REVIEW ARTICLE The critical role of RNA processing and degradation in the control of gene expression Cec´ ılia M. Arraiano, Jos ´ e M. Andrade, Susana Domingues, Ine ˆ s B. Guinote, Michal Malecki, Rute G. Matos, Ricardo N. Moreira, Va ˆnia Pobre, Filipa P. Reis, Margarida Saramago, Ine ˆ s J. Silva & Sandra C. Viegas Instituto de Tecnologia Qu´ ımica e Biol ´ ogica, Universidade Nova de Lisboa, Apartado, Oeiras, Portugal Correspondence: Cec´ ılia M. Arraiano, Instituto de Tecnologia Qu´ ımica e Biol ´ ogica, Universidade Nova de Lisboa, Apartado 127, 2781-901 Oeiras, Portugal. Tel.: 1351 214 469 547; fax: 1351 214 469 549; e-mail: cecilia@itqb.unl.pt Received 30 April 2010; revised 18 June 2010; accepted 20 June 2010. Final version published online 26 July 2010. DOI:10.1111/j.1574-6976.2010.00242.x Editor: William Margolin Keywords RNases; RNA; post-transcriptional control of gene expression. Abstract The continuous degradation and synthesis of prokaryotic mRNAs not only give rise to the metabolic changes that are required as cells grow and divide but also rapid adaptation to new environmental conditions. In bacteria, RNAs can be degraded by mechanisms that act independently, but in parallel, and that target different sites with different efficiencies. The accessibility of sites for degradation depends on several factors, including RNA higher-order structure, protection by translating ribosomes and polyadenylation status. Furthermore, RNA degradation mechanisms have shown to be determinant for the post-transcriptional control of gene expression. RNases mediate the processing, decay and quality control of RNA. RNases can be divided into endonucleases that cleave the RNA internally or exonucleases that cleave the RNA from one of the extremities. Just in Escherichia coli there are 4 20 different RNases. RNase E is a single-strand-specific endonuclease critical for mRNA decay in E. coli. The enzyme interacts with the exonuclease polynucleotide phosphorylase (PNPase), enolase and RNA helicase B (RhlB) to form the degradosome. However, in Bacillus subtilis, this enzyme is absent, but it has other main endonucleases such as RNase J1 and RNase III. RNase III cleaves double-stranded RNA and family members are involved in RNA interference in eukaryotes. RNase II family members are ubiquitous exonucleases, and in eukaryotes, they can act as the catalytic subunit of the exosome. RNases act in different pathways to execute the maturation of rRNAs and tRNAs, and intervene in the decay of many different mRNAs and small noncoding RNAs. In general, RNases act as a global regulatory network extremely important for the regulation of RNA levels. Introduction General outline Many cellular mechanisms cannot be fully understood with- out a profound knowledge of the RNA metabolism. Protein production depends not only on the levels of mRNAs but also on other RNA species. The translation of mRNAs is mediated by tRNAs and rRNAs and functional RNAs also intervene in the regulation of gene expression. Synergies between the structure and function of RNAs contribute towards orchestrating their fundamental role in cell viability. Bacterial mRNAs are rapidly degraded and this allows the microorganisms to rapidly adapt to changing environments. Even though transcription is quite important to determine steady-state levels, increasingly it is being established that the role of post-transcriptional control is critical in the regulation of gene expression. Analyzing RNA degradation in prokar- yotes has been particularly difficult not only due to the coupling of transcription, translation and mRNA degradation but also because most mRNAs undergo a rapid exponential decay with an average of 1.3 min at 37 1C. The rRNAs and tRNAs are usually more stable, but in order to be functionally active, they have to be processed to the mature form. It has been shown that the levels of small noncoding RNAs (sRNAs) are also highly dependent on post-transcriptional events. The knowledge collected makes it clear how far our understanding of RNA degradation has come in the last few years and how much remains to be discovered about this important genetic regulatory process. Applications of this knowledge in medi- cine and biotechnology are underway. FEMS Microbiol Rev 34 (2010) 883–923 c  2010 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved MICROBIOLOGY REVIEWS Downloaded from https://academic.oup.com/femsre/article/34/5/883/801732 by guest on 06 June 2022