaghami S, Ihmels J, et al. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature. 2006;441:840–846.
  • Bar-Even A, Paulsson J, Maheshri N, et al. Noise in protein expression scales with natural protein abundance. Nat Genet. 2006;38(6):636–643.
  • Pérez-Ortín JE, Alepuz PM, Moreno J. Genomics and gene transcription kinetics in yeast. Trends Genet. 2007;23(5):250–257.
  • Dworkin JP, Lazcano A, Miller SL. The roads to and from the RNA world. J Theor Biol. 2003;222(1):127–134.
  • Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;362:709–715.
  • Bakshi S, Siryaporn A, Goulian M, et al. Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol. 2012;85(1):21–38.
  • Bartholomäus A. Bacteria differently regulate mRNA abundance to specifically respond to various stresses. Philos Trans A Math Phys Eng Sci. 2016;374(2063):20150069.
  • Bremer H, Dennis PP. Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt, et al. editor. Escherichia coli and Salmonella typhimurium: cellular and molecular biology. 2nd. Washington (DC): ASM Press; 1996. 1559. chapter 97.
  • Grossman N, Ron EZ, Woldringh CL. Changes in cell dimensions during amino acid starvation of Escherichia coli. J Bacteriol. 1982;152(1):35–41.
  • Ho B, Baryshnikova A, Brown GW. Unification of protein abundance datasets yields a quantitative saccharomyces cerevisiae proteome. Cell Syst. 2018;6(2):192–205.e3.
  • Zenklusen D, Larson DR, Singer RH. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat Struct Mol Biol. 2008;15:1263–1271.
  • Maclean N. Ribosome numbers in a fission yeast. Nature. 1965;207:322–323.
  • Sun M, Schwalb B, Schulz D, et al. Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res. 2012;J22(7):1350–1359.
  • Carter MG, Sharov AA, VanBuren V, et al. Transcript copy number estimation using a mouse whole-genome oligonucleotide microarray. Genome Biol. 2005;6:R61.
  • Schwanhäusser B, Busse D, Li N, et al. Global quantification of mammalian gene expression control. Nature. 2011;473:337–342.
  • Siwiak M, Zielenkiewicz P. Transimulation - protein biosynthesis web service. PloS ONE. 2013 Sep 05;8(9):e73943. .
  • Velculescu VE, Madden SL, Zhang L, et al. Analysis of human transcriptomes. Nat Genet. 1999;23(4):387–388.
  • Kulak NA, Pichler G, Paron I, et al. Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat Methods. 2014;11(3):319–324.
  • PaxDb: protein abundance database. [cited 2019 Jun]. Available from: https://pax-db.org/
  • Mackie GA. RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol. 2013;11(1):45–57.
  • Moran MA, Satinsky B, Gifford SM, et al. Sizing up metatranscriptomics. Isme J. 2013;7(2):237–243.
  • Presnyak V, Alhusaini N, Chen YH, et al. Codon optimality is a major determinant of mRNA stability. Cell. 2015;160(6):1111–1124.

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