Detection of 5'- and 3'-UTR-derived Small RNAs and Cis-encoded Antisense RNAs in Escherichia Coli

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2005 Feb 19

PMID 15718303

Citations 127

Authors

Mitsuoki Kawano

April A Reynolds

Juan Miranda-Rios

Gisela Storz

Affiliations

Soon will be listed here.

Abstract

Evidence is accumulating that small, noncoding RNAs are important regulatory molecules. Computational and experimental searches have led to the identification of approximately 60 small RNA genes in Escherichia coli. However, most of these studies focused on the intergenic regions and assumed that small RNAs were >50 nt. Thus, the previous screens missed small RNAs encoded on the antisense strand of protein-coding genes and small RNAs of <50 nt. To identify additional small RNAs, we carried out a cloning-based screen focused on RNAs of 30-65 nt. In this screen, we identified RNA species corresponding to fragments of rRNAs, tRNAs and known small RNAs. Several of the small RNAs also corresponded to 5'- and 3'-untranslated regions (UTRs) and internal fragments of mRNAs. Four of the 3'-UTR-derived RNAs were highly abundant and two showed expression patterns that differed from the corresponding mRNAs, suggesting independent functions for the 3'-UTR-derived small RNAs. We also detected three previously unidentified RNAs encoded in intergenic regions and RNAs from the long direct repeat and hok/sok elements. In addition, we identified a few small RNAs that are expressed opposite protein-coding genes and could base pair with 5' or 3' ends of the mRNAs with perfect complementarity.

Citing Articles

Template switching enables chemical probing of native RNA structures.

Hall I, OSteen M, Gold S, Keane S, Weidmann C RNA. 2024; 31(1):113-125.

PMID: 39438135 PMC: 11648929. DOI: 10.1261/rna.079926.123.

Role of Small Non-Coding RNA in Gram-Negative Bacteria: New Insights and Comprehensive Review of Mechanisms, Functions, and Potential Applications.

Khaledi M, Khatami M, Hemmati J, Bakhti S, Hoseini S, Ghahramanpour H Mol Biotechnol. 2024; .

PMID: 39153013 DOI: 10.1007/s12033-024-01248-w.

Devising Isolation Forest-Based Method to Investigate the sRNAome of Using sRNA-seq Data.

Maity U, Aggarwal R, Balasubramanian R, Venkatraman D, Hegde S Bioinform Biol Insights. 2024; 18:11779322241263674.

PMID: 39091283 PMC: 11292719. DOI: 10.1177/11779322241263674.

EcCas6e-based antisense crRNA for gene repression and RNA editing in microorganisms.

Li M, Cai Z, Song S, Yue X, Lu W, Rao S Nucleic Acids Res. 2024; 52(14):8628-8642.

PMID: 38994565 PMC: 11317134. DOI: 10.1093/nar/gkae612.

A simple BLASTn-based approach generates novel insights into the regulation and biological function of type I toxin-antitoxins.

Shore S, Ptacek M, Steen A, Fozo E mSystems. 2024; 9(7):e0120423.

PMID: 38856235 PMC: 11264685. DOI: 10.1128/msystems.01204-23.

References

Pedersen K, Gerdes K . Multiple hok genes on the chromosome of Escherichia coli. Mol Microbiol. 1999; 32(5):1090-102. DOI: 10.1046/j.1365-2958.1999.01431.x. View

Gerdes K, Gultyaev A, Franch T, Pedersen K, Mikkelsen N . Antisense RNA-regulated programmed cell death. Annu Rev Genet. 1997; 31:1-31. DOI: 10.1146/annurev.genet.31.1.1. View

Storz G, Altuvia S, Wassarman K . An abundance of RNA regulators. Annu Rev Biochem. 2005; 74:199-217. DOI: 10.1146/annurev.biochem.74.082803.133136. View

GRUNBERG-MANAGO M . Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet. 2000; 33:193-227. DOI: 10.1146/annurev.genet.33.1.193. View

Fernandez de Henestrosa A, Ogi T, Aoyagi S, Chafin D, HAYES J, Ohmori H . Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol. 2000; 35(6):1560-72. DOI: 10.1046/j.1365-2958.2000.01826.x. View

Urbanowski M, Stauffer L, Stauffer G . The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol. 2000; 37(4):856-68. DOI: 10.1046/j.1365-2958.2000.02051.x. View

Selinger D, Cheung K, Mei R, Johansson E, Richmond C, Blattner F . RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nat Biotechnol. 2000; 18(12):1262-8. DOI: 10.1038/82367. View

Elbashir S, Lendeckel W, Tuschl T . RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 2001; 15(2):188-200. PMC: 312613. DOI: 10.1101/gad.862301. View

Wassarman K, Repoila F, Rosenow C, Storz G, Gottesman S . Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev. 2001; 15(13):1637-51. PMC: 312727. DOI: 10.1101/gad.901001. View

10.

Argaman L, HERSHBERG R, Vogel J, Bejerano G, WAGNER E, Margalit H . Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol. 2001; 11(12):941-50. DOI: 10.1016/s0960-9822(01)00270-6. View

11.

Rivas E, Klein R, Jones T, Eddy S . Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol. 2001; 11(17):1369-73. DOI: 10.1016/s0960-9822(01)00401-8. View

12.

Rauhut R, Lendeckel W, Tuschl T . Identification of novel genes coding for small expressed RNAs. Science. 2001; 294(5543):853-8. DOI: 10.1126/science.1064921. View

13.

Wagner E, Altuvia S, Romby P . Antisense RNAs in bacteria and their genetic elements. Adv Genet. 2002; 46:361-98. DOI: 10.1016/s0065-2660(02)46013-0. View

14.

Chen S, Lesnik E, Hall T, Sampath R, Griffey R, Ecker D . A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems. 2002; 65(2-3):157-77. DOI: 10.1016/s0303-2647(02)00013-8. View

15.

Kawano M, Oshima T, Kasai H, Mori H . Molecular characterization of long direct repeat (LDR) sequences expressing a stable mRNA encoding for a 35-amino-acid cell-killing peptide and a cis-encoded small antisense RNA in Escherichia coli. Mol Microbiol. 2002; 45(2):333-49. DOI: 10.1046/j.1365-2958.2002.03042.x. View

16.

Yamamoto K, Ogasawara H, Fujita N, Utsumi R, Ishihama A . Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol Microbiol. 2002; 45(2):423-38. DOI: 10.1046/j.1365-2958.2002.03017.x. View

17.

Tjaden B, Saxena R, Stolyar S, Haynor D, Kolker E, Rosenow C . Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res. 2002; 30(17):3732-8. PMC: 137427. DOI: 10.1093/nar/gkf505. View

18.

Hershberg R, Altuvia S, Margalit H . A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res. 2003; 31(7):1813-20. PMC: 152812. DOI: 10.1093/nar/gkg297. View

19.

Gottesman S, Storz G, Rosenow C, Majdalani N, Repoila F, Wassarman K . Small RNA regulators of translation: mechanisms of action and approaches for identifying new small RNAs. Cold Spring Harb Symp Quant Biol. 2003; 66:353-62. DOI: 10.1101/sqb.2001.66.353. View

20.

Huerta A, Collado-Vides J . Sigma70 promoters in Escherichia coli: specific transcription in dense regions of overlapping promoter-like signals. J Mol Biol. 2003; 333(2):261-78. DOI: 10.1016/j.jmb.2003.07.017. View