The Lost Language of the RNA World

Overview

Journal Sci Signal

Specialties Cell Biology
Physiology
Science

Date 2017 Jun 15

PMID 28611182

Citations 56

Authors

James W Nelson

Ronald R Breaker

Affiliations

Soon will be listed here.

Abstract

The possibility of an RNA World is based on the notion that life on Earth passed through a primitive phase without proteins, a time when all genomes and enzymes were composed of ribonucleic acids. Numerous apparent vestiges of this ancient RNA World remain today, including many nucleotide-derived coenzymes, self-processing ribozymes, metabolite-binding riboswitches, and even ribosomes. Many of the most common signaling molecules and second messengers used by modern organisms are also formed from RNA nucleotides or their precursors. For example, nucleotide derivatives such as cAMP, ppGpp, and ZTP, as well as the cyclic dinucleotides c-di-GMP and c-di-AMP, are intimately involved in signaling diverse physiological or metabolic changes in bacteria and other organisms. We describe the potential diversity of this "lost language" of the RNA World and speculate on whether additional components of this ancient communication machinery might remain hidden though still very much relevant to modern cells.

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References

Koizumi M, Breaker R . Molecular recognition of cAMP by an RNA aptamer. Biochemistry. 2000; 39(30):8983-92. DOI: 10.1021/bi000149n. View

Kellenberger C, Wilson S, Sales-Lee J, Hammond M . RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J Am Chem Soc. 2013; 135(13):4906-9. PMC: 3775879. DOI: 10.1021/ja311960g. View

Sudarsan N, Lee E, Weinberg Z, Moy R, Kim J, Link K . Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science. 2008; 321(5887):411-3. PMC: 5304454. DOI: 10.1126/science.1159519. View

Romling U, Galperin M, Gomelsky M . Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 2013; 77(1):1-52. PMC: 3591986. DOI: 10.1128/MMBR.00043-12. View

Corrigan R, Grundling A . Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol. 2013; 11(8):513-24. DOI: 10.1038/nrmicro3069. View

Desch M, Schinner E, Kees F, Hofmann F, Seifert R, Schlossmann J . Cyclic cytidine 3',5'-monophosphate (cCMP) signals via cGMP kinase I. FEBS Lett. 2010; 584(18):3979-84. DOI: 10.1016/j.febslet.2010.07.059. View

Waters C, Bassler B . Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol. 2005; 21:319-46. DOI: 10.1146/annurev.cellbio.21.012704.131001. View

Potrykus K, Cashel M . (p)ppGpp: still magical?. Annu Rev Microbiol. 2008; 62:35-51. DOI: 10.1146/annurev.micro.62.081307.162903. View

CASHEL M, Gallant J . Two compounds implicated in the function of the RC gene of Escherichia coli. Nature. 1969; 221(5183):838-41. DOI: 10.1038/221838a0. View

10.

Witte G, Hartung S, Buttner K, Hopfner K . Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell. 2008; 30(2):167-78. DOI: 10.1016/j.molcel.2008.02.020. View

11.

Welz R, Breaker R . Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. RNA. 2007; 13(4):573-82. PMC: 1831863. DOI: 10.1261/rna.407707. View

12.

Kim P, Nelson J, Breaker R . An ancient riboswitch class in bacteria regulates purine biosynthesis and one-carbon metabolism. Mol Cell. 2015; 57(2):317-28. PMC: 4538711. DOI: 10.1016/j.molcel.2015.01.001. View

13.

Vitreschak A, Rodionov D, Mironov A, Gelfand M . Riboswitches: the oldest mechanism for the regulation of gene expression?. Trends Genet. 2003; 20(1):44-50. DOI: 10.1016/j.tig.2003.11.008. View

14.

Kots A, Martin E, Sharina I, Murad F . A short history of cGMP, guanylyl cyclases, and cGMP-dependent protein kinases. Handb Exp Pharmacol. 2008; (191):1-14. PMC: 3932363. DOI: 10.1007/978-3-540-68964-5_1. View

15.

Nissen P, Hansen J, Ban N, Moore P, Steitz T . The structural basis of ribosome activity in peptide bond synthesis. Science. 2000; 289(5481):920-30. DOI: 10.1126/science.289.5481.920. View

16.

Jimenez R, Polanco J, Luptak A . Chemistry and Biology of Self-Cleaving Ribozymes. Trends Biochem Sci. 2015; 40(11):648-661. PMC: 4630146. DOI: 10.1016/j.tibs.2015.09.001. View

17.

Sudarsan N, Hammond M, Block K, Welz R, Barrick J, Roth A . Tandem riboswitch architectures exhibit complex gene control functions. Science. 2006; 314(5797):300-4. DOI: 10.1126/science.1130716. View

18.

Wachter A, Tunc-Ozdemir M, Grove B, Green P, Shintani D, Breaker R . Riboswitch control of gene expression in plants by splicing and alternative 3' end processing of mRNAs. Plant Cell. 2007; 19(11):3437-50. PMC: 2174889. DOI: 10.1105/tpc.107.053645. View

19.

Jackson E . Discovery and Roles of 2',3'-cAMP in Biological Systems. Handb Exp Pharmacol. 2016; 238:229-252. DOI: 10.1007/164_2015_40. View

20.

Gao A, Serganov A . Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat Chem Biol. 2014; 10(9):787-92. PMC: 4294798. DOI: 10.1038/nchembio.1607. View