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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

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

2021

Cross-species RNA-seq for deciphering host–microbe interactions

Westermann AJ, Vogel J (2021)

Nature Reviews Genetics (Online ahead of print)

Opposing Wnt signals regulate cervical squamocolumnar homeostasis and emergence of metaplasia

Chumduri C, Gurumurthy RK, Berger H, Dietrich O, Kumar N, Koster S, Brinkmann V, Hoffmann K, Drabkina M, Arampatzi P, …, Saliba A, Meyer TF (2021)

Nature Cell Biology 23 (2): 184

A Grad-seq View of RNA and Protein Complexes in Pseudomonas aeruginosa under Standard and Bacteriophage Predation Conditions

Gerovac M, Wicke L, Chihara K, Schneider C, Lavigne R, Vogel J (2021)

mBio 12 (1): 03454-20

MAPS integrates regulation of actin-targeting effector SteC into the virulence control network of Salmonella small RNA PinT

Correia Santos S, Bischler T, Westermann AJ, Vogel J (2021)

Cell Reports 34 (5): 10872

A genome-wide transcriptomic analysis of embryos fathered by obese males in a murine model of diet-induced obesity

Bernhardt L, Dittrich M, El-Merahbi R, Saliba A, Müller T, Sumara G, Vogel J, Nichols-Burns S, Mitchell M, Haaf T, El Hajj N (2021)

Scientific Reports 11: 1979

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

Severe COVID-19 is marked by a dysregulated myeloid cell compartment

Schulte-Schrepping J, Reusch N, Paclik D, Baßler K, Schlickeiser S, Zhang B, Krämer B, Krammer T, Brumhard S, Bonaguro L, …, Saliba AE, Sander LE (2020)

Cell 182 (6): 1419-1440

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

An RNA biology perspective on species-specific programmable RNA antibiotics

Vogel J (2020)

Molecular Microbiology 113 (3): 550-559

A global data-driven census of Salmonella small proteins and their potential functions in bacterial virulence

Venturini E, Svensson SL, Maaß S, Gelhausen R, Eggenhofer F, Li L, Cain AK, Parkhill J, Becher D, Backofen R, …, Westermann AJ, Vogel J (2020)

microLife 1 (1): 597

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 6 (3): 339-353

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 (Online ahead of print)

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): 619

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 (8): 1069-1078

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

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

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 in Molecular Biology 1737: 59-75

2017

Global snapshots of bacterial RNA networks

Hör J, Vogel J (2017)

The EMBO Journal 36 (3): 245-247

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

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

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

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

2015

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

A bacterial seek-and-destroy system for foreign DNA

Vogel J (2014)

Science 344 (6187): 972-3

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

A small RNA serving both the Hfq and CsrA regulons

Holmqvist E, Vogel J (2013)

Genes & Development 27 (10): 1073-8

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 Polymerase

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

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

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

Noncoding RNAs encoded by bacterial chromosomes

Wagner EG, Vogel J (2003)

In: Noncoding RNAs (eds Barciszewski J, Erdmann V): 243-259

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