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Title: A transcriptomic analysis of Yersinia enterocolitica biovar 1B infecting murine macrophages reveals new mechanisms of intracellular survival

Journal Article · · Infection and Immunity
DOI:https://doi.org/10.1128/IAI.02922-14· OSTI ID:1235333

Yersinia enterocolitica is typically considered an extracellular pathogen; however, during the course of an infection, a significant number of bacteria are stably maintained within host cell vacuoles. Little is known about this population and the role it plays during an infection. To address this question and to elucidate the spatially and temporally dynamic gene expression patterns of Y. enterocoliticabiovar 1B through the course of an in vitro infection, transcriptome sequencing and differential gene expression analysis of bacteria infecting murine macrophage cells were performed under four distinct conditions. Bacteria were first grown in a nutrient-rich medium at 26°C to establish a baseline of gene expression that is unrelated to infection. The transcriptomes of these bacteria were then compared to bacteria grown in a conditioned cell culture medium at 37°C to identify genes that were differentially expressed in response to the increased temperature and medium but not in response to host cells. Infections were then performed, and the transcriptomes of bacteria found on the extracellular surface and intracellular compartments were analyzed individually. The upregulated genes revealed potential roles for a variety of systems in promoting intracellular virulence, including the Ysa type III secretion system, the Yts2 type II secretion system, and the Tad pilus. It was further determined that mutants of each of these systems had decreased virulence while infecting macrophages. Overall, these results reveal the complete set of genes expressed by Y. enterocolitica in response to infection and provide the groundwork for future virulence studies.

Research Organization:
Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Sponsoring Organization:
USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
AC04-94AL85000
OSTI ID:
1235333
Report Number(s):
SAND-2014-3732J; 516866
Journal Information:
Infection and Immunity, Vol. 83, Issue 7; ISSN ‎0019-9567
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 12 works
Citation information provided by
Web of Science

References (68)

In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted journal August 2006
RNA sequencing: advances, challenges and opportunities journal December 2010
Comparative Genome Analyses of the Pathogenic Yersiniae Based on the Genome Sequence of Yersinia enterocolitica Strain 8081 book January 2007
The Yersinia Ysc–Yop 'Type III' weaponry journal October 2002
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation journal May 2010
Na + /H + Antiport Is Essential for Yersinia pestis Virulence journal June 2013
Yersiniosis journal January 1990
Curli Biogenesis and Function journal October 2006
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions journal January 2013
Peregrine: A rapid and unbiased method to produce strand-specific RNA-Seq libraries from small quantities of starting material journal April 2013
Population-Based Incidence of Infection With Selected Bacterial Enteric Pathogens in Children Younger Than Five Years of Age, 1996???1998 journal January 2006
A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. journal June 1988
The Myf fibrillae of Yersinia enterocolitica journal August 1993
The tad locus: postcards from the widespread colonization island journal May 2007
The sugar-specific outer membrane channel ScrY contains functional characteristics of general diffusion pores and substrate-specific porins journal September 1991
Yersinia Entry into Host Cells Requires Rab5-Dependent Dephosphorylation of PI(4,5)P2 and Membrane Scission journal February 2012
Global Gene Expression Profiling of Yersinia pestis Replicating inside Macrophages Reveals the Roles of a Putative Stress-Induced Operon in Regulating Type III Secretion and Intracellular Cell Division journal June 2010
Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake journal February 2006
Strategies used by Yersinia enterocolitica to evade killing by the host: thinking beyond Yops journal February 2014
Yersinia Enterocolitica journal July 1989
Glycogen and Maltose Utilization by Escherichia coli O157:H7 in the Mouse Intestine journal March 2008
Morphological, cytochemical, functional, and proliferative characteristics of four murine macrophage-like cell lines journal February 1985
Proteomic analysis of iron acquisition, metabolic and regulatory responses of Yersinia pestis to iron starvation journal January 2010
Identification of novel chromosomal loci affecting Yersinia enterocolitica pathogenesis journal July 1997
Translocated effectors of Yersinia journal February 2009
Transcriptional regulation of the Yts1 type II secretion system of Yersinia enterocolitica and identification of secretion substrates: T2SS of Y. enterocolitica journal December 2009
populacDNA normalization by hydroxyapatite chromatography to enrich transcriptome diversity in RNA-seq applications journal December 2012
The bacterial injection kit: Type III secretion systems journal June 2005
Concerted Actions of a Thermo-labile Regulator and a Unique Intergenic RNA Thermosensor Control Yersinia Virulence journal February 2012
An Infection-Relevant Transcriptomic Compendium for Salmonella enterica Serovar Typhimurium journal December 2013
Dual RNA-seq of pathogen and host journal August 2012
Yersinia enterocolitica YadA Mediates Complement Evasion by Recruitment and Inactivation of C3 Products journal October 2012
Bacterial Injectisomes: Needle Length Does Matter journal February 2005
Type II secretion in Yersinia—a secretion system for pathogenicity and environmental fitness journal January 2012
Hierarchy of Iron Uptake Systems: Yfu and Yiu Are Functional in Yersinia pestis journal September 2006
Use of a Capture-Based Pathogen Transcript Enrichment Strategy for RNA-Seq Analysis of the Francisella Tularensis LVS Transcriptome during Infection of Murine Macrophages journal October 2013
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. journal January 1989
Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica. journal January 1996
RNA-Seq: a revolutionary tool for transcriptomics journal January 2009
The Complete Campylobacter jejuni Transcriptome during Colonization of a Natural Host Determined by RNAseq journal August 2013
The Yersinia enterocolitica Ysa type III secretion system is expressed during infections both in vitro and in vivo journal October 2013
Transcriptional Activation of the tad Type IVb Pilus Operon by PypB in Yersinia enterocolitica journal May 2010
The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia enterocolitica Strain 8081 journal January 2006
A Phenotype at Last: Essential Role for the Yersinia enterocolitica Ysa Type III Secretion System in a Drosophila melanogaster S2 Cell Model journal April 2013
Common and Specific Characteristics of the High-Pathogenicity Island of Yersinia enterocolitica journal October 1999
Amplification of cDNA ends based on template-switching effect and step- out PCR journal March 1999
A Rationale for Repression and/or Loss of Motility by Pathogenic Yersinia in the Mammalian Host book January 2007
Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae journal March 2005
Three Yersinia pestis Adhesins Facilitate Yop Delivery to Eukaryotic Cells and Contribute to Plague Virulence journal August 2010
Temperature sensing in Yersinia pestis: regulation of yopE transcription by lcrF. journal January 1992
Assembly of the Yersinia injectisome: the missing pieces: Assembly of the Yersinia injectisome journal July 2012
Neglected but amazingly diverse type IVb pili journal November 2012
Enriching pathogen transcripts from infected samples: A capture-based approach to enhanced host–pathogen RNA sequencing journal July 2013
YplA Is Exported by the Ysc, Ysa, and Flagellar Type III Secretion Systems of Yersinia enterocolitica journal March 2002
A Regulatory Network Controls Expression of the In Vivo-Expressed HreP Protease of Yersinia enterocolitica journal December 2008
Modulation of innate immune responses by Yersinia type III secretion system translocators and effectors: Immune modulation by Yersinia translocon and effectors journal July 2013
YAPI, a New Yersinia pseudotuberculosis Pathogenicity Island journal July 2004
Salmonella T3SSs: successful mission of the secret(ion) agents journal February 2013
Characterization of the ysa Pathogenicity Locus in the Chromosome of Yersinia enterocolitica and Phylogeny Analysis of Type III Secretion Systems journal July 2002
The Sequence Alignment/Map format and SAMtools journal June 2009
β 1 Integrin-Dependent Engulfment of Yersinia enterocolitica by Macrophages Is Coupled to the Activation of Autophagy and Suppressed by Type III Protein Secretion journal October 2009
Transcriptome analysis of Vibrio parahaemolyticus in type III secretion system 1 inducing conditions journal January 2014
Characteristics of virulence in human isolates of Yersinia enterocolitica. journal January 1981
A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence: Yersinia enterocolitica chromosomal type III secretion journal June 2000
The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence: RhoGAP activity of Yersinia YopE journal August 2000
Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. journal January 1981
The Yersinia Ysc-Yop virulence apparatus journal January 2001

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