On a stake-out: Mycobacterial small RNA identification and regulation

Cosma, 2003, The secret lives of the pathogenic Mycobacteria, Annu. Rev. Microbiol., 57, 641, 10.1146/annurev.micro.57.030502.091033 Jagielski, 2014, Current methods in the molecular typing of Mycobacterium tuberculosis and other mycobacteria, BioMed Res. Int., 645802 Ingen, 2013, Diagnosis of nontuberculous mycobacterial infections, Semin. Respir. Crit. Care Med., 34, 103, 10.1055/s-0033-1333569 Ernst, 1998, Macrophage receptors for Mycobacterium tuberculosis, Infect. Immun., 66, 1277, 10.1128/IAI.66.4.1277-1281.1998 Dannenberg, 1993, Immuno-pathogenesis of pulmonary tuberculosis, Hosp. Pract., 28, 51, 10.1080/21548331.1993.11442738 Arnvig, 2012, Noncoding RNA and its potential role in Mycobacterium tuberculosis pathogenesis, RNA Biol., 9, 427, 10.4161/rna.20105 Wayne, 2001, Nonreplicating persistence of Mycobacterium tuberculosis, Annu. Rev. Microbiol., 55, 139, 10.1146/annurev.micro.55.1.139 Barry, 2009, The spectrum of latent tuberculosis: rethinking the biology and intervention strategies, Nat. Rev. Microbiol., 7, 845, 10.1038/nrmicro2236 Haning, 2014, Small RNAs in mycobacteria: an unfolding story, Front. Cellullar Infect. Microbiol., 4, 1 Flynn, 1998, Effects of aminoguanidine on latent murine tuberculosis, J. Immunol., 160, 1796, 10.4049/jimmunol.160.4.1796 Flynn, 2001, Tuberculosis: latency and reactivation, Infect. Immun., 69, 4195, 10.1128/IAI.69.7.4195-4201.2001 Cole, 1998, Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence, Nature, 393, 537, 10.1038/31159 Garnier, 2003, The complete genome sequence of Mycobacterium bovis, Proc. Natl. Acad. Sci. U.S.A., 100, 7877, 10.1073/pnas.1130426100 Scollard, 2000, Endothelial cells and the pathogenesis of lepromatous neuritis: insights from the armadillo model, Microb. Infect., 2, 1835, 10.1016/S1286-4579(00)01335-6 Gottesman, 2011, Bacterial small RNA regulators: versatile roles and rapidly evolving variations, Cold Spring Harb. Perspect. Biol., 3, a003798, 10.1101/cshperspect.a003798 Wei, 2018, Mycobacterium tuberculosis type III-A CRISPR/Cas system crRNA and its maturation have atypical features, FASEB J. Zhang, 2018, Regulation of the CRISPR-associated genes by Rv2837c (CnpB) via an Orn-like activity in TB complex mycobacteria, J. Bacteriol., 10.1128/JB.00743-17 Schwenk, 2018, Cell-wall synthesis and ribosome maturation are co-regulated by an RNA switch in Mycobacterium tuberculosis, Nucleic Acids Res., 46, 5837, 10.1093/nar/gky226 Sherwood, 2018, New tRNA contacts facilitate ligand binding in a Mycobacterium smegmatis T box riboswitch, Proc. Natl. Acad. Sci. U.S.A., 115, 3894, 10.1073/pnas.1721254115 Gottesman, 2004, The small RNA regulators of Escherichia coli: roles and mechanisms, Annu. Rev. Microbiol., 58, 273, 10.1146/annurev.micro.58.030603.123841 Gottesman, 2005, Micros for microbes: noncoding regulatory RNAs in bacteria, Trends Genet., 21, 399, 10.1016/j.tig.2005.05.008 Gottesman, 2011, Bacterial small RNA regulators: versatile roles and rapidly evolving variations, Cold Spring Harb. Perspect. Biol., 3, 1, 10.1101/cshperspect.a003798 Papenfort, 2009, Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level, Res. Microbiol., 160, 278, 10.1016/j.resmic.2009.03.004 Wagner, 2002, Antisense RNAs in bacteria and their genetic elements, Adv. Genet., 46, 361, 10.1016/S0065-2660(02)46013-0 Wagner, 2006, Small regulatory RNAs in bacteria, 1 Wagner, 2015, Small RNAs in bacteria and archaea: who they are, what they do, and how they do it, Adv. Genet., 90, 1 Water, 2009, Regulatory RNAs in bacteria, Cell, 136, 615, 10.1016/j.cell.2009.01.043 Storz, 2011, Regulation by small RNAs in bacteria: expanding frontiers, Mol. Cell, 43, 880, 10.1016/j.molcel.2011.08.022 Frohlich, 2009, Activation of gene expression by small RNA, Curr. Opin. Microbiol., 12, 674, 10.1016/j.mib.2009.09.009 Bobrovskyy, 2013, Regulation of bacterial metabolism by small RNAs using diverse mechanisms, Annu. Rev. Genet., 47, 227, 10.1146/annurev-genet-111212-133445 Dutta, 2018, Small RNA-mediated regulation in bacteria: a growing palette of diverse mechanisms, Gene, 656, 60, 10.1016/j.gene.2018.02.068 Chao, 2010, The role of Hfq in bacterial pathogens, Curr. Opin. Microbiol., 13, 24, 10.1016/j.mib.2010.01.001 Wasserman, 2007, 6S RNA: a small RNA regulator of transcription, Curr. Opin. Microbiol., 10, 156 Babitzke, 2007, CsrB sRNA family: sequestration of RNA-binding regulatory proteins, Curr. Opin. Microbiol., 10, 156, 10.1016/j.mib.2007.03.007 Lucchetti-Miganeh, 2008, The post–transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts, Microbiology, 154, 16, 10.1099/mic.0.2007/012286-0 Papenfort, 2010, Regulatory RNA in bacterial pathogens, Cell Host Microbe, 8, 116, 10.1016/j.chom.2010.06.008 Bohn, 2007, No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus, BMC Microbiol., 7, 10, 10.1186/1471-2180-7-10 Liu, 2010, Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus, PLoS One, 5, 5 Smirnov, 2016, Grad-seq guides the discovery of ProQ as a major small RNA-binding protein, Proc. Natl. Acad. Sci. U. S. A., 113, 11591, 10.1073/pnas.1609981113 Pandey, 2011, A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq, Nucleic Acids Res., 39, 4691, 10.1093/nar/gkr060 Vogel, 2011, Hfq and its constellation of RNA, Nat. Rev. Microbiol., 9, 578, 10.1038/nrmicro2615 Gripenland, 2010, RNAs: regulators of bacterial virulence, Nat. Rev. Microbiol., 8, 857, 10.1038/nrmicro2457 Toledo-Arana, 2009, The Listeria transcriptional landscape from saprophytism to virulence, Nature, 459, 950, 10.1038/nature08080 Arnvig, 2010, Regulation of pathogen metabolism by small RNA, Drug Discov, Today Dis. Mech, 7, 19, 10.1016/j.ddmec.2010.09.001 Feng, 2015, A Qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics, Cell, 160, 228, 10.1016/j.cell.2014.11.051 Svenningsen, 2009, Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing, EMBO J., 28, 429, 10.1038/emboj.2008.300 Chabelskaya, 2010, A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune evasion molecule, PLoS Pathog., 6, 1000927, 10.1371/journal.ppat.1000927 Mann, 2012, Control of virulence by small RNAs in Streptococcus pneumonia, PLoS Pathog., 8, e1002788, 10.1371/journal.ppat.1002788 Roberts, 2007, RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon, Mol. Microbiol., 66, 1506 Wen, 2012, Helicobacter pylori 5ꞌ-ureB-sRNA, a cis-encoded antisense small RNA, negatively regulates ureAB expression by transcription termination, J. Bacteriol., 195, 444, 10.1128/JB.01022-12 Gaida, 2013, Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress, Nucleic Acids Res., 41, 8726, 10.1093/nar/gkt651 Soper, 2010, Positive regulation by small RNAs and the role of Hfq, Proc. Natl. Acad. Sci. U. S. A., 107, 9602, 10.1073/pnas.1004435107 Mellin, 2012, The non-coding RNA world of the bacterial pathogen Listeria monocytogenes, RNA Biol., 9, 372, 10.4161/rna.19235 Caldelari, 2013, RNA-mediated regulation in pathogenic bacteria, Cold Spring Harb. Perspect. Med., 3, a010298, 10.1101/cshperspect.a010298 Tomasini, 2014, The importance of regulatory RNAs in Staphylococcus aureus, Infect. Genet. Evol., 21, 616, 10.1016/j.meegid.2013.11.016 Gong, 2011, A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors, PLoS Pathog., 7, 1002120, 10.1371/journal.ppat.1002120 Mizuno, 1984, A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA), Proc. Natl. Acad. Sci. U. S. A., 81, 1966, 10.1073/pnas.81.7.1966 Wassarman, 2001, Identification of novel small RNAs using comparative genomics and microarrays, Genes Dev., 15, 1637, 10.1101/gad.901001 Argaman, 2001, Novel small RNA-encoding genes in the intergenic regions of Escherichia coli, Curr. Biol., 11, 941, 10.1016/S0960-9822(01)00270-6 Rivas, 2001, Computational identification of noncoding RNAs in E. coli by comparative genomics, Curr. Biol., 11, 1369, 10.1016/S0960-9822(01)00401-8 Hen, 2002, A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome, Biosystems, 65, 157, 10.1016/S0303-2647(02)00013-8 Sittka, 2008, Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet., 4, e1000163, 10.1371/journal.pgen.1000163 Sharma, 2009, Experimental approaches for the discovery and characterization of regulatory small RNAs, Curr. Opin. Microbiol., 12, 536, 10.1016/j.mib.2009.07.006 Melamed, 2016, Global mapping of small RNA-target interactions in bacteria, Mol. Cell, 63, 884, 10.1016/j.molcel.2016.07.026 Arnvig, 2009, Identification of small RNAs in Mycobacterum tuberculosis, Mol. Microbiol., 73, 397, 10.1111/j.1365-2958.2009.06777.x Panek, 2008, Biocomputational prediction of small non-coding RNAs in Streptomyces, BMC Genomics, 9, 217, 10.1186/1471-2164-9-217 Bohn, 2007, No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus, BMC Microbiol., 7, 10, 10.1186/1471-2180-7-10 Geisinger, 2006, Inhibition of rot translation by RNAIII, a key feature of agr function, Mol. Microbiol., 61, 1038, 10.1111/j.1365-2958.2006.05292.x Dichiara, 2010, Multiple sRNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis, Nucleic Acids Res., 38, 4067, 10.1093/nar/gkq101 Arnvig, 2011, Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis, Plos Pathogn, 7, e1002342, 10.1371/journal.ppat.1002342 Tsai, 2013, Identification of novel sRNAs in Mycobacterial species, PLoS One, 8, e79411, 10.1371/journal.pone.0079411 Wang, 2016, An automated approach for global identification of sRNA-encoding regions in RNA-seq data from Mycobacterium tuberculosis, Acta Biochim. Biophys. Sin., 48, 544, 10.1093/abbs/gmw037 Akama, 2010, Whole genome expression analysis of Mycobacterium leprae and its clinical application, Jpn. J. Infect. Dis., 63, 387, 10.7883/yoken.63.387 Li, 2013, Identification of small RNAs in Mycobacterium smegmatis using heterologous Hfq, RNA, 19, 74, 10.1261/rna.034116.112 Schwenk, 2018, Regulatory RNA in Mycobacterium tuberculosis, back to basics, Pathogens Disease, 76, 1, 10.1093/femspd/fty035 Updegrove, 2015, How do base-pairing small RNAs evolve?, FEMS Microbiol. Rev., 39, 379, 10.1093/femsre/fuv014 Otaka, 2011, PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action, Proc. Natl. Acad. Sci. U. S. A., 108, 13059, 10.1073/pnas.1107050108 Sauer, 2011, Structural basis of RNA 3′-end recognition by Hfq, Proc. Natl. Acad. Sci. U. S. A., 108, 13065, 10.1073/pnas.1103420108 Desnoyer, 2012, New insights into small RNA dependent translation regulation in prokaryotes, Trends Genet., 29, 92, 10.1016/j.tig.2012.10.004 Boudvillain, 2012, A role for rho-dependent polarity in gene regulation by a noncoding small RNA, Genes Dev., 26, 1864, 10.1101/gad.195412.112 Chao, 2017, In vivo cleavage map illuminates the central role of RNase E in coding and non-coding RNA pathway, Mol. Cell, 65, 39, 10.1016/j.molcel.2016.11.002 Massé, 2003, Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli, Genes Dev., 17, 2374, 10.1101/gad.1127103 Sonnleitner, 2014, Regulation of hfq by the RNA CrcZ in pseudomonasaeruginosa carbon catabolite repression, PLoS Genet., 10, e1004440, 10.1371/journal.pgen.1004440 Bobrovsky, 2014, The small RNA SgrS: roles in metabolism and pathogenesis of enteric bacteria, Front. Cellular Infec. Microbiol., 4, 1, 10.3389/fcimb.2014.00061 Papenfort, 2015, Target activation of regulatory RNAs in bacteria, FEMS Microbiol. Rev., 39, 362, 10.1093/femsre/fuv016 Opdyke, 2004, GadY, a small RNA regulator of acid response genes in Escherichia coli, J. Bacteriol., 186, 6698, 10.1128/JB.186.20.6698-6705.2004 Opdyke, 2011, RNase III participates in GadY dependent cleavage of the gadX-gadW mRNA, J. Mol. Biol., 406, 29, 10.1016/j.jmb.2010.12.009 Babitzke, 2007, CsrB sRNA family: sequestration of RNA binding regulatory proteins, Curr. Opin. Microbiol., 10, 156, 10.1016/j.mib.2007.03.007 Baker, 2002, CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli, Mol. Microbiol., 44, 1599, 10.1046/j.1365-2958.2002.02982.x Suzuki, 2006, Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E, Genes Dev., 20, 2605, 10.1101/gad.1461606 Schnappinger, 2003, Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment, J. Exp. Med., 198, 693, 10.1084/jem.20030846 Stewart, 2002, The heat shock response of Mycobacterium tuberculosis: linking gene expression, immunology and pathogenesis, Comp. Funct. Genom., 3, 348, 10.1002/cfg.183 Zhou, 2010, The roles of Pathogen small RNAs, J. Cell. Physiol., 226, 968, 10.1002/jcp.22483 Sassetti, 2003, Genes required for mycobacterial growth defined by high density mutagenesis, Mol. Microbiol., 48, 77, 10.1046/j.1365-2958.2003.03425.x Matsunaga, 2004, Mycobacterium tuberculosis pks12 produces a novel polyketide presented by CD1c to T cells, J. Exp. Med., 200, 1559, 10.1084/jem.20041429 Schnappinger, 2003, Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment, J. Exp. Med., 198, 693, 10.1084/jem.20030846 Houghton, 2013, A small RNA encoded in the Rv2660c locus of Mycobacterium tuberculosis is induced during starvation and infection, PLoS One, 8, e80047, 10.1371/journal.pone.0080047 Sturgill-Koszycki, 1994, Lack of acidification in Mycobacterial phagosomes produced by exclusion of the vesicular proton-ATPase, Science, 263, 678, 10.1126/science.8303277 Monohan, 2001, Differential expression of mycobacterial proteins following phagocytosis by macrophages, Microbiology, 147, 459, 10.1099/00221287-147-2-459 Hobson, 2002, Use of an arrayed promoter -probe library for the identification of macrophage-regulated genes in Mycobacterium tuberculosis, Microbiology, 148, 1571, 10.1099/00221287-148-5-1571 Gazdik, 2009, Rv1675c (cmr) regulates intramacrophage and cAMP-induced gene expression in Mycobacterium tuberculosis-complex mycobacteria, Mol. Microbiol., 71, 434, 10.1111/j.1365-2958.2008.06541.x Arnvig, 2005, The mechanism of upstream activation in the rrnB operon of Mycobacteriumsmegmatis is different from the Escherichia coli paradigm, Microbiology, 151, 467, 10.1099/mic.0.27597-0 Solans, 2014, The PhoP-dependent ncRNAMcr7 modulates the TAT secretion system in Mycobacterium tuberculosis, PLoS Pathog., 10, e1004183, 10.1371/journal.ppat.1004183 Walters, 2006, The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis, Mol. Microbiol., 60, 312, 10.1111/j.1365-2958.2006.05102.x Perez, 2001, An essential role for phoP in Mycobacterium tuberculosis virulence, Mol. Microbiol., 41, 179, 10.1046/j.1365-2958.2001.02500.x Lee, 2008, Mutation in the transcriptional regulator PhoP contributes to avirulence of Mycobacterium tuberculosis H37Ra strain, Cell Host Microbe, 3, 97, 10.1016/j.chom.2008.01.002 Brosch, 2002, A new evolutionary scenario for the Mycobacterium tuberculosis complex, Proc. Natl. Acad. Sci. U. S. A., 99, 3684, 10.1073/pnas.052548299 Joanis, 2006, Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases beta-lactam susceptibility and virulence, J. Bacteriol., 188, 6669, 10.1128/JB.00631-06 Palmer, 2012, The twin-arginine translocation (Tat) protein export pathway, Nat. Rev. Microbiol., 10, 483, 10.1038/nrmicro2814 Moores, 2017, Expression, maturation and turnover of DrrS, an unusually stable, DosR regulated small RNA in Mycobacterium tuberculosis, PLoS One, 12, e0174079, 10.1371/journal.pone.0174079 Chauhan, 2011, Comprehensive insights into Mycobacterium tuberculosis DevR (DosR) regulon activation switch, Nucleic Acids Res., 39, 7400, 10.1093/nar/gkr375 Gerrick, 2018, Small RNA profiling in Mycobacterium tuberculosis identifies MsrI as necessary for an anticipatory iron sparing response, Proc. Natl. Acad. Sci. U.S.A., 115, 6464, 10.1073/pnas.1718003115 Rock, 2017, Programmable transcriptional repression in mycobacteria using an orthogonal CRISPR interference platform, Nat. Microbiol., 2, 16274, 10.1038/nmicrobiol.2016.274 Panek, 2011, The suboptimal structures find the optimal RNAs: homology search for bacterial non-coding RNAs using suboptimal RNA structures, Nucleic Acids Res., 39, 3418, 10.1093/nar/gkq1186 Hnilicova, 2014, Ms1, a novel sRNA interacting with RNA polymerase core in mycobacteria, Nucleic Acids Res., 42, 11763, 10.1093/nar/gku793 Sikova, 2018, Ms1 RNA increases the amount of RNA polymerase in Mycobacterium smegmatis, Mol. Microbiol. Wassarman, 2000, 6S RNA regulates E. coli RNA polymerase activity, Cell, 101, 613, 10.1016/S0092-8674(00)80873-9 Cavanagh, 2014, 6S RNA, a global regulator of transcription in Escherichia coli, Bacillus subtilis and beyond, Annu. Rev. Microbiol., 68, 45, 10.1146/annurev-micro-092611-150135 Steuten, 2014, 6S RNA: recent answers - future questions, Mol. Microbiol., 91, 641, 10.1111/mmi.12484 Cao, 2017, Systems-level understanding of ethanol-induced stresses and adaptation in E. coli, Sci. Rep., 7, 44150, 10.1038/srep44150 Schaible, 2004, Iron and microbial infection, Nat. Rev. Microbiol., 2, 946, 10.1038/nrmicro1046 Stallings, 2010, Is Mycobacterium tuberculosis stressed out? A criticalassessment of the genetic evidence, Microb. Infect., 12, 1091, 10.1016/j.micinf.2010.07.014 Purdy, 2009, Decreased outer membrane permeability protects mycobacteria from killing by ubiquitin-derived peptides, Mol. Microbiol., 73, 844, 10.1111/j.1365-2958.2009.06801.x Liu, 2007, Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin, J. Immunol., 179, 2060, 10.4049/jimmunol.179.4.2060 Beisel, 2010, Base pairing small RNAs and their roles in global regulatory networks, FEMS Microbiol. Rev., 34, 866, 10.1111/j.1574-6976.2010.00241.x Sassetti, 2003, Genetic requirements for mycobacterial survival during infection, Proc. Natl. Acad. Sci. U.S.A., 100, 12989, 10.1073/pnas.2134250100 Sassetti, 2003, Genes required for mycobacterial growth defined by high density mutagenesis, Mol. Microbiol., 48, 77, 10.1046/j.1365-2958.2003.03425.x