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

Prof Jörg Vogel
Group Leader

Dr Tobias Kerrinnes
Lab Coordinator

Dr Afsaneh Khani
Postdoc

Dr Karl Gatterdam
Postdoc

Dr Kotaro Chihara
Postdoc

Dr Linda Popella
Postdoc

Dr Milan Gerovac
Postdoc

Petia Kovatcheva-Datchary
Postdoc

Svetlana Durica-Mitic
Postdoc

Dr Wael Bazzi
Postdoc

Dr Youssef Elmouali
Postdoc

Christina Homberger
PhD Student

Elisa Venturini
PhD Student

Falk Ponath
PhD Student

Gianluca Matera
PhD Student

Jakob Jung
PhD Student

Jens Hör
PhD Student

Barbara Plaschke
Technical Assistant

Dr Esther Gottwald
Technical Assistant
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.

Publications
2020
Grad-seq shines light on unrecognized RNA and protein complexes in the model bacterium Escherichia coli
Hör J, Di Giorgio S, Gerovac M, Venturini E, Förstner KU, Vogel J (2020)
Nucleic Acids Research, 48 (16): 9301-9319
LifeTime and improving European healthcare through cell-based interceptive medicine
Rajewsky N, Almouzni G, Gorski SA, Aerts S, Amit I, Bertero MG, Bock C, Bredenoord AL, Cavalli G, Chiocca S, …, Vidal M, Voet T (2020)
Nature, 587 (7834): 377-386
Single-cell RNA-sequencing reports growth-condition-specific global transcriptomes of individual bacteria
Imdahl F, Vafadarnejad E, Homberger C, Saliba AE, Vogel J (2020)
Nature Microbiology, 5 (10): 1202
Dual RNA-seq of Orientia tsutsugamushi informs on host-pathogen interactions for this neglected intracellular human pathogen
Mika-Gospodorz B, Giengkam S, Westermann AJ, Wongsantichon J, Kion-Crosby W, Chuenklin S, Wang LC, Sunyakumthorn P, Sobota RM, Subbian S, …, Barquist L, Salje J (2020)
Nature Communications, 11: 3363
Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression
Parhi L, Alon-Maimon T, Sol A, Nejman D, Shhadeh A, Fainsod-Levi T, Yajuk O, Isaacson B, Abed J, Maalouf N, …, Straussman R, Bachrach G (2020)
Nature Communications, 11: 3259
The minimal meningococcal ProQ protein has an intrinsic capacity for structure-based global RNA recognition
Bauriedl S, Gerovac M, Heidrich N, Bischler T, Barquist L, Vogel J, Schoen C (2020)
Nature Communications, 11: 2823
Grad-seq in a Gram-positive bacterium reveals exonucleolytic sRNA activation in competence control
Hör J, Garriss G, Di Giorgio S, Hack L, Vanselow JT, Förstner KU, Schlosser A, Henriques-Normark B, Vogel J (2020)
The EMBO Journal, 39 (9): 10385
The conserved 3' UTR-derived small RNA NarS mediates mRNA crossregulation during nitrate respiration
Wang C, Chao Y, Matera G, Gao Q, Vogel J (2020)
Nucleic Acids Research, 48 (4): 2126-2143
Single-Nucleotide RNA Maps for the Two Major Nosocomial Pathogens Enterococcus faecalis and Enterococcus faecium
Michaux C, Hansen EE, Jenniches L, Gerovac M, Barquist L, Vogel J (2020)
Frontiers in Cellular and Infection Microbiology, 10: 60032
The SARS-CoV-2 RNA-protein interactome in infected human cells
Schmidt N, Lareau CA, Keshishian H, Ganskih S, Schneider C, Hennig T, Melanson R, Werner S, Wei Y, Zimmer M, …, Bodem J, Munschauer M (2020)
Nature Microbiology, Preprint
Triple RNA-Seq Reveals Synergy in a Human Virus-Fungus Co-infection Model
Seelbinder B, Wallstabe J, Marischen L, Weiss E, Wurster S, Page L, Löffler C, Bussemer L, Schmitt A, Wolf T, …, Schäuble S, Loeffler J (2020)
Cell Reports, 33 (7): 10838
Introducing differential RNA-seq mapping to track the early infection phase for Pseudomonas phage ɸKZ
Wicke L, Ponath F, Coppens L, Gerovac M, Lavigne R, Vogel J (2020)
RNA Biology: 1-12
Global discovery of bacterial RNA-binding proteins by RNase-sensitive gradient profiles reports a new FinO domain protein
Gerovac M, El Mouali Y, Kuper J, Kisker C, Barquist L, Vogel J (2020)
RNA, 26 (10): 1448-1463
Amidochelocardin Overcomes Resistance Mechanisms Exerted on Tetracyclines and Natural Chelocardin
Hennessen F, Miethke M, Zaburannyi N, Loose M, Lukežic T, Bernecker S, Hüttel S, Jansen R, Schmiedel J, Fritzenwanker M, …, Herrmann J, Müller R (2020)
Antibiotics, 9 (9): 1-19
Seropositivity for pathogens associated with chronic infections is a risk factor for all-cause mortality in the elderly: findings from the Memory and Morbidity in Augsburg Elderly (MEMO) Study
Zeeb M, Kerrinnes T, Cicin-Sain L, Guzman CA, Puppe W, Schulz TF, Peters A, Berger K, Castell S, Karch A (2020)
Geroscience, 42: 1365-1376
Increasing storage stability of freeze-dried plasma using trehalose
Brogna R, Oldenhof H, Sieme H, Figueiredo C, Kerrinnes T, Wolkers WF (2020)
PLOS One, 15 (6): 02345
Improved bacterial RNA-seq by Cas9-based depletion of ribosomal RNA reads
Prezza G, Heckel T, Dietrich S, Homberger C, Westermann AJ, Vogel J (2020)
RNA, 26 (11)
Trans-Acting Small RNAs and Their Effects on Gene Expression in Escherichia coli and Salmonella enterica
Hör J, Matera G, Vogel J, Gottesman S, Storz G (2020)
EcoSal Plus, 9 (1)
Tracheal brush cells release acetylcholine in response to bitter tastants for paracrine and autocrine signaling
Hollenhorst MI, Jurastow I, Nandigama R, Appenzeller S, Li L, Vogel J, Wiederhold S, Althaus M, Empting M, Altmüller J, …, Saliba AE, Krasteva-Christ G (2020)
The FASEB Journal, 34 (1): 316-332
An Advanced Human Intestinal Coculture Model Reveals Compartmentalized Host and Pathogen Strategies during Salmonella Infection
Schulte LN, Schweinlin M, Westermann AJ, Janga H, Santos SC, Appenzeller S, Walles H, Vogel J, Metzger M (2020)
mBio, 11 (1): 03348-19
2019
An RNA Surprise in Bacterial Effector Mechanisms
Gerovac M, Vogel J (2019)
Cell Host & Microbe, 26 (6): 709-711
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 Research, 47 (4): 2075-2088
Conditional Hfq Association with Small Noncoding RNAs in Pseudomonas aeruginosa Revealed through Comparative UV Cross-Linking Immunoprecipitation Followed by High-Throughput Sequencing
Chihara K, Bischler T, Barquist L, Monzon VA, Noda N, Vogel J, Tsuneda S (2019)
mSystems, 4 (6)
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): 390-396
The Major RNA-Binding Protein ProQ Impacts Virulence Gene Expression in Salmonella enterica Serovar Typhimurium
Westermann AJ, Venturini E, Sellin ME, Förstner KU, Hardt W, Vogel J (2019)
mBio, 10 (1): 02504-18
2018
Salmonella persisters undermine host immune defenses during antibiotic treatment
Stapels DA, Hill PW, Westermann AJ, Fisher RA, Thurston TL, Saliba AE, Blommestein I, Vogel J, Helaine S (2018)
Science, 362 (6419): 1156-1160
Genome organization and DNA accessibility control antigenic variation in trypanosomes
Müller LS, Cosentino RO, Förstner KU, Guizetti J, Wedel C, Kaplan N, Janzen CJ, Arampatzi P, Vogel J, Steinbiss S, …, Sebra RP, Siegel TN (2018)
Nature, 563 (7729): 121-125
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)
The EMBO Journal, 37 (23): 98529
RNA-binding proteins in bacteria
Holmqvist E, Vogel J (2018)
Nature Reviews Microbiology, 16 (10): 601-615
Bacterial RNA Biology on a Genome Scale
Hör J, Gorski SA, Vogel J (2018)
Molecular Cell, 70 (5): 785-799
Nuclear lncRNA stabilization in the host response to bacterial infection
Munschauer M, Vogel J (2018)
The EMBO Journal, 37 (13): 99875
Global Maps of ProQ Binding In Vivo Reveal Target Recognition via RNA Structure and Stability Control at mRNA 3' Ends
Holmqvist E, Li L, Bischler T, Barquist L, Vogel J (2018)
Molecular Cell, 70 (5): 971-982
ANNOgesic: a Swiss army knife for the RNA-seq based annotation of bacterial/archaeal genomes
Yu S, Vogel J, Förstner KU (2018)
GigaScience, 7 (9): 096
CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level
El Mouali Y, Gaviria-Cantin T, Sánchez-Romero MA, Gibert M, Westermann AJ, Vogel J, Balsalobre C (2018)
PLOS Genetics, 14 (6): 10074
Host-Pathogen Transcriptomics by Dual RNA-Seq
Westermann AJ, Vogel J (2018)
In: Arluison V., Valverde C. (eds) Bacterial Regulatory RNA, Methods Mol Biol (Methods in Molecular Biology), 1737: 59-75
2017
RNA-based recognition and targeting: sowing the seeds of specificity
Gorski SA, Vogel J, Doudna JA (2017)
Nature Reviews Molecular Cell Biology, 18 (4): 215-228
APRICOT: an integrated computational pipeline for the sequence-based identification and characterization of RNA-binding proteins
Sharan M, Förstner KU, Eulalio A, Vogel J (2017)
Nucleic Acids Research, 45 (11): 96
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 KU, Said N, Corcoran C, Smiga M, Papenfort K, Reinhardt R, Wieden H, Luisi BF, Vogel J (2017)
Molecular Cell, 65 (1): 39-51
Molecular mechanism of mRNA repression in trans by a ProQ‐dependent small RNA
Smirnov A, Wang C, Drewry LL, Vogel J (2017)
The EMBO Journal, 36 (8): 1029-45
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 Research, 45 (10): 6147-6167
A systematic analysis of the RNA-targeting potential of secreted bacterial effector proteins
Tawk C, Sharan M, Eulalio A, Vogel J (2017)
Scientific Reports, 7 (1): 9328
Einzelzell-RNA-Sequenzierung beleuchtet den Infektionsprozess
Saliba AE, Westermann AJ, Vogel J (2017)
BIOspektrum, 23 (5): 525-528
Structure of the Escherichia coli ProQ RNA-binding protein
Gonzalez GM, Hardwick SW, Maslen SL, Skehel JM, Holmqvist E, Vogel J, Bateman A, Luisi BF, Broadhurst RW (2017)
RNA, 23 (5): 696-711
New RNA-seq approaches for the study of bacterial pathogens
Saliba AE, Santos SC, Vogel J (2017)
Current Opinion in Microbiology, 35: 78-87
Discovery of new RNA classes and global RNA-binding proteins
Smirnov A, Schneider C, Hör J, Vogel J (2017)
Current Opinion in Microbiology, 39: 152-160
RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE
Michaux C, Holmqvist E, Vasicek E, Sharan M, Barquist L, Westermann AJ, Gunn JS, Vogel J (2017)
Proceedings of the National Academy of Sciences of the United States of America, 114 (26): 6824-6829
Resolving host-pathogen interactions by dual RNA-seq
Westermann AJ, Barquist L, Vogel J (2017)
PLOS Pathogens, 13 (2): 10060
2016
An expanded evaluation of protein function prediction methods shows an improvement in accuracy
Jiang Y, Oron TR, Clark WT, Bankapur AR, D'Andrea D, Lepore R, Funk CS, Kahanda I, Verspoor KM, Ben-Hur A, …, Friedberg I, Radivojac P (2016)
Genome Biology, 17 (1): 184
The target spectrum of SdsR small RNA in Salmonella
Fröhlich KS, Haneke K, Papenfort K, Vogel J (2016)
Nucleic Acids Research, 44 (21): 10406-22
A 3' UTR-Derived Small RNA Provides the Regulatory Noncoding Arm of the Inner Membrane Stress Response
Chao Y, Vogel J (2016)
Molecular Cell, 61 (3): 352-363
Single-cell RNA-seq ties macrophage polarization to growth rate of intracellular Salmonella
Saliba AE, Li L, Westermann AJ, Appenzeller S, Stapels DA, Schulte LN, Helaine S, Vogel J (2016)
Nature Microbiology, 2: 16206
Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions
Westermann AJ, Forstner KU, Amman F, Barquist L, Chao Y, Schulte LN, Muller L, Reinhardt R, Stadler PF, Vogel J (2016)
Nature, 529 (7587): 496-501
cis-Encoded Small RNAs, a Conserved Mechanism for Repression of Polysaccharide Utilization in Bacteroides
Cao Y, Förstner KU, Vogel J, Smith CJ (2016)
Journal of Bacteriology, 198 (18): 2410-8
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 KU, Berger M, Bertling C, Sharma CM, Vogel J, Karch H, Dobrindt U, Mellmann A (2016)
Scientific Reports, 6: 35307
Natural mutations in a Staphylococcus aureus virulence regulator attenuate cytotoxicity but permit bacteremia and abscess formation
Das S, Lindemann C, Young BC, Muller J, Österreich B, Ternette N, Winkler A, Paprotka K, Reinhardt R, Förstner KU, …, Wyllie DH, Fraunholz MJ (2016)
Proceedings of the National Academy of Sciences of the United States of America, 113 (22): 3101-10
An NK Cell Perforin Response Elicited via IL-18 Controls Mucosal Inflammation Kinetics during Salmonella Gut Infection
Müller AA, Dolowschiak T, Sellin ME, Felmy B, Verbree C, Gadient S, Westermann AJ, Vogel J, LeibundGut-Landmann S, Hardt W (2016)
PLOS Pathogens, 12 (6): 10057
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 Genetics, 12 (4): 10059
Emerging roles of RNA modifications in bacteria
Marbaniang CN, Vogel J (2016)
Current Opinion in Microbiology, 30: 50-57
Grad-seq guides the discovery of ProQ as a major small RNA-binding protein
Smirnov A, Förstner KU, Holmqvist E, Otto A, Günster R, Becher D, Reinhardt R, Vogel J (2016)
Proceedings of the National Academy of Sciences of the United States of America, 113 (41): 11591-11596
Molecular phenotyping of infection-associated small non-coding RNAs
Barquist L, Westermann AJ, Vogel J (2016)
Philosophical Transactions of the Royal Society of London B: Biological Sciences, 371 (1707): 20160
Global RNA recognition patterns of post-transcriptional regulators Hfq and CsrA revealed by UV crosslinking in vivo
Holmqvist E, Wright PR, Li L, Bischler T, Barquist L, Reinhardt R, Backofen R, Vogel J (2016)
The EMBO Journal, 35 (9): 991-1011
2015
The end is not the end: remnants of tRNA precursors live on to sponge up small regulatory RNAs
Ziebuhr W, Vogel J (2015)
Molecular Cell, 58 (3): 389-90
Accelerating Discovery and Functional Analysis of Small RNAs with New Technologies
Barquist L, Vogel J (2015)
Annual Review of Genetics, 49: 367-94
Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella
Papenfort K, Espinosa E, Casadesús J, Vogel J (2015)
Proceedings of the National Academy of Sciences of the United States of America, 112 (34): 4772-81
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): 01420
Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA
Miyakoshi M, Chao Y, Vogel J (2015)
The EMBO Journal, 34 (11): 1478-92
Investigating CRISPR RNA Biogenesis and Function Using RNA-seq
Heidrich N, Dugar G, Vogel J, Sharma CM (2015)
In: CRISPR: Methods and protocols (eds Lundgren M, Charpentier E, Fineran PC), Methods Mol Biol (Methods in Molecular Biology), 1311: 1-21
Regulatory small RNAs from the 3' regions of bacterial mRNAs
Miyakoshi M, Chao Y, Vogel J (2015)
Current Opinion in Microbiology, 24: 132-9
Genome-wide transcription start site profiling in biofilm-grown Burkholderia cenocepacia J2315
Sass AM, van Acker H, Förstner KU, van Nieuwerburgh F, Deforce D, Vogel J, Coenye T (2015)
BMC Genomics, 16: 775
Dual 3'Seq using deepSuperSAGE uncovers transcriptomes of interacting Salmonella enterica Typhimurium and human host cells
Afonso-Grunz F, Hoffmeier K, Müller S, Westermann AJ, Rotter B, Vogel J, Winter P, Kahl G (2015)
BMC Genomics, 16: 323
2014
Identification and Characterization of Small Non-coding RNAs in Bacteria
Podkaminski D, Bouvier M, Vogel J (2014)
, 136: 719-786
READemption-a tool for the computational analysis of deep-sequencing-based transcriptome data
Förstner KU, Vogel J, Sharma CM (2014)
Bioinformatics, 30 (23): 3421-3
Meeting report: Regulating with RNA in Bacteria 2013
Vogel J, Gottesman S, Belasco J, Narberhaus F (2014)
RNA Biology, 11 (5): 403-12
Small RNA functions in carbon metabolism and virulence of enteric pathogens
Papenfort K, Vogel J (2014)
Frontiers in Cellular and Infection Microbiology, 4: 91
Recognition of the small regulatory RNA RydC by the bacterial Hfq protein
Dimastrogiovanni D, Fröhlich KS, Bandyra KJ, Bruce HA, Hohensee S, Vogel J, Luisi BF (2014)
eLife, 3: 05375
Differential RNA-seq: the approach behind and the biological insight gained
Sharma CM, Vogel J (2014)
Current Opinion in Microbiology, 19: 97-105
Single-cell RNA-seq: advances and future challenges
Saliba AE, Westermann AJ, Gorski SA, Vogel J (2014)
Nucleic Acids Research, 42 (14): 8845-60
2013
Same same but different: new structural insight into CRISPR-Cas complexes
Heidrich N, Vogel J (2013)
Molecular Cell, 52 (1): 4-7
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: 1610
Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis
Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS, Schoen C, Vogel J, Sontheimer EJ (2013)
Molecular Cell, 50 (4): 488-503
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)
Genes & Development, 27 (5): 552-64
A small RNA activates CFA synthase by isoform-specific mRNA stabilization
Fröhlich KS, Papenfort K, Fekete A, Vogel J (2013)
The EMBO Journal, 32 (22): 2963-79
CRISPRs extending their reach: prokaryotic RNAi protein Cas9 recruited for gene regulation
Heidrich N, Vogel J (2013)
The EMBO Journal, 32 (13): 1802-4
Small RNA-Mediated Activation of Sugar Phosphatase mRNA Regulates Glucose Homeostasis
Papenfort K, Sun Y, Miyakoshi M, Vanderpool CK, Vogel J (2013)
Cell, 153 (2): 426-437
Regulatory Mechanisms of Special Significance: Role of Small RNAs in Virulence Regulation
Papenfort K, Corcoran CP, Gupta SK, Miyakoshi M, Heidrich N, Chao Y, Fröhlich KS, Ziebuhr W, Böhm A, Vogel J, Sharma CM (2013)
In: Regulation of Bacterial Virulence (eds Darwin AJ, Vasil ML): 493-527
RNA-mediated regulation in pathogenic bacteria
Caldelari I, Chao Y, Romby P, Vogel J (2013)
Cold Spring Harbor Perspectives In Medicine, 3 (9): 01029
Bacterial regulatory mechanisms: the gene and beyond
Bassler B, Vogel J (2013)
Current Opinion in Microbiology, 16 (2): 109-11
Comparative genomics boosts target prediction for bacterial small RNAs
Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J (2013)
Proceedings of the National Academy of Sciences of the United States of America, 110 (37): 3487-96
Alexander Böhm (1971-2012)
Boos W, Parkinson JS, Jenal U, Vogel J, Søgaard-Andersen L (2013)
Molecular Microbiology, 88 (2): 219-21
Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing
Schulte LN, Westermann AJ, Vogel J (2013)
Nucleic Acids Research, 41 (1): 542-53
2012
The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E
Bandyra KJ, Said N, Pfeiffer V, Górna MW, Vogel J, Luisi BF (2012)
Molecular Cell, 47 (6): 943-53
Dual RNA-seq of pathogen and host
Westermann AJ, Gorski SA, Vogel J (2012)
Nature Reviews Microbiology, 10 (9): 618-30
The mammalian microRNA response to bacterial infections
Eulalio A, Schulte LN, Vogel J (2012)
RNA Biology, 9 (6): 742-50
Experimental tools to identify RNA-protein interactions in Helicobacter pylori
Rieder R, Reinhardt R, Sharma CM, Vogel J (2012)
RNA Biology, 9 (4): 520-31
Small RNAs of the Bradyrhizobium/Rhodopseudomonas lineage and their analysis
Madhugiri R, Pessi G, Voss B, Hahn J, Sharma CM, Reinhardt R, Vogel J, Hess WR, Fischer H, Evguenieva-Hackenberg E (2012)
RNA Biology, 9 (1): 47-58
The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair
Papenfort K, Podkaminski D, Hinton JC, Vogel J (2012)
Proceedings of the National Academy of Sciences of the United States of America, 109 (13): 757-64
The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium
Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, Chao Y, Sittka A, Hébrard M, Händler K, …, Vogel J, Hinton JC (2012)
Proceedings of the National Academy of Sciences of the United States of America, 109 (20): 1277-86
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)
Proceedings of the National Academy of Sciences of the United States of America, 109 (12): 4621-6
Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression
Lioliou E, Sharma CM, Caldelari I, Helfer A, Fechter P, Vandenesch F, Vogel J, Romby P (2012)
PLOS Genetics, 8 (6): 10027
The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA PolymeraseCWOA
Zhelyazkova P, Sharma CM, Förstner KU, Liere K, Vogel J, Börner T (2012)
The Plant Cell, 24 (1): 123-36
Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA
Corcoran CP, Podkaminski D, Papenfort K, Urban JH, Hinton JC, Vogel J (2012)
Molecular Microbiology, 84 (3): 428-45
The csgD mRNA as a hub for signal integration via multiple small RNAs
Boehm A, Vogel J (2012)
Molecular Microbiology, 84 (1): 1-5
An atlas of Hfq-bound transcripts reveals 3' UTRs as a genomic reservoir of regulatory small RNAs
Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J (2012)
The EMBO Journal, 31 (20): 4005-19
Use of aptamer tagging to identify in vivo protein binding partners of small regulatory RNAs
Corcoran CP, Rieder R, Podkaminski D, Hofmann B, Vogel J (2012)
In: Bacterial Regulatory RNA: Methods and protocols (ed Keiler KC), 905: 177-200
Hfq-associated Regulatory Small RNAs
Corcoran CP, Papenfort K, Vogel J (2012)
In: Regulatory RNAs in Prokaryotes (eds Marchfelder A, Hess WR): 15-50
Differential RNA Sequencing (dRNA-Seq): Deep-Sequencing-Based Analysis of Primary Transcriptomes
Borries A, Vogel J, Sharma CM (2012)
In: Tag-based next generation sequencing (eds Kahl G, Harbers M ), 316: 109-121
2011
Hfq and its constellation of RNA
Vogel J, Luisi BF (2011)
Nature Reviews Microbiology, 9 (8): 578-89
Regulation by small RNAs in bacteria: expanding frontiers
Storz G, Vogel J, Wassarman KM (2011)
Molecular Cell, 43 (6): 880-91
Sweet Business: Spot42 RNA networks with CRP to Modulate Catabolite Repression
Papenfort K, Vogel J (2011)
Molecular Cell, 41 (3): 245-6
CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III
Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011)
Nature, 471 (7340): 602-7
A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD
Fröhlich KS, Papenfort K, Berger AA, Vogel J (2011)
Nucleic Acids Research, 40 (8): 3623-40
Helicobacter pylori interferes with an embryonic stem cell micro RNA cluster to block cell cycle progression
Belair C, Baud J, Chabas S, Sharma CM, Vogel J, Staedel C, Darfeuille F (2011)
Silence, 2 (1): 7
Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon
Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA (2011)
Proceedings of the National Academy of Sciences of the United States of America, 108 (31): 12875-80
An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803
Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J, Voss B, Steglich C, Wilde A, Vogel J, Hess WR (2011)
Proceedings of the National Academy of Sciences of the United States of America, 108 (5): 2124-9
A candidate approach implicates the secreted Salmonella effector protein SpvB in P-body disassembly
Eulalio A, Fröhlich KS, Mano M, Giacca M, Vogel J (2011)
PLOS One, 6 (3): 17296
Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions
Schmidtke C, Findeiß S, Sharma CM, Kuhfuß J, Hoffmann S, Vogel J, Stadler PF, Bonas U (2011)
Nucleic Acids Research, 40 (5): 2020-31
Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA
Sharma CM, Papenfort K, Pernitzsch SR, Mollenkopf H, Hinton JC, Vogel J (2011)
Molecular Microbiology, 81 (5): 1144-65
Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides
Berghoff BA, Glaeser J, Sharma CM, Zobawa M, Lottspeich F, Vogel J, Klug G (2011)
Molecular Microbiology, 80 (6): 1479-95
Microbes at their best: first Mol Micro Meeting Würzburg
Böhm A, Papenfort K, Lopez D, Vogel J (2011)
Molecular Microbiology, 82 (4): 797-806
The transcriptional landscape of Chlamydia pneumoniae
Albrecht M, Sharma CM, Dittrich MT, Müller T, Reinhardt R, Vogel J, Rudel T (2011)
Genome Biology, 12 (10): 98
Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family
Schulte LN, Eulalio A, Mollenkopf H, Reinhardt R, Vogel J (2011)
The EMBO Journal, 30 (10): 1977-89
2010
Regulatory RNA in bacterial pathogens
Papenfort K, Vogel J (2010)
Cell Host & Microbe, 8 (1): 116-27
The primary transcriptome of the major human pathogen Helicobacter pylori
Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt R, Stadler PF, Vogel J (2010)
Nature, 464 (7286): 250-5
The small RNAs of Salmonella
Javayel S, Papenfort K, Vogel J (2010)
In: Salmonella: From Genome to Function (ed Prowollik S)
Analysis of A to I editing of miRNA in macrophages exposed to salmonella
Heale BS, Eulalio A, Schulte LN, Vogel J, O'Connell MA (2010)
RNA Biology, 7 (5): 621-7
Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA
Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J (2010)
Proceedings of the National Academy of Sciences of the United States of America, 107 (47): 20435-40
Identification of regulatory RNAs in Bacillus subtilis
Irnov I, Sharma CM, Vogel J, Winkler WC (2010)
Nucleic Acids Research, 38 (19): 6637-51
Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome
Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T (2010)
Nucleic Acids Research, 38 (3): 868-77
Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism
Bohn C, Rigoulay C, Chabelskaya S, Sharma CM, Marchais A, Skorski P, Borezée-Durant E, Barbet R, Jacquet E, Jacq A, …, Vogel J, Bouloc P (2010)
Nucleic Acids Research, 38 (19): 6620-36
Small RNAs promote mRNA stability to activate the synthesis of virulence factors
Podkaminski D, Vogel J (2010)
Molecular Microbiology, 78 (6): 1327-31
The role of Hfq in bacterial pathogens
Chao Y, Vogel J (2010)
Current Opinion in Microbiology, 13 (1): 24-33
2009
Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation
Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J (2009)
Nature Structural & Molecular Biology, 16 (8): 840-6
A small RNA cascade regulates aminosugar synthesis
Vogel J (2009)
In: Nova Acta Leopoldina, 378: 41-50
A green fluorescent protein (GFP)-based plasmid system to study post-transcriptional control of gene expression in vivo
Urban JH, Vogel J (2009)
In: Riboswitches: Methods and protocols (ed Serganov A), Methods Mol Biol, 540: 301-19
Deep sequencing of Salmonella RNA associated with heterologous Hfq proteins in vivo reveals small RNAs as a major target class and identifies RNA processing phenotypes
Sittka A, Sharma CM, Rolle K, Vogel J (2009)
RNA Biology, 6 (3): 266-75
Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level
Papenfort K, Vogel J (2009)
Research in Microbiology, 160 (4): 278-87
Deep sequencing analysis of the Methanosarcina mazei Gö1 transcriptome in response to nitrogen availability
Jäger D, Sharma CM, Thomsen J, Ehlers C, Vogel J, Schmitz RA (2009)
Proceedings of the National Academy of Sciences of the United States of America, 106 (51): 21878-82
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 Research, 37 (20): 133-
An RNA trap helps bacteria get the most out of chitosugars
Vogel J (2009)
Molecular Microbiology, 73 (5): 737-41
A rough guide to the non-coding RNA world of Salmonella
Vogel J (2009)
Molecular Microbiology, 71 (1): 1-11
Regulatory RNAs in prokaryotes: here, there and everywhere
Narberhaus F, Vogel J (2009)
Molecular Microbiology, 74 (2): 261-9
Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides
Berghoff BA, Glaeser J, Sharma CM, Vogel J, Klug G (2009)
Molecular Microbiology, 74 (6): 1497-512
Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA
Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009)
Molecular Microbiology, 74 (1): 139-158
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 FC (2009)
Molecular Microbiology, 71 (5): 1228-38
Fast mapping of short sequences with mismatches, insertions and deletions using index structures
Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J, Stadler PF, Hackermüller J (2009)
PLOS Computational Biology, 5 (9): 10005
Experimental approaches for the discovery and characterization of regulatory small RNA
Sharma CM, Vogel J (2009)
Current Opinion in Microbiology, 12 (5): 536-46
Activation of gene expression by small RNA
Fröhlich KS, Vogel J (2009)
Current Opinion in Microbiology, 12 (6): 674-82
2008
Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation
Urban JH, Vogel J (2008)
PLOS Biology, 6 (3): 64
Small RNA binding to 5' mRNA coding region inhibits translational initiation
Bouvier M, Sharma CM, Mika F, Nierhaus KH, Vogel J (2008)
Molecular Cell, 32 (6): 827-837
Noncoding RNA control of the making and breaking of sugars
Görke B, Vogel J (2008)
Genes & Development, 22 (21): 2914-25
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 WR, Wilde A (2008)
Microbiology, 154 (Pt 10): 3134-3143
RNA: Noncoding
Henry AA, Vogel J (2008)
In: Wiley Encyclopedia of Chemical Biology (ed Begley TP), 22: 2183
Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq
Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J (2008)
PLOS Genetics, 4 (8): 10001
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 SN (2008)
Molecular Microbiology, 70 (1): 100-111
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 JC, Vogel J (2008)
Molecular Microbiology, 68 (4): 890-906
A Glimpse at the Evolution of Virulence Control
Sittka A, Vogel J (2008)
Cell Host & Microbe, 4 (4): 310-312
2007
An antisense RNA inhibits translation by competing with standby ribosomes
Darfeuille F, Unoson C, Vogel J, Wagner EG (2007)
Molecular Cell, 26 (3): 381-92
A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites
Sharma CM, Darfeuille F, Plantinga TH, Vogel J (2007)
Genes & Development, 21 (21): 2804-17
Recent advances in the expression, evolution, and dynamics of prokaryotic genomes
Arraiano CM, Bamford J, Brüssow H, Carpousis AJ, Pelicic V, Pflüger K, Polard P, Vogel J (2007)
Journal of Bacteriology, 189 (17): 6093-100
Sensory and regulatory RNAs in prokaryotes: a new German research focus
Narberhaus F, Vogel J (2007)
RNA Biology, 4 (3): 160-4
The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium
Sittka A, Pfeiffer V, Tedin K, Vogel J (2007)
Molecular Microbiology, 63 (1): 193-217
Translational control and target recognition by Escherichia coli small RNAs in vivo
Urban JH, Vogel J (2007)
Journal of Molecular Biology, 35 (3): 1018-37
A conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis
Urban JH, Papenfort K, Thomsen J, Schmitz RA, Vogel J (2007)
Journal of Molecular Biology, 373 (3): 521-8
Characterization of the role of ribonucleases in Salmonella small RNA decay
Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, Arraiano CM (2007)
Nucleic Acids Research, 35 (22): 7651-64
Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq
Wilson JW, Ott CM, Höner zu Bentrup K, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, …, Stefanyshyn-Piper HM, Nickerson CA (2007)
Proceedings of the National Academy of Sciences of the United States of America, 104 (41): 16299-304
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)
Molecular Microbiology, 66 (5): 1174-91
Target identification of small noncoding RNAs in bacteria
Vogel J, Wagner EG (2007)
Current Opinion in Microbiology, 10 (3): 262-70
2006
Small non-coding RNAs and the bacterial outer membrane
Vogel J, Papenfort K (2006)
Current Opinion in Microbiology, 9 (6): 605-11
Experimental approaches to identify non-coding RNAs
Hüttenhofer A, Vogel J (2006)
Nucleic Acids Research, 34 (2): 635-46
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 JC, Vogel J (2006)
Molecular Microbiology, 62 (6): 1674-1688
2005
Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA
Udekwu KI, Darfeuille F, Vogel J, Reimegård J, Holmqvist E, Wagner EG (2005)
Genes & Development, 19 (19): 2355-66
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: 614-642
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: 595-613
How to find small non-coding RNAs in bacteria
Vogel J, Sharma CM (2005)
Biological Chemistry, 386 (12): 1219-38
Identification of cyanobacterial non-coding RNAs by comparative genome analysis
Axmann IM, Kensche P, Vogel J, Kohl S, Herzel H, Hess WR (2005)
Genome Biology, 6 (9): 73
2004
The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide
Vogel J, Argaman L, Wagner EG, Altuvia S (2004)
Current Biology, 14 (24): 2271-6
2003
Experimental and computational analysis of transcriptional start sites in the cyanobacterium Prochlorococcus MED4
Vogel J, Axmann IM, Herzel H, Hess WR (2003)
Nucleic Acids Research, 31 (11): 2890-9
RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria
Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jäger JG, Hüttenhofer A, Wagner EG (2003)
Nucleic Acids Research, 31 (22): 6435-43
2002
Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing
Vogel J, Börner T (2002)
The EMBO Journal, 21 (14): 3794-803
2001
Complete 5' and 3' end maturation of group II intron-containing tRNA precursors
Vogel J, Hess WR (2001)
RNA, 7 (2): 285-92
Novel small RNA-encoding genes in the intergenic regions of Escherichia coli
Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S (2001)
Current Biology, 11 (12): 941-50
The ins and outs of group II introns
Bonen L, Vogel J (2001)
Trends In Genetics, 17 (6): 322-31