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Prof Jörg Vogel

RNA Biology of Bacterial Infections

Work in the Vogel lab focuses on the role of noncoding RNA during infections. This includes studying RNA and RNA-binding proteins of bacterial pathogens or members of the microbiome both globally and in particular on a single-cell level.

Our research and approach

RNA Biology of Bacterial Infections

The Vogel lab strives to chart the diversity of noncoding RNA functions and RNA-binding proteins in major bacterial pathogens and in the hundreds of different bacteria that make up the human microbiome. We develop new RNA deep sequencing-based techniques to capture the RNA world of any microbe, ideally at the single cell level. We want to understand how and why bacteria use noncoding RNA as a regulator during infection and exploit this knowledge to target pathogens and edit the microbiota with precision. Projects focus on several bacteria from our major workhorse Salmonella Typhimurium to anaerobic microbes that are associated with colorectal cancer such as Fusobacterium nucleatum.

Team members

Publications

2019

The CRISPR/Cas system in Neisseria meningitidis affects bacterial adhesion to human nasopharyngeal epithelial cells

Heidrich N, Hagmann A, Bauriedl S, Vogel J, Schoen C (2019)

RNA biology, 16 (4): 390-396DOI: 10.1080/15476286.2018.1486660

The conserved 3' UTR-derived small RNA NarS mediates mRNA crossregulation during nitrate respiration

Wang C, Chao Y, Matera G, Gao Q, Vogel J (2019)

Nucleic Acids ResDOI: 10.1093/nar/gkz1168

The Major RNA-Binding Protein ProQ Impacts Virulence Gene Expression in Salmonella enterica Serovar Typhimurium

Westermann A, Venturini E, Sellin M, Förstner K, Hardt W, Vogel J (2019)

MBio, 10 (1): 02504-18DOI: 10.1128/mBio.02504-18

Functional expansion of a TCA cycle operon mRNA by a 3' end-derived small RNA

Miyakoshi M, Matera G, Maki K, Sone Y, Vogel J (2019)

Nucleic Acids Res, 47 (4): 2075-2088DOI: 10.1093/nar/gky1243

An RNA Surprise in Bacterial Effector Mechanisms

Gerovac M, Vogel J (2019)

Cell Host Microbe, 26 (6): 709-711DOI: 10.1016/j.chom.2019.11.005

2018

CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level

El Mouali Y, Gaviria-Cantin T, Sánchez-Romero M, Gibert M, Westermann A, Vogel J, Balsalobre C (2018)

Plos Genet, 14 (6): 10074DOI: 10.1371/journal.pgen.1007401

ANNOgesic: a Swiss army knife for the RNA-seq based annotation of bacterial/archaeal genomes

Yu S, Vogel J, Förstner K (2018)

Gigascience, 7 (9): 096DOI: 10.1093/gigascience/giy096

Salmonella persisters undermine host immune defenses during antibiotic treatment

Stapels D, Hill P, Westermann A, Fisher R, Thurston T, Saliba A, Blommestein I, Vogel J, Helaine S (2018)

Science, 362 (6419): 1156-1160DOI: 10.1126/science.aat7148

Genome organization and DNA accessibility control antigenic variation in trypanosomes

Müller L, Cosentino R, Förstner K, Guizetti J, Wedel C, Kaplan N, Janzen C, Arampatzi P, Vogel J, Steinbiss S, …, Sebra R, Siegel T (2018)

Nature, 563 (7729): 121-125DOI: 10.1038/s41586-018-0619-8

Bacterial RNA Biology on a Genome Scale

Hör J, Gorski S, Vogel J (2018)

Mol Cell, 70 (5): 785-799DOI: 10.1016/j.molcel.2017.12.023

RNA-binding proteins in bacteria

Holmqvist E, Vogel J (2018)

Nat Rev Microbiol, 16 (10): 601-615DOI: 10.1038/s41579-018-0049-5

Stress-induced host membrane remodeling protects from infection by non-motile bacterial pathogens

Tawk C, Nigro G, Rodrigues Lopes I, Aguilar C, Lisowski C, Mano M, Sansonetti P, Vogel J, Eulalio A (2018)

EMBO J, 37 (23): 98529DOI: 10.15252/embj.201798529

2017

APRICOT: an integrated computational pipeline for the sequence-based identification and characterization of RNA-binding proteins

Sharan M, Förstner K, Eulalio A, Vogel J (2017)

Nucleic Acids Res, 45 (11): 96DOI: 10.1093/nar/gkx137

A systematic analysis of the RNA-targeting potential of secreted bacterial effector proteins

Tawk C, Sharan M, Eulalio A, Vogel J (2017)

Sci Rep, 7 (1): 9328DOI: 10.1038/s41598-017-09527-0

Global snapshots of bacterial RNA networks

Hör J, Vogel J (2017)

EMBO J, 36 (3): 245-247DOI: 10.15252/embj.201696072

The primary transcriptome of Neisseria meningitidis and its interaction with the RNA chaperone Hfq

Heidrich N, Bauriedl S, Barquist L, Li L, Schoen C, Vogel J (2017)

Nucleic Acids Res, 45 (10): 6147-6167DOI: 10.1093/nar/gkx168

Molecular mechanism of mRNA repression in trans by a ProQ‐dependent small RNA

Smirnov A, Wang C, Drewry L, Vogel J (2017)

EMBO J, 36 (8): 1029-45DOI: 10.15252/embj.201696127

RNA-based recognition and targeting: sowing the seeds of specificity

Gorski S, Vogel J, Doudna J (2017)

Nat Rev Mol Cell Biol, 18 (4): 215-228DOI: 10.1038/nrm.2016.174

Discovery of new RNA classes and global RNA-binding proteins

Smirnov A, Schneider C, Hör J, Vogel J (2017)

Curr Opin Microbiol, 39: 152-160DOI: 10.1016/j.mib.2017.11.016

Structure of the Escherichia coli ProQ RNA-binding protein

Gonzalez G, Hardwick S, Maslen S, Skehel J, Holmqvist E, Vogel J, Bateman A, Luisi B, Broadhurst R (2017)

RNA (New York, N.Y.C), 23 (5): 696-711DOI: 10.1261/rna.060343.116

In Vivo Cleavage Map Illuminates the Central Role of RNase E in Coding and Non-coding RNA Pathways

Chao Y, Li L, Girodat D, Förstner K, Said N, Corcoran C, Smiga M, Papenfort K, Reinhardt R, Wieden H, Luisi B, Vogel J (2017)

Mol Cell, 65 (1): 39-51DOI: 10.1016/j.molcel.2016.11.002

2016

Natural mutations in a Staphylococcus aureus virulence regulator attenuate cytotoxicity but permit bacteremia and abscess formation

Das S, Lindemann C, Young B, Muller J, Österreich B, Ternette N, Winkler A, Paprotka K, Reinhardt R, Förstner K, …, Wyllie D, Fraunholz M (2016)

Proc Natl Acad Sci U S A, 113 (22): 3101-10DOI: 10.1073/pnas.1520255113

An NK Cell Perforin Response Elicited via IL-18 Controls Mucosal Inflammation Kinetics during Salmonella Gut Infection

Müller A, Dolowschiak T, Sellin M, Felmy B, Verbree C, Gadient S, Westermann A, Vogel J, LeibundGut-Landmann S, Hardt W (2016)

Plos Pathog, 12 (6): 10057DOI: 10.1371/journal.ppat.1005723

A 3' UTR-Derived Small RNA Provides the Regulatory Noncoding Arm of the Inner Membrane Stress Response

Chao Y, Vogel J (2016)

Mol Cell, 61 (3): 352-363DOI: 10.1016/j.molcel.2015.12.023

Grad-seq guides the discovery of ProQ as a major small RNA-binding protein

Smirnov A, Förstner K, Holmqvist E, Otto A, Günster R, Becher D, Reinhardt R, Vogel J (2016)

Proc Natl Acad Sci U S A, 113 (41): 11591-11596DOI: 10.1073/pnas.1609981113

An expanded evaluation of protein function prediction methods shows an improvement in accuracy

Jiang Y, Oron T, Clark W, Bankapur A, D'Andrea D, Lepore R, Funk C, Kahanda I, Verspoor K, Ben-Hur A, …, Friedberg I, Radivojac P (2016)

Genome Biol, 17 (1): 184DOI: 10.1186/s13059-016-1037-6

Single-cell RNA-seq ties macrophage polarization to growth rate of intracellular Salmonella

Saliba A, Li L, Westermann A, Appenzeller S, Stapels D, Schulte L, Helaine S, Vogel J (2016)

Nat Microbiol, 2: 16206DOI: 10.1038/nmicrobiol.2016.206

The target spectrum of SdsR small RNA in Salmonella

Fröhlich K, Haneke K, Papenfort K, Vogel J (2016)

Nucleic Acids Res, 44 (21): 10406-22DOI: 10.1093/nar/gkw632

cis-Encoded Small RNAs, a Conserved Mechanism for Repression of Polysaccharide Utilization in Bacteroides

Cao Y, Förstner K, Vogel J, Smith C (2016)

J Bacteriol, 198 (18): 2410-8DOI: 10.1128/JB.00381-16

Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions

Westermann A, Forstner K, Amman F, Barquist L, Chao Y, Schulte L, Muller L, Reinhardt R, Stadler P, Vogel J (2016)

Nature, 529 (7587): 496-501DOI: 10.1038/nature16547

The primary transcriptome of the Escherichia coli O104:H4 pAA plasmid and novel insights into its virulence gene expression and regulation

Berger P, Knödler M, Förstner K, Berger M, Bertling C, Sharma C, Vogel J, Karch H, Dobrindt U, Mellmann A (2016)

Sci Rep, 6: 35307DOI: 10.1038/srep35307

Emerging roles of RNA modifications in bacteria

Marbaniang C, Vogel J (2016)

Curr Opin Microbiol, 30: 50-57DOI: 10.1016/j.mib.2016.01.001

Gifsy-1 Prophage IsrK with Dual Function as Small and Messenger RNA Modulates Vital Bacterial Machineries

Hershko-Shalev T, Odenheimer-Bergman A, Elgrably-Weiss M, Ben-Zvi T, Govindarajan S, Seri H, Papenfort K, Vogel J, Altuvia S (2016)

Plos Genet, 12 (4): 10059DOI: 10.1371/journal.pgen.1005975

2015

Dual 3'Seq using deepSuperSAGE uncovers transcriptomes of interacting Salmonella enterica Typhimurium and human host cells

Afonso-Grunz F, Hoffmeier K, Müller S, Westermann A, Rotter B, Vogel J, Winter P, Kahl G (2015)

BMC Genomics, 16: 323DOI: 10.1186/s12864-015-1489-1

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Papenfort K, Espinosa E, Casadesús J, Vogel J (2015)

Proc Natl Acad Sci U S A, 112 (34): 4772-81DOI: 10.1073/pnas.1507825112

dRNA-Seq Reveals Genomewide TSSs and Noncoding RNAs of Plant Beneficial Rhizobacterium Bacillus amyloliquefaciens FZB42

Fan B, Li L, Chao Y, Förstner K, Vogel J, Borriss R, Wu X (2015)

Plos One, 10 (11): 01420DOI: 10.1371/journal.pone.0142002

Regulatory small RNAs from the 3' regions of bacterial mRNAs

Miyakoshi M, Chao Y, Vogel J (2015)

Curr Opin Microbiol, 24: 132-9DOI: 10.1016/j.mib.2015.01.013

Investigating CRISPR RNA Biogenesis and Function Using RNA-seq

Heidrich N, Dugar G, Vogel J, Sharma C (2015)

In: CRISPR: Methods and protocols (eds Lundgren M, Charpentier E, Fineran PC), Methods Mol Biol (Methods in Molecular Biology), 1311: 1-21DOI: 10.1007/978-1-4939-2687-9_1

Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA

Miyakoshi M, Chao Y, Vogel J (2015)

EMBO J, 34 (11): 1478-92DOI: 10.15252/embj.201490546

The end is not the end: remnants of tRNA precursors live on to sponge up small regulatory RNAs

Ziebuhr W, Vogel J (2015)

Mol Cell, 58 (3): 389-90DOI: 10.1016/j.molcel.2015.04.032

Genome-wide transcription start site profiling in biofilm-grown Burkholderia cenocepacia J2315

Sass A, van Acker H, Förstner K, van Nieuwerburgh F, Deforce D, Vogel J, Coenye T (2015)

BMC Genomics, 16: 775DOI: 10.1186/s12864-015-1993-3

2014

Differential RNA-seq: the approach behind and the biological insight gained

Sharma C, Vogel J (2014)

Curr Opin Microbiol, 19: 97-105DOI: 10.1016/j.mib.2014.06.010

READemption-a tool for the computational analysis of deep-sequencing-based transcriptome data

Förstner K, Vogel J, Sharma C (2014)

Bioinformatics, 30 (23): 3421-3DOI: 10.1093/bioinformatics/btu533

Recognition of the small regulatory RNA RydC by the bacterial Hfq protein

Dimastrogiovanni D, Fröhlich K, Bandyra K, Bruce H, Hohensee S, Vogel J, Luisi B (2014)

Elife, 3: 05375DOI: 10.7554/eLife.05375

A bacterial seek-and-destroy system for foreign DNA

Vogel J (2014)

Science, 344 (6187): 972-3DOI: 10.1126/science.1252962

Small RNA functions in carbon metabolism and virulence of enteric pathogens

Papenfort K, Vogel J (2014)

Front Cell Infect Microbiol, 4: 91DOI: 10.3389/fcimb.2014.00091

Identification and Characterization of Small Non-coding RNAs in Bacteria

Podkaminski D, Bouvier M, Vogel J (2014)

, 136: 719-786DOI: 10.1002/9783527647064.ch33

2013

β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity

Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A, Blázquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I (2013)

Nature Communications, 4: 1610DOI: 10.1038/ncomms2607

Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA

Göpel Y, Papenfort K, Reichenbach B, Vogel J, Görke B (2013)

Gene Dev, 27 (5): 552-64DOI: 10.1101/gad.210112.112

Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis

Zhang Y, Heidrich N, Ampattu B, Gunderson C, Seifert H, Schoen C, Vogel J, Sontheimer E (2013)

Mol Cell, 50 (4): 488-503DOI: 10.1016/j.molcel.2013.05.001

Same same but different: new structural insight into CRISPR-Cas complexes

Heidrich N, Vogel J (2013)

Mol Cell, 52 (1): 4-7DOI: 10.1016/j.molcel.2013.09.023.

Comparative genomics boosts target prediction for bacterial small RNAs

Wright P, Richter A, Papenfort K, Mann M, Vogel J, Hess W, Backofen R, Georg J (2013)

Proc Natl Acad Sci U S A, 110 (37): 3487-96DOI: 10.1073/pnas.1303248110

Alexander Böhm (1971-2012)

Boos W, Parkinson J, Jenal U, Vogel J, Søgaard-Andersen L (2013)

Mol Microbiol, 88 (2): 219-21DOI: 10.1111/mmi.12198

Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing

Schulte L, Westermann A, Vogel J (2013)

Nucleic Acids Res, 41 (1): 542-53DOI: 10.1093/nar/gks1030

Bacterial regulatory mechanisms: the gene and beyond

Bassler B, Vogel J (2013)

Curr Opin Microbiol, 16 (2): 109-11DOI: 10.1016/j.mib.2013.04.001

CRISPRs extending their reach: prokaryotic RNAi protein Cas9 recruited for gene regulation

Heidrich N, Vogel J (2013)

EMBO J, 32 (13): 1802-4DOI: 10.1038/emboj.2013.141

Small RNA-Mediated Activation of Sugar Phosphatase mRNA Regulates Glucose Homeostasis

Papenfort K, Sun Y, Miyakoshi M, Vanderpool C, Vogel J (2013)

Cell, 153 (2): 426-437DOI: 10.1016/j.cell.2013.03.003

RNA-mediated regulation in pathogenic bacteria

Caldelari I, Chao Y, Romby P, Vogel J (2013)

Cold Spring Harb Perspect Med, 3 (9): 01029DOI: 10.1101/cshperspect.a010298

A small RNA activates CFA synthase by isoform-specific mRNA stabilization

Fröhlich K, Papenfort K, Fekete A, Vogel J (2013)

EMBO J, 32 (22): 2963-79DOI: 10.1038/emboj.2013.222

Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation

Papenfort K, Corcoran C, Gupta S, Miyakoshi M, Heidrich N, Chao Y, Fröhlich K, Ziebuhr W, Böhm A, Vogel J, Sharma C (2013)

In: Regulation of Bacterial Virulence (eds Darwin AJ, Vasil ML): 493-527DOI: 10.1128/9781555818524.ch25

2012

Experimental tools to identify RNA-protein interactions in Helicobacter pylori

Rieder R, Reinhardt R, Sharma C, Vogel J (2012)

RNA biology, 9 (4): 520-31DOI: 10.4161/rna.20331

Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA

Corcoran C, Podkaminski D, Papenfort K, Urban J, Hinton J, Vogel J (2012)

Mol Microbiol, 84 (3): 428-45DOI: 10.1111/j.1365-2958.2012.08031.x

Hfq-associated Regulatory Small RNAs

Corcoran C, Papenfort K, Vogel J (2012)

In: Regulatory RNAs in Prokaryotes (eds Marchfelder A, Hess WR): 15-50DOI: 10.1007/978-3-7091-0218-3_2

The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E

Bandyra K, Said N, Pfeiffer V, Górna M, Vogel J, Luisi B (2012)

Mol Cell, 47 (6): 943-53DOI: 10.1016/j.molcel.2012.07.015

Differential RNA Sequencing (dRNA-Seq): Deep-Sequencing-Based Analysis of Primary Transcriptomes

Borries A, Vogel J, Sharma C (2012)

In: Tag-based next generation sequencing (eds Kahl G, Harbers M ), 316: 109-121DOI: 10.1002/9783527644582.ch7

The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA PolymeraseCWOA

Zhelyazkova P, Sharma C, Förstner K, Liere K, Vogel J, Börner T (2012)

Plant Cell, 24 (1): 123-36DOI: 10.1105/tpc.111.089441

An atlas of Hfq-bound transcripts reveals 3' UTRs as a genomic reservoir of regulatory small RNAs

Chao Y, Papenfort K, Reinhardt R, Sharma C, Vogel J (2012)

EMBO J, 31 (20): 4005-19DOI: 10.1038/emboj.2012.229

RelA protein stimulates the activity of RyhB small RNA by acting on RNA-binding protein Hfq

Argaman L, Elgrably-Weiss M, Hershko T, Vogel J, Altuvia S (2012)

Proc Natl Acad Sci U S A, 109 (12): 4621-6DOI: 10.1073/pnas.1113113109

The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair

Papenfort K, Podkaminski D, Hinton J, Vogel J (2012)

Proc Natl Acad Sci U S A, 109 (13): 757-64DOI: 10.1073/pnas.1119414109

Small RNAs of the Bradyrhizobium/Rhodopseudomonas lineage and their analysis

Madhugiri R, Pessi G, Voss B, Hahn J, Sharma C, Reinhardt R, Vogel J, Hess W, Fischer H, Evguenieva-Hackenberg E (2012)

RNA biology, 9 (1): 47-58DOI: 10.4161/rna.9.1.18008

Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression

Lioliou E, Sharma C, Caldelari I, Helfer A, Fechter P, Vandenesch F, Vogel J, Romby P (2012)

Plos Genet, 8 (6): 10027DOI: 10.1371/journal.pgen.1002782

The csgD mRNA as a hub for signal integration via multiple small RNAs

Boehm A, Vogel J (2012)

Mol Microbiol, 84 (1): 1-5DOI: 10.1111/j.1365-2958.2012.08033.x

Use of aptamer tagging to identify in vivo protein binding partners of small regulatory RNAs

Corcoran C, Rieder R, Podkaminski D, Hofmann B, Vogel J (2012)

In: Bacterial Regulatory RNA: Methods and protocols (ed Keiler KC), 905: 177-200DOI: 10.1007/978-1-61779-949-5_11

The mammalian microRNA response to bacterial infections

Eulalio A, Schulte L, Vogel J (2012)

RNA biology, 9 (6): 742-50DOI: 10.4161/rna.20018

The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium

Kröger C, Dillon S, Cameron A, Papenfort K, Sivasankaran S, Hokamp K, Chao Y, Sittka A, Hébrard M, Händler K, …, Vogel J, Hinton J (2012)

Proc Natl Acad Sci U S A, 109 (20): 1277-86DOI: 10.1073/pnas.1201061109

2011

The transcriptional landscape of Chlamydia pneumoniae

Albrecht M, Sharma C, Dittrich M, Müller T, Reinhardt R, Vogel J, Rudel T (2011)

Genome Biol, 12 (10): 98DOI: 10.1186/gb-2011-12-10-r98

Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA

Sharma C, Papenfort K, Pernitzsch S, Mollenkopf H, Hinton J, Vogel J (2011)

Mol Microbiol, 81 (5): 1144-65DOI: 10.1111/j.1365-2958.2011.07751.x

Sweet Business: Spot42 RNA networks with CRP to Modulate Catabolite Repression

Papenfort K, Vogel J (2011)

Mol Cell, 41 (3): 245-6DOI: 10.1016/j.molcel.2011.01.011

Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions

Schmidtke C, Findeiß S, Sharma C, Kuhfuß J, Hoffmann S, Vogel J, Stadler P, Bonas U (2011)

Nucleic Acids Res, 40 (5): 2020-31DOI: 10.1093/nar/gkr904

CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III

Deltcheva E, Chylinski K, Sharma C, Gonzales K, Chao Y, Pirzada Z, Eckert M, Vogel J, Charpentier E (2011)

Nature, 471 (7340): 602-7DOI: 10.1038/nature09886

Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides

Berghoff B, Glaeser J, Sharma C, Zobawa M, Lottspeich F, Vogel J, Klug G (2011)

Mol Microbiol, 80 (6): 1479-95DOI: 10.1111/j.1365-2958.2011.07658.x

Microbes at their best: first Mol Micro Meeting Würzburg

Böhm A, Papenfort K, Lopez D, Vogel J (2011)

Mol Microbiol, 82 (4): 797-806DOI: 10.1111/j.1365-2958.2011.07852.x

Regulation by small RNAs in bacteria: expanding frontiers

Storz G, Vogel J, Wassarman K (2011)

Mol Cell, 43 (6): 880-91DOI: 10.1016/j.molcel.2011.08.022

A candidate approach implicates the secreted Salmonella effector protein SpvB in P-body disassembly

Eulalio A, Fröhlich K, Mano M, Giacca M, Vogel J (2011)

Plos One, 6 (3): 17296DOI: 10.1371/journal.pone.0017296

Helicobacter pylori interferes with an embryonic stem cell micro RNA cluster to block cell cycle progression

Belair C, Baud J, Chabas S, Sharma C, Vogel J, Staedel C, Darfeuille F (2011)

Silence, 2 (1): 7DOI: 10.1186/1758-907X-2-7

Hfq and its constellation of RNA

Vogel J, Luisi B (2011)

Nat Rev Microbiol, 9 (8): 578-89DOI: 10.1038/nrmicro2615

A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD

Fröhlich K, Papenfort K, Berger A, Vogel J (2011)

Nucleic Acids Res, 40 (8): 3623-40DOI: 10.1093/nar/gkr1156

Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon

Gogol E, Rhodius V, Papenfort K, Vogel J, Gross C (2011)

Proc Natl Acad Sci U S A, 108 (31): 12875-80DOI: 10.1073/pnas.1109379108

Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family

Schulte L, Eulalio A, Mollenkopf H, Reinhardt R, Vogel J (2011)

EMBO J, 30 (10): 1977-89DOI: 10.1038/emboj.2011.94

An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803

Mitschke J, Georg J, Scholz I, Sharma C, Dienst D, Bantscheff J, Voss B, Steglich C, Wilde A, Vogel J, Hess W (2011)

Proc Natl Acad Sci U S A, 108 (5): 2124-9DOI: 10.1073/pnas.1015154108

2010

The primary transcriptome of the major human pathogen Helicobacter pylori

Sharma C, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt R, Stadler P, Vogel J (2010)

Nature, 464 (7286): 250-5DOI: 10.1038/nature08756

The role of Hfq in bacterial pathogens

Chao Y, Vogel J (2010)

Curr Opin Microbiol, 13 (1): 24-33DOI: 10.1016/j.mib.2010.01.001

Analysis of A to I editing of miRNA in macrophages exposed to salmonella

Heale B, Eulalio A, Schulte L, Vogel J, O'Connell M (2010)

RNA biology, 7 (5): 621-7DOI: 10.4161/rna.7.5.13269

Small RNAs promote mRNA stability to activate the synthesis of virulence factors

Podkaminski D, Vogel J (2010)

Mol Microbiol, 78 (6): 1327-31DOI: 10.1111/j.1365-2958.2010.07428.x

Identification of regulatory RNAs in Bacillus subtilis

Irnov I, Sharma C, Vogel J, Winkler W (2010)

Nucleic Acids Res, 38 (19): 6637-51DOI: 10.1093/nar/gkq454

Regulatory RNA in bacterial pathogens

Papenfort K, Vogel J (2010)

Cell Host Microbe, 8 (1): 116-27DOI: 10.1016/j.chom.2010.06.008

Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA

Papenfort K, Bouvier M, Mika F, Sharma C, Vogel J (2010)

Proc Natl Acad Sci U S A, 107 (47): 20435-40DOI: 10.1073/pnas.1009784107

Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome

Albrecht M, Sharma C, Reinhardt R, Vogel J, Rudel T (2010)

Nucleic Acids Res, 38 (3): 868-77DOI: 10.1093/nar/gkp1032

Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism

Bohn C, Rigoulay C, Chabelskaya S, Sharma C, Marchais A, Skorski P, Borezée-Durant E, Barbet R, Jacquet E, Jacq A, …, Vogel J, Bouloc P (2010)

Nucleic Acids Res, 38 (19): 6620-36DOI: 10.1093/nar/gkq462

2009

Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation

Pfeiffer V, Papenfort K, Lucchini S, Hinton J, Vogel J (2009)

Nat Struct Mol Biol, 16 (8): 840-6DOI: 10.1038/nsmb.1631

Fast mapping of short sequences with mismatches, insertions and deletions using index structures

Hoffmann S, Otto C, Kurtz S, Sharma C, Khaitovich P, Vogel J, Stadler P, Hackermüller J (2009)

PLos Comput Biol, 5 (9): 10005DOI: 10.1371/journal.pcbi.1000502

In vivo expression and purification of aptamer-tagged small RNA regulators

Said N, Rieder R, Hurwitz R, Deckert J, Urlaub H, Vogel J (2009)

Nucleic Acids Res, 37 (20): 133-DOI: 10.1093/nar/gkp719

A green fluorescent protein (GFP)-based plasmid system to study post-transcriptional control of gene expression in vivo

Urban J, Vogel J (2009)

In: Riboswitches: Methods and protocols (ed Serganov A), Methods Mol Biol, 540: 301-19DOI: 10.1007/978-1-59745-558-9_22

Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA

Papenfort K, Said N, Welsink T, Lucchini S, Hinton J, Vogel J (2009)

Mol Microbiol, 74 (1): 139-158DOI: 10.1111/j.1365-2958.2009.06857.x

An RNA trap helps bacteria get the most out of chitosugars

Vogel J (2009)

Mol Microbiol, 73 (5): 737-41DOI: 10.1111/j.1365-2958.2009.06806.x

Deep sequencing analysis of the Methanosarcina mazei Gö1 transcriptome in response to nitrogen availability

Jäger D, Sharma C, Thomsen J, Ehlers C, Vogel J, Schmitz R (2009)

Proc Natl Acad Sci U S A, 106 (51): 21878-82DOI: 10.1073/pnas.0909051106

Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level

Papenfort K, Vogel J (2009)

Res Microbiol, 160 (4): 278-87DOI: 10.1016/j.resmic.2009.03.004

Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides

Berghoff B, Glaeser J, Sharma C, Vogel J, Klug G (2009)

Mol Microbiol, 74 (6): 1497-512DOI: 10.1111/j.1365-2958.2009.06949.x

Experimental approaches for the discovery and characterization of regulatory small RNA

Sharma C, Vogel J (2009)

Curr Opin Microbiol, 12 (5): 536-46DOI: 10.1016/j.mib.2009.07.006

A rough guide to the non-coding RNA world of Salmonella

Vogel J (2009)

Mol Microbiol, 71 (1): 1-11DOI: 10.1111/j.1365-2958.2008.06505.x

Activation of gene expression by small RNA

Fröhlich K, Vogel J (2009)

Curr Opin Microbiol, 12 (6): 674-82DOI: 10.1016/j.mib.2009.09.009

Acid stress activation of the sigma(E) stress response in Salmonella enterica serovar Typhimurium

Muller C, Bang I, Velayudhan J, Karlinsey J, Papenfort K, Vogel J, Fang F (2009)

Mol Microbiol, 71 (5): 1228-38DOI: 10.1111/j.1365-2958.2009.06597.x

Regulatory RNAs in prokaryotes: here, there and everywhere

Narberhaus F, Vogel J (2009)

Mol Microbiol, 74 (2): 261-9DOI: 10.1111/j.1365-2958.2009.06869.x

2008

Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq

Sittka A, Lucchini S, Papenfort K, Sharma C, Rolle K, Binnewies T, Hinton J, Vogel J (2008)

Plos Genet, 4 (8): 10001DOI: 10.1371/journal.pgen.1000163

Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation

Urban J, Vogel J (2008)

PLos Biol, 6 (3): 64DOI: 10.1371/journal.pbio.0060064

A Glimpse at the Evolution of Virulence Control

Sittka A, Vogel J (2008)

Cell Host Microbe, 4 (4): 310-312DOI: 10.1016/j.chom.2008.09.006

Small RNA binding to 5' mRNA coding region inhibits translational initiation

Bouvier M, Sharma C, Mika F, Nierhaus K, Vogel J (2008)

Mol Cell, 32 (6): 827-837DOI: 10.1016/j.molcel.2008.10.027

A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles

Song T, Mika F, Lindmark B, Liu Z, Schild S, Bishop A, Zhu J, Camilli A, Johansson J, Vogel J, Wai S (2008)

Mol Microbiol, 70 (1): 100-111DOI: 10.1111/j.1365-2958.2008.06392.x

Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis

Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton J, Vogel J (2008)

Mol Microbiol, 68 (4): 890-906DOI: 10.1111/j.1365-2958.2008.06189.x

RNA: Noncoding

Henry A, Vogel J (2008)

In: Wiley Encyclopedia of Chemical Biology (ed Begley TP), 22: 2183DOI: 10.1002/9780470048672.wecb522

Noncoding RNA control of the making and breaking of sugars

Görke B, Vogel J (2008)

Gene Dev, 22 (21): 2914-25DOI: 10.1101/gad.1717808

The cyanobacterial homologue of the RNA chaperone Hfq is essential for motility of Synechocystis sp. PCC 6803

Dienst D, Dühring U, Mollenkopf H, Vogel J, Golecki J, Hess W, Wilde A (2008)

Microbiology, 154 (Pt 10): 3134-3143DOI: 10.1099/mic.0.2008/020222-0.

2007

Translational control and target recognition by Escherichia coli small RNAs in vivo

Urban J, Vogel J (2007)

Nucleic Acids Res, 35 (3): 1018-37DOI: 10.1093/nar/gkl1040

Sensory and regulatory RNAs in prokaryotes: a new German research focus

Narberhaus F, Vogel J (2007)

RNA biology, 4 (3): 160-4DOI: 10.4161/rna.4.3.5308

An antisense RNA inhibits translation by competing with standby ribosomes

Darfeuille F, Unoson C, Vogel J, Wagner E (2007)

Mol Cell, 26 (3): 381-92DOI: 10.1016/j.molcel.2007.04.003

A conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis

Urban J, Papenfort K, Thomsen J, Schmitz R, Vogel J (2007)

J Mol Biol, 373 (3): 521-8DOI: 10.1016/j.jmb.2007.07.035

The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium

Sittka A, Pfeiffer V, Tedin K, Vogel J (2007)

Mol Microbiol, 63 (1): 193-217DOI: 10.1111/j.1365-2958.2006.05489.x

A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome

Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J (2007)

Mol Microbiol, 66 (5): 1174-91DOI: 10.1111/j.1365-2958.2007.05991.x

Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq

Wilson J, Ott C, Höner zu Bentrup K, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, …, Stefanyshyn-Piper H, Nickerson C (2007)

Proc Natl Acad Sci U.S.A., 104 (41): 16299-304DOI: 10.1073/pnas.0707155104

Characterization of the role of ribonucleases in Salmonella small RNA decay

Viegas S, Pfeiffer V, Sittka A, Silva I, Vogel J, Arraiano C (2007)

Nucleic Acids Res, 35 (22): 7651-64DOI: 10.1093/nar/gkm916

A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites

Sharma C, Darfeuille F, Plantinga T, Vogel J (2007)

Gene Dev, 21 (21): 2804-17DOI: 10.1101/gad.447207

Recent advances in the expression, evolution, and dynamics of prokaryotic genomes

Arraiano C, Bamford J, Brüssow H, Carpousis A, Pelicic V, Pflüger K, Polard P, Vogel J (2007)

J Bacteriol, 189 (17): 6093-100DOI: 10.1128/JB.00612-07

Target identification of small noncoding RNAs in bacteria

Vogel J, Wagner E (2007)

Curr Opin Microbiol, 10 (3): 262-70DOI: 10.1016/j.mib.2007.06.001

2006

Experimental approaches to identify non-coding RNAs

Hüttenhofer A, Vogel J (2006)

Nucleic Acids Res, 34 (2): 635-46DOI: 10.1093/nar/gkj469

σE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay

Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton J, Vogel J (2006)

Mol Microbiol, 62 (6): 1674-1688DOI: 10.1111/j.1365-2958.2006.05524.x

Small non-coding RNAs and the bacterial outer membrane

Vogel J, Papenfort K (2006)

Curr Opin Microbiol, 9 (6): 605-11DOI: 10.1016/j.mib.2006.10.006

2005

Approaches to Identify Novel Non-messenger RNAs in Bacteria and to Investigate their Biological Functions: Functional Analysis of Identified Non-mRNAs

Gerhart E, Wagner H, Vogel J (2005)

In: Handbook of RNA Biochemistry (eds Hartmann RK, Bindereif A, Schön A, Westhof E), 2: 614-642DOI: 10.1002/9783527619504.ch37

Approaches to Identify Novel Non-messenger RNAs in Bacteria and to Investigate their Biological Functions: RNA Mining

Vogel J, Gerhart E, Wagner H (2005)

In: Handbook of RNA Biochemistry (eds Hartmann RK, Bindereif A, Schön A, Westhof E), 2: 595-613DOI: 10.1002/9783527619504.ch36

How to find small non-coding RNAs in bacteria

Vogel J, Sharma C (2005)

Biol Chem, 386 (12): 1219-38DOI: 10.1515/BC.2005.140

Identification of cyanobacterial non-coding RNAs by comparative genome analysis

Axmann I, Kensche P, Vogel J, Kohl S, Herzel H, Hess W (2005)

Genome Biol, 6 (9): 73DOI: 10.1186/gb-2005-6-9-r73

Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA

Udekwu K, Darfeuille F, Vogel J, Reimegård J, Holmqvist E, Wagner E (2005)

Gene Dev, 19 (19): 2355-66DOI: 10.1101/gad.354405

2004

The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide

Vogel J, Argaman L, Wagner E, Altuvia S (2004)

Curr Biol, 14 (24): 2271-6DOI: 10.1016/j.cub.2004.12.003

2002

Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing

Vogel J, Börner T (2002)

EMBO J, 21 (14): 3794-803DOI: 10.1093/emboj/cdf359

2001

Novel small RNA-encoding genes in the intergenic regions of Escherichia coli

Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner E, Margalit H, Altuvia S (2001)

Curr Biol, 11 (12): 941-50

Research projects

Discovery of functional RNAs in the microbiome

The major classes of bacterial noncoding RNA are known only for a few species, meaning that the RNA biology of the vast majority of microbes that are important for human health remains unexplored. Exploiting RNA as a programmable antibiotic to treat bacterial infections and dysbiosis requires that we comprehensively understand the major RNA-based pathways and mechanisms in these species. Over the years, we have pioneered a number of RNA deep sequencing-based methods such as differential RNA-seq (Sharma et al. 2010 Nature) or Dual RNA-seq (Westermann et al. 2016 Nature) to understand which and when RNAs are expressed during the course of an infection. Moreover, with Grad-seq (Smirnov et al. 2016 PNAS) we can now classify potentially all cellular transcripts in an unbiased manner based on their biochemical behaviour. Using these approaches, we are beginning to chart the full cosmos of noncoding RNA functions in the human microbiome.
 

New RNA-binding proteins

Noncoding RNA molecules generally interact with RNA-binding proteins (RBPs) to become functional in the cellular environment. Decades of work in eukaryotes have established RBPs as a pillar of post-transcriptional gene control, with numbers ranging from the hundreds to thousands in vertebrates, invertebrates and yeast cells. Ironically, we know relatively little about the number of RBPs and the mechanisms by which they function in the organisms that seem the easiest to analyse: bacteria. Although bacteria extensively regulate gene expression at the RNA level, our knowledge of global RBPs remains limited to the small RNA chaperone Hfq and the translational repressor CsrA. However, increasing evidence, including the serendipitous discovery of CRISPR-Cas systems, suggests that many RBPs await discovery especially in less well studied microbes.

We have discovered the “osmoregulatory” protein ProQ as a new abundant RBP which binds hundreds cellular RNAs in Salmonella and E. coli (Smirnov et al. 2016 PNAS), including various small RNAs. Our results for ProQ suggest new molecular mechanisms of bacterial gene control at mRNA 3’ ends and a novel regulatory network whereby ProQ recognizes RNA structure rather than primary sequence (Smirnov et al. 2017 EMBO J Holmqvist et al. 2018 Molecular Cell). We are also addressing the fundamental principles involved in RNA recognition by trying to understand how members of this RBP family use the FinO domain for either highly specific or global RNA recognition in the same cellular environment. Continuing with RBP discovery, we are now exploring the microbiome for new RBPs.

Single-cell RNA biology

The development of single-cell RNA-seq and its ability to describe the gene expression profiles of individual cells rather than the average cellular population is rapidly changing our view of many aspects of biology, including the discovery of new cell types and functions. Single-cell RNA-seq is also emerging as a powerful tool to determine cell-to-cell variability in bacterial pathogenesis, however, technical issues have restricted its use to the analysis of eukaryotic transcriptomes. For example, we have studied how heterogeneous intracellular growth of Salmonella drives the polarization state of individually infected macrophages (Saliba et al. 2016 Nature Microbiology). 

Our grand challenge is to fully establish single-cell RNA-seq for bacteria, which is currently hampered by the small amounts of cellular RNA present and the lack of a polyA tail for easy cDNA priming as in eukaryotes. Transcriptomes from single bacteria will provide insight into the basis for phenotypic resistance to antibiotic treatment, stochastic persister formation, and phenotypic diversification for bet hedging, poorly understood phenomena that are threatening our ability to successfully treat bacterial infections. It will also be the next step for developing single-cell Dual RNA-seq to simultaneously study individual host-pathogen interactions. Going beyond simple single-cell transcriptomics, our long-term ambition is to develop robust methodologies for routine high-throughput RNA biochemistry to study post-transcriptional control in single bacterial cells.

The RNA route to manipulation of the microbiota

Our body is colonized by a vast array of bacteria, which together form the human microbiome. The gut alone harbours more than 1,000 bacterial species. An understanding of their individual or synergistic contributions to human health and disease demands a means to interfere and perturb their functions on the species level, with a selectivity that is not possible using currently available antibiotics. 

Our ultimate goal is precision manipulation of the human microbiome using “programmable antibiotics” in the form of RNA-directed antisense oligonucleotides (ASOs). The same approach can be taken to target antibiotic-resistant pathogens as an alternative to standard antibiotics. These ASOs are coupled to small peptides that carry them inside the bacteria to silence the mRNAs of essential genes. There is already proof-of-principle for this exciting concept, but many open questions remain. What does it take to make these ASOs truly species-specific; how can we minimize potential off-target effects; what are the most effective peptides for delivery; what about the host response and bacterial resistance mechanisms? Since there is unlikely to be a one case-fits-all solution for all microbiome species, this project can only succeed by integrating diverse expertise from RNA biology, microbiology, immunology, single-cell biology, and pharmacy.

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