Use of a Capture-Based Pathogen Transcript Enrichment Strategy for RNA-Seq Analysis of the Francisella Tularensis LVS Transcriptome during Infection of Murine Macrophages

Bent, Zachary W.; Brazel, David M.; Tran-Gyamfi, Mary B.; Hamblin, Rachelle Y.; VanderNoot, Victoria A.; Branda, Steven S.

doi:10.1371/journal.pone.0077834

Title: 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 Article · Mon Oct 14 00:00:00 EDT 2013 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0077834· OSTI ID:1627647

Bent, Zachary W. ^[1]; Brazel, David M. ^[1]; Tran-Gyamfi, Mary B. ^[1]; Hamblin, Rachelle Y. ^[1]; VanderNoot, Victoria A. ^[1]; Branda, Steven S. ^[1]

Sandia National Lab. (SNL-CA), Livermore, CA (United States)

Francisella tularensis is a zoonotic intracellular pathogen that is capable of causing potentially fatal human infections. Like all successful bacterial pathogens, F. tularensis rapidly responds to changes in its environment during infection of host cells, and upon encountering different microenvironments within those cells. This ability to appropriately respond to the challenges of infection requires rapid and global shifts in gene expression patterns. In this study, we use a novel pathogen transcript enrichment strategy and whole transcriptome sequencing (RNA-Seq) to perform a detailed characterization of the rapid and global shifts in F. tularensis LVS gene expression during infection of murine macrophages. We performed differential gene expression analysis on all bacterial genes at two key stages of infection: phagosomal escape, and cytosolic replication. By comparing the F. tularensis transcriptome at these two stages of infection to that of the bacteria grown in culture, we were able to identify sets of genes that are differentially expressed over the course of infection. This analysis revealed the temporally dynamic expression of a number of known and putative transcriptional regulators and virulence factors, providing insight into their role during infection. In addition, we identified several F. tularensis genes that are significantly up-regulated during infection but had not been previously identified as virulence factors. These unknown genes may make attractive therapeutic or vaccine targets.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1627647

Journal Information:: PLoS ONE, Vol. 8, Issue 10; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

The ecology of tularaemia: -EN- -FR- -ES- Morner, T. Revue Scientifique et Technique de l'OIE, Vol. 11, Issue 4 https://doi.org/10.20506/rst.11.4.657	journal	December 1992
Francisella tularensis: Taxonomy, Genetics, and Immunopathogenesis of a Potential Agent of Biowarfare McLendon, Molly K.; Apicella, Michael A.; Allen, Lee-Ann H. Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142126	journal	October 2006
Tularaemia: bioterrorism defence renews interest in Francisella tularensis Oyston, Petra C. F.; Sjöstedt, Anders; Titball, Richard W. Nature Reviews Microbiology, Vol. 2, Issue 12 https://doi.org/10.1038/nrmicro1045	journal	December 2004
Tularemia as a Biological Weapon: Medical and Public Health Management Dennis, David T.; Inglesby, Thomas V.; Henderson, Donald A. JAMA, Vol. 285, Issue 21 https://doi.org/10.1001/jama.285.21.2763	journal	June 2001
Public Health Assessment of Potential Biological Terrorism Agents Rotz, Lisa D. Emerging Infectious Diseases, Vol. 8, Issue 2 https://doi.org/10.3201/eid0802.010164	journal	February 2002
Francisella tularensis: unravelling the secrets of an intracellular pathogen Oyston, P. C. F. Journal of Medical Microbiology, Vol. 57, Issue 8 https://doi.org/10.1099/jmm.0.2008/000653-0	journal	August 2008
Generation of a Convalescent Model of Virulent Francisella tularensis Infection for Assessment of Host Requirements for Survival of Tularemia Crane, Deborah D.; Scott, Dana P.; Bosio, Catharine M. PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033349	journal	March 2012
Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication Checroun, C.; Wehrly, T. D.; Fischer, E. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 39 https://doi.org/10.1073/pnas.0601838103	journal	September 2006
Life on the inside: the intracellular lifestyle of cytosolic bacteria Ray, Katrina; Marteyn, Benoit; Sansonetti, Philippe J. Nature Reviews Microbiology, Vol. 7, Issue 5 https://doi.org/10.1038/nrmicro2112	journal	May 2009
Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages Wehrly, Tara D.; Chong, Audrey; Virtaneva, Kimmo Cellular Microbiology, Vol. 11, Issue 7 https://doi.org/10.1111/j.1462-5822.2009.01316.x	journal	July 2009
Francisella tularensis subsp. tularensis Induces a Unique Pulmonary Inflammatory Response: Role of Bacterial Gene Expression in Temporal Regulation of Host Defense Responses Walters, Kathie-Anne; Olsufka, Rachael; Kuestner, Rolf E. PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0062412	journal	May 2013
Enriching pathogen transcripts from infected samples: A capture-based approach to enhanced host–pathogen RNA sequencing Bent, Zachary W.; Tran-Gyamfi, Mary B.; Langevin, Stanley A. Analytical Biochemistry, Vol. 438, Issue 1, p. 90-96 https://doi.org/10.1016/j.ab.2013.03.008	journal	July 2013
Virulent and Avirulent Strains of Francisella tularensis Prevent Acidification and Maturation of Their Phagosomes and Escape into the Cytoplasm in Human Macrophages Clemens, Daniel L.; Lee, Bai-Yu; Horwitz, Marcus A. Infection and Immunity, Vol. 72, Issue 6 https://doi.org/10.1128/IAI.72.6.3204-3217.2004	journal	June 2004
An Attenuated Strain of the Facultative Intracellular Bacterium Francisella tularensis Can Escape the Phagosome of Monocytic Cells Golovliov, I.; Baranov, V.; Krocova, Z. Infection and Immunity, Vol. 71, Issue 10 https://doi.org/10.1128/IAI.71.10.5940-5950.2003	journal	September 2003
Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape McCaffrey, Ramona L.; Allen, Lee-Ann H. Journal of Leukocyte Biology, Vol. 80, Issue 6 https://doi.org/10.1189/jlb.0406287	journal	August 2006
Modulation of biogenesis of the Francisella tularensis subsp. novicida-containing phagosome in quiescent human macrophages and its maturation into a phagolysosome upon activation by IFN-γ: Biogenesis of the Francisella-containing phagosome Santic, Marina; Molmeret, Maelle; Abu Kwaik, Yousef Cellular Microbiology, Vol. 7, Issue 7 https://doi.org/10.1111/j.1462-5822.2005.00529.x	journal	June 2005
The Early Phagosomal Stage of Francisella tularensis Determines Optimal Phagosomal Escape and Francisella Pathogenicity Island Protein Expression Chong, Audrey; Wehrly, Tara D.; Nair, Vinod Infection and Immunity, Vol. 76, Issue 12 https://doi.org/10.1128/IAI.00682-08	journal	October 2008
Factors affecting the escape of Francisella tularensis from the phagolysosome Lindgren, Helena; Golovliov, Igor; Baranov, Vladimir Journal of Medical Microbiology, Vol. 53, Issue 10 https://doi.org/10.1099/jmm.0.45685-0	journal	October 2004
A new cell assay to determine the virulence of Francisella tularensis Mack, K.; Fulop, M.; Manchee, R. J. Letters in Applied Microbiology, Vol. 19, Issue 3 https://doi.org/10.1111/j.1472-765X.1994.tb00931.x	journal	September 1994
The Role of the Francisella Tularensis Pathogenicity Island in Type VI Secretion, Intracellular Survival, and Modulation of Host Cell Signaling Bröms, Jeanette E.; Sjöstedt, Anders; Lavander, Moa Frontiers in Microbiology, Vol. 1 https://doi.org/10.3389/fmicb.2010.00136	journal	January 2010
Small Molecule Control of Virulence Gene Expression in Francisella tularensis Charity, James C.; Blalock, LeeAnn T.; Costante-Hamm, Michelle M. PLoS Pathogens, Vol. 5, Issue 10 https://doi.org/10.1371/journal.ppat.1000641	journal	October 2009
Twin RNA Polymerase–Associated Proteins Control Virulence Gene Expression in Francisella tularensis Charity, James C.; Costante-Hamm, Michelle M.; Balon, Emmy L. PLoS Pathogens, Vol. 3, Issue 6 https://doi.org/10.1371/journal.ppat.0030084	journal	June 2007
Pivotal role of the Francisella tularensis heat-shock sigma factor RpoH Grall, Nathalie; Livny, Jonathan; Waldor, Matthew Microbiology, Vol. 155, Issue 8 https://doi.org/10.1099/mic.0.029058-0	journal	August 2009
Generation and Characterization of an Attenuated Mutant in a Response Regulator Gene of Francisella tularensis Live Vaccine Strain (LVS) Sammons-Jackson, Wendy L.; McClelland, Karen; Manch-Citron, Jean N. DNA and Cell Biology, Vol. 27, Issue 7 https://doi.org/10.1089/dna.2007.0687	journal	July 2008
Identification of fevR, a Novel Regulator of Virulence Gene Expression in Francisella novicida Brotcke, Anna; Monack, Denise M. Infection and Immunity, Vol. 76, Issue 8 https://doi.org/10.1128/IAI.00430-08	journal	June 2008
Identification of migR, a Regulatory Element of the Francisella tularensis Live Vaccine Strain iglABCD Virulence Operon Required for Normal Replication and Trafficking in Macrophages Buchan, Blake W.; McCaffrey, Ramona L.; Lindemann, Stephen R. Infection and Immunity, Vol. 77, Issue 6 https://doi.org/10.1128/IAI.00229-09	journal	April 2009
IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins : Positive regulation of the Yeo, Won-Sik; Lee, Joon-Hee; Lee, Kyung-Chang Molecular Microbiology, Vol. 61, Issue 1 https://doi.org/10.1111/j.1365-2958.2006.05220.x	journal	May 2006
Oxidant-Responsive Induction of the suf Operon, Encoding a Fe-S Assembly System, through Fur and IscR in Escherichia coli Lee, K. -C.; Yeo, W. -S.; Roe, J. -H. Journal of Bacteriology, Vol. 190, Issue 24 https://doi.org/10.1128/JB.01161-08	journal	October 2008
Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria Chiang, Sarah M.; Schellhorn, Herb E. Archives of Biochemistry and Biophysics, Vol. 525, Issue 2, p. 161-169 https://doi.org/10.1016/j.abb.2012.02.007	journal	September 2012
Reciprocal Analysis of Francisella novicida Infections of a Drosophila melanogaster Model Reveal Host-Pathogen Conflicts Mediated by Reactive Oxygen and imd-Regulated Innate Immune Response Moule, Madeleine G.; Monack, Denise M.; Schneider, David S. PLoS Pathogens, Vol. 6, Issue 8 https://doi.org/10.1371/journal.ppat.1001065	journal	August 2010
Characterization of fig operon mutants of Francisella novicida U112 Kiss, Katalin; Liu, Wei; Huntley, Jason F. FEMS Microbiology Letters, Vol. 285, Issue 2 https://doi.org/10.1111/j.1574-6968.2008.01237.x	journal	August 2008
Cyclic Di-GMP Stimulates Biofilm Formation and Inhibits Virulence of Francisella novicida Zogaj, Xhavit; Wyatt, Geoff C.; Klose, Karl E. Infection and Immunity, Vol. 80, Issue 12 https://doi.org/10.1128/IAI.00702-12	journal	September 2012
The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth de Bruin, Olle M.; Ludu, Jagjit S.; Nano, Francis E. BMC Microbiology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2180-7-1	journal	January 2007
The Francisella Pathogenicity Island Nano, F. E.; Schmerk, C. Annals of the New York Academy of Sciences, Vol. 1105, Issue 1 https://doi.org/10.1196/annals.1409.000	journal	March 2007
A Francisella tularensis Pathogenicity Island Required for Intramacrophage Growth Nano, F. E.; Zhang, N.; Cowley, S. C. Journal of Bacteriology, Vol. 186, Issue 19 https://doi.org/10.1128/JB.186.19.6430-6436.2004	journal	September 2004
Identification of MglA-Regulated Genes Reveals Novel Virulence Factors in Francisella tularensis Brotcke, Anna; Weiss, David S.; Kim, Charles C. Infection and Immunity, Vol. 74, Issue 12 https://doi.org/10.1128/IAI.01250-06	journal	September 2006
Glutathione Provides a Source of Cysteine Essential for Intracellular Multiplication of Francisella tularensis Alkhuder, Khaled; Meibom, Karin L.; Dubail, Iharilalao PLoS Pathogens, Vol. 5, Issue 1 https://doi.org/10.1371/journal.ppat.1000284	journal	January 2009
The identification of five genetic loci of Francisella novicida associated with intracellular growth Gray, Catherine G.; Cowley, SiobhÃ¡n C.; Cheung, Karen K. M. FEMS Microbiology Letters, Vol. 215, Issue 1 https://doi.org/10.1111/j.1574-6968.2002.tb11369.x	journal	September 2002
Identification of transposon insertion mutants of Francisella tularensis tularensis strain Schu S4 deficient in intracellular replication in the hepatic cell line HepG2 Qin, Aiping; Mann, Barbara J. BMC Microbiology, Vol. 6, Issue 1, p. 69 https://doi.org/10.1186/1471-2180-6-69	journal	January 2006
Francisella tularensis Genes Required for Inhibition of the Neutrophil Respiratory Burst and Intramacrophage Growth Identified by Random Transposon Mutagenesis of Strain LVS Schulert, Grant S.; McCaffrey, Ramona L.; Buchan, Blake W. Infection and Immunity, Vol. 77, Issue 4 https://doi.org/10.1128/IAI.01318-08	journal	February 2009
In vivo negative selection screen identifies genes required for Francisella virulence Weiss, D. S.; Brotcke, A.; Henry, T. Proceedings of the National Academy of Sciences, Vol. 104, Issue 14 https://doi.org/10.1073/pnas.0609675104	journal	March 2007
A Francisella tularensis SCHU S4 mutant deficient in γ-glutamyltransferase activity induces protective immunity: characterization of an attenuated vaccine candidate Ireland, Philip M.; LeButt, Helen; Thomas, Rebecca M. Microbiology, Vol. 157, Issue 11 https://doi.org/10.1099/mic.0.052902-0	journal	November 2011
A Francisella tularensis Schu S4 Purine Auxotroph Is Highly Attenuated in Mice but Offers Limited Protection against Homologous Intranasal Challenge Pechous, Roger D.; McCarthy, Travis R.; Mohapatra, Nrusingh P. PLoS ONE, Vol. 3, Issue 6 https://doi.org/10.1371/journal.pone.0002487	journal	June 2008
Construction and Characterization of an Attenuated Purine Auxotroph in a Francisella tularensis Live Vaccine Strain Pechous, Roger; Celli, Jean; Penoske, Renee Infection and Immunity, Vol. 74, Issue 8 https://doi.org/10.1128/IAI.00666-06	journal	August 2006
Dual RNA-seq of pathogen and host Westermann, Alexander J.; Gorski, Stanislaw A.; Vogel, Jörg Nature Reviews Microbiology, Vol. 10, Issue 9 https://doi.org/10.1038/nrmicro2852	journal	August 2012
Peregrine: A rapid and unbiased method to produce strand-specific RNA-Seq libraries from small quantities of starting material Langevin, Stanley A.; Bent, Zachary W.; Solberg, Owen D. RNA Biology, Vol. 10, Issue 4 https://doi.org/10.4161/rna.24284	journal	April 2013
Regulation of Virulence Gene Transcripts by the Francisella novicida Orphan Response Regulator PmrA: Role of Phosphorylation and Evidence of MglA/SspA Interaction Bell, Brian L.; Mohapatra, Nrusingh P.; Gunn, John S. Infection and Immunity, Vol. 78, Issue 5 https://doi.org/10.1128/IAI.00021-10	journal	March 2010
Environmental and intracellular regulation of Francisella tularensis ripA Fuller, James R.; Kijek, Todd M.; Taft-Benz, Sharon BMC Microbiology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2180-9-216	journal	January 2009
Transcription factor distribution in Escherichia coli : studies with FNR protein Grainger, David C.; Aiba, Hirofumi; Hurd, Douglas Nucleic Acids Research, Vol. 35, Issue 1 https://doi.org/10.1093/nar/gkl1023	journal	December 2006
populacDNA normalization by hydroxyapatite chromatography to enrich transcriptome diversity in RNA-seq applications VanderNoot, Victoria A.; Langevin, Stanley A.; Solberg, Owen D. BioTechniques, Vol. 53, Issue 6 https://doi.org/10.2144/000113937	journal	December 2012
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
Salinity tolerance mechanisms of an Arctic Pelagophyte using comparative transcriptomic and gene expression analysis Freyria, Nastasia J.; Kuo, Alan; Chovatia, Mansi Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03461-2	journal	May 2022
REBASE--enzymes and genes for DNA restriction and modification Roberts, R. J.; Vincze, T.; Posfai, J. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl891	journal	January 2007
Tularemia Ellis, Jill; Oyston, Petra C. F.; Green, Michael Clinical Microbiology Reviews, Vol. 15, Issue 4 https://doi.org/10.1128/cmr.15.4.631-646.2002	journal	October 2002
The Francisella tularensis migR, trmE , and cphA Genes Contribute to F. tularensis Pathogenicity Island Gene Regulation and Intracellular Growth by Modulation of the Stress Alarmone ppGpp Faron, Matthew; Fletcher, Joshua R.; Rasmussen, Jed A. Infection and Immunity, Vol. 81, Issue 8 https://doi.org/10.1128/iai.00073-13	journal	May 2013
MglA and Igl Proteins Contribute to the Modulation of Francisella tularensis Live Vaccine Strain-Containing Phagosomes in Murine Macrophages Bönquist, Linda; Lindgren, Helena; Golovliov, Igor Infection and Immunity, Vol. 76, Issue 8 https://doi.org/10.1128/iai.00226-08	journal	May 2008
Identification of Francisella tularensis Himar1-Based Transposon Mutants Defective for Replication in Macrophages Maier, Tamara M.; Casey, Monika S.; Becker, Rachel H. Infection and Immunity, Vol. 75, Issue 11 https://doi.org/10.1128/iai.00238-07	journal	August 2007
Identification of an Orphan Response Regulator Required for the Virulence of Francisella spp. and Transcription of Pathogenicity Island Genes Mohapatra, Nrusingh P.; Soni, Shilpa; Bell, Brian L. Infection and Immunity, Vol. 75, Issue 7 https://doi.org/10.1128/iai.00351-07	journal	April 2007
Effects of the Putative Transcriptional Regulator IclR on Francisella tularensis Pathogenesis Mortensen, Brittany L.; Fuller, James R.; Taft-Benz, Sharon Infection and Immunity, Vol. 78, Issue 12 https://doi.org/10.1128/iai.00544-10	journal	October 2010
Attenuated Francisella novicida Transposon Mutants Protect Mice against Wild-Type Challenge Tempel, Rebecca; Lai, Xin-He; Crosa, Lidia Infection and Immunity, Vol. 74, Issue 9 https://doi.org/10.1128/iai.00598-06	journal	September 2006
Genome-Wide Screen in Francisella novicida for Genes Required for Pulmonary and Systemic Infection in Mice Kraemer, Petra S.; Mitchell, Allison; Pelletier, Mark R. Infection and Immunity, Vol. 77, Issue 1 https://doi.org/10.1128/iai.00978-08	journal	October 2008
Genome-Wide Identification of Francisella tularensis Virulence Determinants Su, J.; Yang, J.; Zhao, D. Infection and Immunity, Vol. 75, Issue 6 https://doi.org/10.1128/iai.01865-06	journal	April 2007
Identification of Francisella tularensis Genes Affected by Iron Limitation Deng, Kaiping; Blick, Robert J.; Liu, Wei Infection and Immunity, Vol. 74, Issue 7 https://doi.org/10.1128/iai.01975-05	journal	July 2006
Discovery of a Role for Hsp82 in Histoplasma Virulence through a Quantitative Screen for Macrophage Lethality Edwards, Jessica A.; Zemska, Olga; Rappleye, Chad A. Infection and Immunity, Vol. 79, Issue 8 https://doi.org/10.1128/iai.05124-11	journal	May 2011
Live vaccine strain of Francisella tularensis: infection and immunity in mice. Fortier, A. H.; Slayter, M. V.; Ziemba, R. Infection and Immunity, Vol. 59, Issue 9 https://doi.org/10.1128/iai.59.9.2922-2928.1991	journal	January 1991
Characterization of the Siderophore of Francisella tularensis and Role of fslA in Siderophore Production Sullivan, Jonathan Tabb; Jeffery, Erin Field; Shannon, John D. Journal of Bacteriology, Vol. 188, Issue 11 https://doi.org/10.1128/jb.00027-06	journal	June 2006
Regulation of Francisella Tularensis Virulence Dai, Shipan; Mohapatra, Nrusingh P.; Schlesinger, Larry S. Frontiers in Microbiology, Vol. 1 https://doi.org/10.3389/fmicb.2010.00144	journal	January 2011
An Improved Filtering Algorithm for Big Read Datasets Wedemeyer, Axel; Kliemann, Lasse; Srivastav, Anand arXiv https://doi.org/10.48550/arxiv.1610.03443	preprint	January 2016

Cited By (3)

Differential Growth of Francisella tularensis, Which Alters Expression of Virulence Factors, Dominant Antigens, and Surface-Carbohydrate Synthases, Governs the Apparent Virulence of Ft SchuS4 to Immunized Animals Holland, Kristen M.; Rosa, Sarah J.; Kristjansdottir, Kolbrun Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01158	journal	June 2017
Differential Growth of Francisella tularensis, Which Alters Expression of Virulence Factors, Dominant Antigens, and Surface-Carbohydrate Synthases, Governs the Apparent Virulence of Ft SchuS4 to Immunized Animals R. O., Hazlett, Karsten; M., Holland, Kristen; J., Franz, Brian The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/948f-w826	text	January 2017
Validation of a novel Mho microarray for a comprehensive characterisation of the Mycoplasma hominis action in HeLa cell infection Henrich, Birgit; Kretzmer, Freya; Deenen, René PLOS ONE, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pone.0181383	journal	July 2017

Similar Records

Dissection of the molecular circuitry controlling virulence in Francisella tularensis

Journal Article · Fri Sep 01 00:00:00 EDT 2017 · Genes & Development · OSTI ID:1627647

Cuthbert, Bonnie J.; Ross, Wilma; Rohlfing, Amy E.; +4 more

Francisella tularensis type A Strains Cause the Rapid Encystment of Acanthamoeba castellanii and Survive in Amoebal Cysts for Three Weeks post Infection

Journal Article · Tue Jul 28 00:00:00 EDT 2009 · Applied Environmental Microbiology, vol. 75, no. 23, December 15, 2009, pp. 5488 · OSTI ID:1627647

El-Etr, S H; Margolis, J; Monack, D; +4 more

Models Derived from In Vitro Analyses of Spleen, Liver, and Lung Leukocyte Functions Predict Vaccine Efficacy against the Francisella tularensis Live Vaccine Strain (LVS)

Journal Article · Tue Feb 25 00:00:00 EST 2014 · mBio (Online) · OSTI ID:1627647

De Pascalis, Roberto; Chou, Alicia Y.; Ryden, Patrik; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics

Title: Use of a Capture-Based Pathogen Transcript Enrichment Strategy for RNA-Seq Analysis of the Francisella Tularensis LVS Transcriptome during Infection of Murine Macrophages

Citation Formats

References (73)

Cited By (3)

Similar Records

Related Subjects