Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice
Abstract
Francisella tularensis is a Gram-negative bacterium and the etiologic agent of tularemia. F. tularensis may appear encapsulated when examined by transmission electron microscopy (TEM), which is due to production of an extracellular capsule-like complex (CLC) when the bacterium is grown under specific environmental conditions. Deletion of two glycosylation genes in the live vaccine strain (LVS) results in loss of apparent CLC and attenuation of LVS in mice. In contrast, F. novicida, which is also highly virulent for mice, is reported to be non-encapsulated. But, the F. novicida genome contains a putative polysaccharide locus with homology to the CLC glycosylation locus in F. tularensis. Following daily subculture of F. novicida in Chamberlain’s defined medium, an electron dense material surrounding F. novicida, similar to the F. tularensis CLC, was evident. Extraction with urea effectively removed the CLC, and compositional analysis indicated the extract contained galactose, glucose, mannose, and multiple proteins, similar to those found in the F. tularensis CLC. The same glycosylation genes deleted in LVS were targeted for deletion in F. novicida by allelic exchange using the same mutagenesis vector used for mutagenesis of LVS. In contrast, this mutation also resulted in the loss of five additional genes immediately upstream ofmore »
- Authors:
-
- Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Center for Molecular Medicine and Infectous Diseases, Dept. of Biomedical Sciences and Pathobiology
- Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Center for Molecular Medicine and Infectous Diseases, Dept. of Biomedical Sciences and Pathobiology; Virginia Technical Carilion School of Medicine, Roanoke, VA (United States). Dept. of Biomedical Sciences
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1389272
- Grant/Contract Number:
- FG02-93ER20097
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Francisella novicida; capsule-like complex; virulence in mice; tularemia; glycosylation; protective immunity
Citation Formats
Freudenberger Catanzaro, Kelly C., Champion, Anna E., Mohapatra, Nrusingh, Cecere, Thomas, and Inzana, Thomas J. Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice. United States: N. p., 2017.
Web. doi:10.3389/fmicb.2017.00935.
Freudenberger Catanzaro, Kelly C., Champion, Anna E., Mohapatra, Nrusingh, Cecere, Thomas, & Inzana, Thomas J. Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice. United States. https://doi.org/10.3389/fmicb.2017.00935
Freudenberger Catanzaro, Kelly C., Champion, Anna E., Mohapatra, Nrusingh, Cecere, Thomas, and Inzana, Thomas J. Tue .
"Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice". United States. https://doi.org/10.3389/fmicb.2017.00935. https://www.osti.gov/servlets/purl/1389272.
@article{osti_1389272,
title = {Glycosylation of a Capsule-Like Complex (CLC) by Francisella novicida Is Required for Virulence and Partial Protective Immunity in Mice},
author = {Freudenberger Catanzaro, Kelly C. and Champion, Anna E. and Mohapatra, Nrusingh and Cecere, Thomas and Inzana, Thomas J.},
abstractNote = {Francisella tularensis is a Gram-negative bacterium and the etiologic agent of tularemia. F. tularensis may appear encapsulated when examined by transmission electron microscopy (TEM), which is due to production of an extracellular capsule-like complex (CLC) when the bacterium is grown under specific environmental conditions. Deletion of two glycosylation genes in the live vaccine strain (LVS) results in loss of apparent CLC and attenuation of LVS in mice. In contrast, F. novicida, which is also highly virulent for mice, is reported to be non-encapsulated. But, the F. novicida genome contains a putative polysaccharide locus with homology to the CLC glycosylation locus in F. tularensis. Following daily subculture of F. novicida in Chamberlain’s defined medium, an electron dense material surrounding F. novicida, similar to the F. tularensis CLC, was evident. Extraction with urea effectively removed the CLC, and compositional analysis indicated the extract contained galactose, glucose, mannose, and multiple proteins, similar to those found in the F. tularensis CLC. The same glycosylation genes deleted in LVS were targeted for deletion in F. novicida by allelic exchange using the same mutagenesis vector used for mutagenesis of LVS. In contrast, this mutation also resulted in the loss of five additional genes immediately upstream of the targeted mutation (all within the glycosylation locus), resulting in strain F. novicida Δ11212–1218. The subcultured mutant F. novicida Δ11212–1218 was CLC-deficient and the CLC contained significantly less carbohydrate than the subcultured parent strain. The mutant was severely attenuated in BALB/c mice inoculated intranasally, as determined by the lower number of F. novicida Δ11212–1218 recovered in tissues compared to the parent, and by clearance of the mutant by 10–14 days post-challenge. Mice immunized intranasally with F. novicida Δ11212–1218 were partially protected against challenge with the parent, produced significantly reduced levels of inflammatory cytokines, and their spleens contained only areas of lymphoid hyperplasia, whereas control mice challenged with the parent exhibited hypercytokinemia and splenic necrosis. Thus, F. novicida is capable of producing a CLC similar to that of F. tularensis, and glycosylation of the CLC contributed to F. novicida virulence and immunoprotection.},
doi = {10.3389/fmicb.2017.00935},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Tue May 30 00:00:00 EDT 2017},
month = {Tue May 30 00:00:00 EDT 2017}
}
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Works referenced in this record:
Molecular Immune Responses to Aerosol Challenge with Francisella tularensis in Mice Inoculated with Live Vaccine Candidates of Varying Efficacy
journal, October 2010
- Shen, Hua; Harris, Gregory; Chen, Wangxue
- PLoS ONE, Vol. 5, Issue 10
The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis: The H. influenzae HMW1 adhesin is glycosylated
journal, April 2003
- Grass, Susan; Buscher, Amy Z.; Swords, W. Edward
- Molecular Microbiology, Vol. 48, Issue 3
Isolation and Mutagenesis of a Capsule-Like Complex (CLC) from Francisella tularensis, and Contribution of the CLC to F. tularensis Virulence in Mice
journal, April 2011
- Bandara, Aloka B.; Champion, Anna E.; Wang, Xiaoshan
- PLoS ONE, Vol. 6, Issue 4
Biosynthesis and Assembly of Capsular Polysaccharides in Escherichia coli
journal, June 2006
- Whitfield, Chris
- Annual Review of Biochemistry, Vol. 75, Issue 1, p. 39-68
An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis SchuS4 strain
journal, September 2008
- Bakshi, Chandra Shekhar; Malik, Meenakshi; Mahawar, Manish
- Vaccine, Vol. 26, Issue 41
The complete genome sequence of Francisella tularensis, the causative agent of tularemia
journal, January 2005
- Larsson, Pär; Oyston, Petra C. F.; Chain, Patrick
- Nature Genetics, Vol. 37, Issue 2
Working toward the Future: Insights into Francisella tularensis Pathogenesis and Vaccine Development
journal, November 2009
- Pechous, R. D.; McCarthy, T. R.; Zahrt, T. C.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 4
Identification of Francisella tularensis outer membrane protein A (FopA) as a protective antigen for tularemia
journal, July 2011
- Hickey, Anthony J.; Hazlett, Karsten R. O.; Kirimanjeswara, Girish S.
- Vaccine
Comparative review of Francisella tularensis and Francisella novicida
journal, March 2014
- Kingry, Luke C.; Petersen, Jeannine M.
- Frontiers in Cellular and Infection Microbiology, Vol. 4
Uncovering the components of the Francisella tularensis virulence stealth strategy
journal, March 2014
- Jones, Bradley D.; Faron, Matthew; Rasmussen, Jed A.
- Frontiers in Cellular and Infection Microbiology, Vol. 4
MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival
journal, March 2004
- Lauriano, C. M.; Barker, J. R.; Yoon, S. -S.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 12
Characterization of Protein Glycosylation in Francisella tularensis subsp. holarctica: IDENTIFICATION OF A NOVEL GLYCOSYLATED LIPOPROTEIN REQUIRED FOR VIRULENCE
journal, February 2012
- Balonova, Lucie; Mann, Benjamin F.; Cerveny, Lukas
- Molecular & Cellular Proteomics, Vol. 11, Issue 7
[1] Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry
book, January 1994
- Merkle, Roberta K.; Poppe, Izabella
- Methods in Enzymology
Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS
journal, September 2007
- Li, J.; Ryder, C.; Mandal, M.
- Microbiology, Vol. 153, Issue 9
Tularemia Vaccine Study: II. Respiratory Challenge
journal, May 1961
- Saslaw, Samuel
- Archives of Internal Medicine, Vol. 107, Issue 5
Improved shuttle vectors for Francisella tularensis genetics
journal, February 2009
- LoVullo, Eric D.; Sherrill, Lani A.; Pavelka, Martin S.
- FEMS Microbiology Letters, Vol. 291, Issue 1
Multimethodological Approach to Identification of Glycoproteins from the Proteome of Francisella tularensis , an Intracellular Microorganism
journal, April 2010
- Balonova, Lucie; Hernychova, Lenka; Mann, Benjamin F.
- Journal of Proteome Research, Vol. 9, Issue 4
Immunity to Francisella
journal, January 2011
- Cowley, Siobhán C.; Elkins, Karen L.
- Frontiers in Microbiology, Vol. 2
From the Outside-In: The Francisella tularensis Envelope and Virulence
journal, December 2015
- Rowe, Hannah M.; Huntley, Jason F.
- Frontiers in Cellular and Infection Microbiology, Vol. 5
Characterization of a Wild-Type Strain of Francisella Tularensis Isolated from a Cat
journal, September 2004
- Inzana, Thomas J.; Glindemann, Gretchen E.; Snider, Gerald
- Journal of Veterinary Diagnostic Investigation, Vol. 16, Issue 5
Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (ΔiglB) induces protective immunity against homotypic and heterotypic challenge
journal, September 2009
- Cong, Yu; Yu, Jieh-Juen; Guentzel, M. Neal
- Vaccine, Vol. 27, Issue 41
The type IV pilin, PilA, is required for full virulence of Francisella tularensis subspecies tularensis
journal, January 2010
- Forslund, Anna-Lena; Naslund Salomonsson, Emelie; Golovliov, Igor
- BMC Microbiology, Vol. 10, Issue 1
Increased encapsulation and virulence of Francisella tularensis live vaccine strain (LVS) by subculturing on synthetic medium☆
journal, January 1994
- Cherwonogrodzky, J.; Knodel, M.; Spence, M.
- Vaccine, Vol. 12, Issue 9
Innate and Adaptive Immunity to Francisella
journal, March 2007
- Elkins, K. L.; Cowley, S. C.; Bosio, C. M.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Tularemia as a Biological Weapon: Medical and Public Health Management
journal, June 2001
- Dennis, David T.; Inglesby, Thomas V.; Henderson, Donald A.
- JAMA, Vol. 285, Issue 21
Identification, Characterization and Immunogenicity of an O-Antigen Capsular Polysaccharide of Francisella tularensis
journal, July 2010
- Apicella, Michael A.; Post, Deborah M. B.; Fowler, Andrew C.
- PLoS ONE, Vol. 5, Issue 7
Determination of Dextran with Anthrone
journal, November 1953
- Scott, T. A.; Melvin, E. H.
- Analytical Chemistry, Vol. 25, Issue 11
Features of sepsis caused by pulmonary infection with Francisella tularensis Type A strain
journal, July 2011
- Sharma, Jyotika; Mares, Chris A.; Li, Qun
- Microbial Pathogenesis, Vol. 51, Issue 1-2
Vaccines Against Francisella Tularensis
journal, March 2007
- Wayne Conlan, J.; Oyston, P. C. F.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis
journal, March 2006
- Forslund, Anna-Lena; Kuoppa, Kerstin; Svensson, Kerstin
- Molecular Microbiology, Vol. 59, Issue 6
Molecular Epidemiology, Evolution, and Ecology of Francisella
journal, March 2007
- Keim, P.; Johansson, A.; Wagner, D. M.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Glycosylation of DsbA in Francisella tularensis subsp. tularensis
journal, July 2011
- Thomas, R. M.; Twine, S. M.; Fulton, K. M.
- Journal of Bacteriology, Vol. 193, Issue 19
The Structure and Function of Francisella Lipopolysaccharide
journal, March 2007
- Gunn, J. S.; Ernst, R. K.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Inactivated Francisella tularensis Live Vaccine Strain Protects against Respiratory Tularemia by Intranasal Vaccination in an Immunoglobulin A-Dependent Fashion
journal, February 2007
- Baron, S. D.; Singh, R.; Metzger, D. W.
- Infection and Immunity, Vol. 75, Issue 5
Mice vaccinated with the O-antigen of Francisella tularensis LVS lipopolysaccharide conjugated to bovine serum albumin develop varying degrees of protective immunity against systemic or aerosol challenge with virulent type A and type B strains of the pathogen
journal, October 2002
- Conlan, J. Wayne; Shen, Hua; Webb, Ann
- Vaccine, Vol. 20, Issue 29-30
The role of complement opsonization in interactions between F. tularensis subsp. novicida and human neutrophils
journal, July 2009
- Barker, Jason H.; McCaffrey, Ramona L.; Baman, Nicki K.
- Microbes and Infection, Vol. 11, Issue 8-9
Tularemia: History, Epidemiology, Pathogen Physiology, and Clinical Manifestations
journal, March 2007
- Sjostedt, A.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Mucosal Immunopathogenesis of Francisella tularensis
journal, March 2007
- Metzger, D. W.; Bakshi, C. S.; Kirimanjeswara, G.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Genetics and Genetic Manipulation in Francisella Tularensis
journal, March 2007
- Frank, D. W.; Zahrt, T. C.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
A comprehensive transposon mutant library of Francisella novicida , a bioweapon surrogate
journal, January 2007
- Gallagher, Larry A.; Ramage, Elizabeth; Jacobs, Michael A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 3
Lethal pulmonary infection with Francisella novicida is associated with severe sepsis
journal, April 2009
- Sharma, Jyotika; Li, Qun; Mishra, Bibhuti B.
- Journal of Leukocyte Biology, Vol. 86, Issue 3
Role of the wbt Locus of Francisella tularensis in Lipopolysaccharide O-Antigen Biogenesis and Pathogenicity
journal, October 2006
- Raynaud, C.; Meibom, K. L.; Lety, M. -A.
- Infection and Immunity, Vol. 75, Issue 1
Genomic Comparison between a Virulent Type A1 Strain of Francisella tularensis and Its Attenuated O-Antigen Mutant
journal, April 2012
- Modise, T.; Ryder, C.; Mane, S. P.
- Journal of Bacteriology, Vol. 194, Issue 10
An Attenuated Strain of the Facultative Intracellular Bacterium Francisella tularensis Can Escape the Phagosome of Monocytic Cells
journal, September 2003
- Golovliov, I.; Baranov, V.; Krocova, Z.
- Infection and Immunity, Vol. 71, Issue 10
Evaluation of Live Tularemia Vaccine Prepared in a Chemically Defined Medium
journal, January 1965
- Chamberlain, Robert E.
- Applied Microbiology, Vol. 13, Issue 2
Tularemia Vaccine Study: I. Intracutaneous Challenge
journal, May 1961
- Saslaw, Samuel
- Archives of Internal Medicine, Vol. 107, Issue 5
Long-Term Survival of Virulent Tularemia Pathogens outside a Host in Conditions That Mimic Natural Aquatic Environments
journal, February 2021
- Golovliov, Igor; Bäckman, Stina; Granberg, Malin
- Applied and Environmental Microbiology, Vol. 87, Issue 6
Tularemia Vaccine Study: II. Respiratory Challenge
journal, May 1961
- Saslaw, Samuel
- Archives of Internal Medicine, Vol. 107, Issue 5
Tularemia as a Biological Weapon: Medical and Public Health Management
journal, June 2001
- Dennis, David T.; Inglesby, Thomas V.; Henderson, Donald A.
- JAMA, Vol. 285, Issue 21
[1] Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry
book, January 1994
- Merkle, Roberta K.; Poppe, Izabella
- Methods in Enzymology
The role of complement opsonization in interactions between F. tularensis subsp. novicida and human neutrophils
journal, July 2009
- Barker, Jason H.; McCaffrey, Ramona L.; Baman, Nicki K.
- Microbes and Infection, Vol. 11, Issue 8-9
Features of sepsis caused by pulmonary infection with Francisella tularensis Type A strain
journal, July 2011
- Sharma, Jyotika; Mares, Chris A.; Li, Qun
- Microbial Pathogenesis, Vol. 51, Issue 1-2
An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis SchuS4 strain
journal, September 2008
- Bakshi, Chandra Shekhar; Malik, Meenakshi; Mahawar, Manish
- Vaccine, Vol. 26, Issue 41
Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (ΔiglB) induces protective immunity against homotypic and heterotypic challenge
journal, September 2009
- Cong, Yu; Yu, Jieh-Juen; Guentzel, M. Neal
- Vaccine, Vol. 27, Issue 41
Identification of Francisella tularensis outer membrane protein A (FopA) as a protective antigen for tularemia
journal, July 2011
- Hickey, Anthony J.; Hazlett, Karsten R. O.; Kirimanjeswara, Girish S.
- Vaccine
Francisella novicida LPS has greater immunobiological activity in mice than F. tularensis LPS, and contributes to F. novicida murine pathogenesis
journal, April 2003
- Kieffer, T.
- Microbes and Infection, Vol. 5, Issue 5
Determination of Dextran with Anthrone
journal, November 1953
- Scott, T. A.; Melvin, E. H.
- Analytical Chemistry, Vol. 25, Issue 11
Multimethodological Approach to Identification of Glycoproteins from the Proteome of Francisella tularensis , an Intracellular Microorganism
journal, April 2010
- Balonova, Lucie; Hernychova, Lenka; Mann, Benjamin F.
- Journal of Proteome Research, Vol. 9, Issue 4
The complete genome sequence of Francisella tularensis, the causative agent of tularemia
journal, January 2005
- Larsson, Pär; Oyston, Petra C. F.; Chain, Patrick
- Nature Genetics, Vol. 37, Issue 2
The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis: The H. influenzae HMW1 adhesin is glycosylated
journal, April 2003
- Grass, Susan; Buscher, Amy Z.; Swords, W. Edward
- Molecular Microbiology, Vol. 48, Issue 3
MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival
journal, March 2004
- Lauriano, C. M.; Barker, J. R.; Yoon, S. -S.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 12
Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS
journal, September 2007
- Li, J.; Ryder, C.; Mandal, M.
- Microbiology, Vol. 153, Issue 9
Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis
journal, March 2006
- Forslund, Anna-Lena; Kuoppa, Kerstin; Svensson, Kerstin
- Molecular Microbiology, Vol. 59, Issue 6
Evaluation of Live Tularemia Vaccine Prepared in a Chemically Defined Medium
journal, March 1965
- Chamberlain, Robert E.
- Applied Microbiology, Vol. 13, Issue 2
A Francisella tularensis Locus Required for Spermine Responsiveness Is Necessary for Virulence
journal, June 2011
- Russo, Brian C.; Horzempa, Joseph; O'Dee, Dawn M.
- Infection and Immunity, Vol. 79, Issue 9
Initial Delay in the Immune Response to Francisella tularensis Is Followed by Hypercytokinemia Characteristic of Severe Sepsis and Correlating with Upregulation and Release of Damage-Associated Molecular Patterns
journal, April 2008
- Mares, Chris A.; Ojeda, Sandra S.; Morris, Elizabeth G.
- Infection and Immunity, Vol. 76, Issue 7
Vaccination with an Attenuated Strain of Francisella novicida Prevents T-Cell Depletion and Protects Mice Infected with the Wild-Type Strain from Severe Sepsis
journal, July 2009
- Sharma, Jyotika; Li, Qun; Mishra, Bibhuti B.
- Infection and Immunity, Vol. 77, Issue 10
Potential Source of Francisella tularensis Live Vaccine Strain Attenuation Determined by Genome Comparison
journal, September 2006
- Rohmer, Laurence; Brittnacher, Mitchell; Svensson, Kerstin
- Infection and Immunity, Vol. 74, Issue 12
A capsule-deficient mutant of Francisella tularensis LVS exhibits enhanced sensitivity to killing by serum but diminished sensitivity to killing by polymorphonuclear leukocytes.
journal, January 1988
- Sandström, G.; Löfgren, S.; Tärnvik, A.
- Infection and Immunity, Vol. 56, Issue 5
Association of Actinobacillus pleuropneumoniae Capsular Polysaccharide with Virulence in Pigs
journal, June 2003
- Bandara, Aloka B.; Lawrence, Mark L.; Veit, Hugo P.
- Infection and Immunity, Vol. 71, Issue 6
Superoxide Dismutase B Gene (sodB)-Deficient Mutants of Francisella tularensis Demonstrate Hypersensitivity to Oxidative Stress and Attenuated Virulence
journal, September 2006
- Bakshi, Chandra Shekhar; Malik, Meenakshi; Regan, Kevin
- Journal of Bacteriology, Vol. 188, Issue 17
O-Linked Glycosylation of the PilA Pilin Protein of Francisella tularensis: Identification of the Endogenous Protein-Targeting Oligosaccharyltransferase and Characterization of the Native Oligosaccharide
journal, July 2011
- Egge-Jacobsen, W.; Salomonsson, E. N.; Aas, F. E.
- Journal of Bacteriology, Vol. 193, Issue 19
Global Transcriptional Response to Spermine, a Component of the Intramacrophage Environment, Reveals Regulation of Francisella Gene Expression through Insertion Sequence Elements
journal, September 2009
- Carlson, Paul E.; Horzempa, Joseph; O'Dee, Dawn M.
- Journal of Bacteriology, Vol. 191, Issue 22
Genetic Dissection of the Francisella novicida Restriction Barrier
journal, October 2008
- Gallagher, L. A.; McKevitt, M.; Ramage, E. R.
- Journal of Bacteriology, Vol. 190, Issue 23
Biosynthesis and Assembly of Capsular Polysaccharides in Escherichia coli
journal, June 2006
- Whitfield, Chris
- Annual Review of Biochemistry, Vol. 75, Issue 1, p. 39-68
Characterization of a Wild-Type Strain of Francisella Tularensis Isolated from a Cat
journal, September 2004
- Inzana, Thomas J.; Glindemann, Gretchen E.; Snider, Gerald
- Journal of Veterinary Diagnostic Investigation, Vol. 16, Issue 5
The type IV pilin, PilA, is required for full virulence of Francisella tularensis subspecies tularensis
journal, January 2010
- Forslund, Anna-Lena; Naslund Salomonsson, Emelie; Golovliov, Igor
- BMC Microbiology, Vol. 10, Issue 1
Lethal pulmonary infection with Francisella novicida is associated with severe sepsis
journal, April 2009
- Sharma, Jyotika; Li, Qun; Mishra, Bibhuti B.
- Journal of Leukocyte Biology, Vol. 86, Issue 3
The Structure and Function of Francisella Lipopolysaccharide
journal, March 2007
- Gunn, J. S.; Ernst, R. K.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Mucosal Immunopathogenesis of Francisella tularensis
journal, March 2007
- Metzger, D. W.; Bakshi, C. S.; Kirimanjeswara, G.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Genetics and Genetic Manipulation in Francisella Tularensis
journal, March 2007
- Frank, D. W.; Zahrt, T. C.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Tularemia: History, Epidemiology, Pathogen Physiology, and Clinical Manifestations
journal, March 2007
- Sjostedt, A.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Molecular Epidemiology, Evolution, and Ecology of Francisella
journal, March 2007
- Keim, P.; Johansson, A.; Wagner, D. M.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Vaccines Against Francisella Tularensis
journal, March 2007
- Wayne Conlan, J.; Oyston, P. C. F.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Innate and Adaptive Immunity to Francisella
journal, March 2007
- Elkins, K. L.; Cowley, S. C.; Bosio, C. M.
- Annals of the New York Academy of Sciences, Vol. 1105, Issue 1
Identification, Characterization and Immunogenicity of an O-Antigen Capsular Polysaccharide of Francisella tularensis
journal, July 2010
- Apicella, Michael A.; Post, Deborah M. B.; Fowler, Andrew C.
- PLoS ONE, Vol. 5, Issue 7
Molecular Immune Responses to Aerosol Challenge with Francisella tularensis in Mice Inoculated with Live Vaccine Candidates of Varying Efficacy
journal, October 2010
- Shen, Hua; Harris, Gregory; Chen, Wangxue
- PLoS ONE, Vol. 5, Issue 10
Uncovering the components of the Francisella tularensis virulence stealth strategy
journal, March 2014
- Jones, Bradley D.; Faron, Matthew; Rasmussen, Jed A.
- Frontiers in Cellular and Infection Microbiology, Vol. 4
Immunity to Francisella
journal, January 2011
- Cowley, Siobhán C.; Elkins, Karen L.
- Frontiers in Microbiology, Vol. 2
Works referencing / citing this record:
Formation of the Francisella tularensis Biofilm is Affected by Cell Surface Glycosylation, Growth Medium, and a Glucan Exopolysaccharide
journal, August 2019
- Champion, Anna E.; Catanzaro, Kelly C. Freudenberger; Bandara, Aloka B.
- Scientific Reports, Vol. 9, Issue 1
Further Characterization of the Capsule-Like Complex (CLC) Produced by Francisella tularensis Subspecies tularensis: Protective Efficacy and Similarity to Outer Membrane Vesicles
journal, June 2018
- Champion, Anna E.; Bandara, Aloka B.; Mohapatra, Nrusingh
- Frontiers in Cellular and Infection Microbiology, Vol. 8
Formation of the Francisella tularensis Biofilm is Affected by Cell Surface Glycosylation, Growth Medium, and a Glucan Exopolysaccharide
journal, August 2019
- Champion, Anna E.; Catanzaro, Kelly C. Freudenberger; Bandara, Aloka B.
- Scientific Reports, Vol. 9, Issue 1