Identification of Chromosomal Genes in Yersinia pestis that Influence Type III Secretion and Delivery of Yops into Target Cells

Houppert, Andrew S.; Kwiatkowski, Elizabeth; Glass, Elizabeth M.; DeBord, Kristin L.; Merritt, Peter M.; Schneewind, Olaf; Marketon, Melanie M.

doi:10.1371/journal.pone.0034039

**Identification of Chromosomal Genes in Yersinia pestis that Influence Type III Secretion and Delivery of Yops into Target Cells**

Journal Article · Fri Mar 30 00:00:00 EDT 2012 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0034039· OSTI ID:1627507

Houppert, Andrew S. ^[1]; Kwiatkowski, Elizabeth ^[2]; Glass, Elizabeth M. ^[3]; DeBord, Kristin L. ^[2]; Merritt, Peter M. ^[4]; Schneewind, Olaf ^[2]; Marketon, Melanie M. ^[5]

Indiana University, Bloomington, IN (United States); DOE/OSTI
University of Chicago, IL (United States)
Argonne National Laboratory (ANL), Argonne, IL (United States)
Indiana University, Bloomington, IN (United States)
Indiana University, Bloomington, IN (United States); University of Chicago, IL (United States)

Pathogenic Yersinia species possess a type III secretion system, which is required for the delivery of effector Yop proteins into target cells during infection. Genes encoding the type III secretion machinery, its substrates, and several regulatory proteins all reside on a 70-Kb virulence plasmid. Genes encoded in the chromosome of yersiniae are thought to play important roles in bacterial perception of host environments and in the coordinated activation of the type III secretion pathway. Here, we investigate the contribution of chromosomal genes to the complex regulatory process controlling type III secretion in Yersinia pestis. Using transposon mutagenesis, we identified five chromosomal genes required for expression or secretion of Yops in laboratory media. Four out of the five chromosomal mutants were defective to various extents at injecting Yops into tissue culture cells. Interestingly, we found one mutant that was not able to secrete in vitro but was fully competent for injecting Yops into host cells, suggesting independent mechanisms for activation of the secretion apparatus. When tested in a mouse model of plague disease, three mutants were avirulent, whereas two strains were severely attenuated. Together these results demonstrate the importance of Y. pestis chromosomal genes in the proper function of type III secretion and in the pathogenesis of plague.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Great Lakes Regional Center of Excellence; National Institute of Allergy and Infectious Diseases; Indiana University; National Institute of Allergy and Infectious Diseases

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1627507

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 3 Vol. 7; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (111)

Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y.enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus. Boland, A.; Sory, M. P.; Iriarte, M. The EMBO Journal, Vol. 15, Issue 19 https://doi.org/10.1002/j.1460-2075.1996.tb00904.x	journal	October 1996
High-copy-number and low-copy-number plasmid vectors for lacZα-complementation and chloramphenicol- or kanamycin-resistance selection Takeshita, Sunao; Sato, Masahiro; Toba, Mari Gene, Vol. 61, Issue 1 https://doi.org/10.1016/0378-1119(87)90365-9	journal	January 1987
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
A database for post-genome analysis Kanehisa, Minoru Trends in Genetics, Vol. 13, Issue 9 https://doi.org/10.1016/s0168-9525(97)01223-7	journal	September 1997
Genome sequence of Yersinia pestis, the causative agent of plague Parkhill, J.; Wren, B. W.; Thomson, N. R. Nature, Vol. 413, Issue 6855 https://doi.org/10.1038/35097083	journal	October 2001
The type III secretion injectisome Cornelis, Guy R. Nature Reviews Microbiology, Vol. 4, Issue 11 https://doi.org/10.1038/nrmicro1526	journal	November 2006
Identification of novel chromosomal loci affecting Yersinia enterocolitica pathogenesis Young, Glenn M.; Miller, Virginia L. Molecular Microbiology, Vol. 25, Issue 02 https://doi.org/10.1046/j.1365-2958.1997.4661829.x	journal	July 1997
The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring‐shaped multimeric complex Koster, Margot; Bitter, Wilbert; De Cock, Hans Molecular Microbiology, Vol. 26, Issue 4 https://doi.org/10.1046/j.1365-2958.1997.6141981.x	journal	November 1997
YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells Iriarte, Maite; Cornelis, Guy R. Molecular Microbiology, Vol. 29, Issue 3 https://doi.org/10.1046/j.1365-2958.1998.00992.x	journal	August 1998
Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague Sebbane, F.; Jarrett, C. O.; Gardner, D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 14 https://doi.org/10.1073/pnas.0509544103	journal	March 2006
Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells Hoiczyk, E.; Blobel, G. Proceedings of the National Academy of Sciences, Vol. 98, Issue 8 https://doi.org/10.1073/pnas.071065798	journal	April 2001
Large-scale isolation of candidate virulence genes of Pseudomonas aeruginosa by in vivo selection. Wang, J.; Mushegian, A.; Lory, S. Proceedings of the National Academy of Sciences, Vol. 93, Issue 19 https://doi.org/10.1073/pnas.93.19.10434	journal	September 1996
The Effect of Ca++ and Mg++ on Lysis, Growth, and Production of Virulence Antigens by Pasteurella Pestis Brubaker, R. R.; Surgalla, M. J. Journal of Infectious Diseases, Vol. 114, Issue 1 https://doi.org/10.1093/infdis/114.1.13	journal	February 1964
CD-Search: protein domain annotations on the fly Marchler-Bauer, A.; Bryant, S. H. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh454	journal	July 2004
Regulation by Ca ²⁺ in the Yersinia low-Ca ²⁺ response Straley, Susan C.; Plano, Gregory V.; Skrzypek, Elźbieta Molecular Microbiology, Vol. 8, Issue 6 https://doi.org/10.1111/j.1365-2958.1993.tb01644.x	journal	June 1993
Function of the rfb gene cluster and the rfe gene in the synthesis of O antigen by Shigella dysenteriae 1 Klena, J. D.; Schnaitman, C. A. Molecular Microbiology, Vol. 9, Issue 2 https://doi.org/10.1111/j.1365-2958.1993.tb01700.x	journal	July 1993
A Plasminogen-Activating Protease Specifically Controls the Development of Primary Pneumonic Plague Lathem, W. W.; Price, P. A.; Miller, V. L. Science, Vol. 315, Issue 5811 https://doi.org/10.1126/science.1137195	journal	January 2007
Death by Lethal Injection Silhavy, Thomas J. Science, Vol. 278, Issue 5340 https://doi.org/10.1126/science.278.5340.1085	journal	November 1997
Yersinia pestis--etiologic agent of plague. Perry, R. D.; Fetherston, J. D. Clinical Microbiology Reviews, Vol. 10, Issue 1 https://doi.org/10.1128/cmr.10.1.35	journal	January 1997
Transcriptional Induction of the Pseudomonas aeruginosa Type III Secretion System by Low Ca2+ and Host Cell Contact Proceeds through Two Distinct Signaling Pathways Dasgupta, Nandini; Ashare, Alix; Hunninghake, Gary W. Infection and Immunity, Vol. 74, Issue 6 https://doi.org/10.1128/iai.00090-06	journal	June 2006
Resistance of Yersinia pestis to Complement-Dependent Killing Is Mediated by the Ail Outer Membrane Protein Bartra, Sara Schesser; Styer, Katie L.; O'Bryant, Deanna M. Infection and Immunity, Vol. 76, Issue 2 https://doi.org/10.1128/iai.01125-07	journal	November 2007
Plague virulence antigens from Yersinia enterocolitica Carter, P. B.; Zahorchak, R. J.; Brubaker, R. R. Infection and Immunity, Vol. 28, Issue 2 https://doi.org/10.1128/iai.28.2.638-640.1980	journal	May 1980
Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Portnoy, D. A.; Moseley, S. L.; Falkow, S. Infection and Immunity, Vol. 31, Issue 2 https://doi.org/10.1128/iai.31.2.775-782.1981	journal	January 1981
Genetically manipulated virulence of Yersinia enterocolitica. Heesemann, J.; Algermissen, B.; Laufs, R. Infection and Immunity, Vol. 46, Issue 1 https://doi.org/10.1128/iai.46.1.105-110.1984	journal	January 1984
Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Sodeinde, O. A.; Goguen, J. D. Infection and Immunity, Vol. 56, Issue 10 https://doi.org/10.1128/iai.56.10.2743-2748.1988	journal	January 1988
Plasminogen activator/coagulase gene of Yersinia pestis is responsible for degradation of plasmid-encoded outer membrane proteins. Sodeinde, O. A.; Sample, A. K.; Brubaker, R. R. Infection and Immunity, Vol. 56, Issue 10 https://doi.org/10.1128/iai.56.10.2749-2752.1988	journal	January 1988
Secretion of Yop proteins by Yersiniae. Michiels, T.; Wattiau, P.; Brasseur, R. Infection and Immunity, Vol. 58, Issue 9 https://doi.org/10.1128/iai.58.9.2840-2849.1990	journal	January 1990
Expression of the soxR Gene ofPseudomonas aeruginosa Is Inducible during Infection of Burn Wounds in Mice and Is Required To Cause Efficient Bacteremia Ha, Unhwan; Jin, Shouguang Infection and Immunity, Vol. 67, Issue 10 https://doi.org/10.1128/iai.67.10.5324-5331.1999	journal	October 1999
Application of High-Density Array-Based Signature-Tagged Mutagenesis To Discover Novel YersiniaVirulence-Associated Genes Karlyshev, A. V.; Oyston, P. C. F.; Williams, K. Infection and Immunity, Vol. 69, Issue 12 https://doi.org/10.1128/iai.69.12.7810-7819.2001	journal	December 2001
Activation of the Pseudomonas aeruginosa Type III Secretion System Requires an Intact Pyruvate Dehydrogenase aceAB Operon Dacheux, Denis; Epaulard, Olivier; de Groot, Arjan Infection and Immunity, Vol. 70, Issue 7 https://doi.org/10.1128/iai.70.7.3973-3977.2002	journal	July 2002
Generation of Yersinia pestis Attenuated Strains by Signature-Tagged Mutagenesis in Search of Novel Vaccine Candidates Flashner, Yehuda; Mamroud, Emanuelle; Tidhar, Avital Infection and Immunity, Vol. 72, Issue 2 https://doi.org/10.1128/iai.72.2.908-915.2004	journal	February 2004
Effect of Metabolic Imbalance on Expression of Type III Secretion Genes in Pseudomonas aeruginosa Rietsch, Arne; Wolfgang, Matthew C.; Mekalanos, John J. Infection and Immunity, Vol. 72, Issue 3 https://doi.org/10.1128/iai.72.3.1383-1390.2004	journal	March 2004
Calcium-Regulated Type III Secretion of Yop Proteins by an Escherichia coli hha Mutant Carrying a Yersinia pestis pCD1 Virulence Plasmid Bartra, Sara Schesser; Jackson, Michael W.; Ross, Julia A. Infection and Immunity, Vol. 74, Issue 2 https://doi.org/10.1128/iai.74.2.1381-1386.2006	journal	February 2006
Construction of a mobilizable Yersinia enterocolitica virulence plasmid. Heesemann, J.; Laufs, R. Journal of Bacteriology, Vol. 155, Issue 2 https://doi.org/10.1128/jb.155.2.761-767.1983	journal	January 1983
Temperature-controlled plasmid regulon associated with low calcium response in Yersinia pestis. Yother, J.; Chamness, T. W.; Goguen, J. D. Journal of Bacteriology, Vol. 165, Issue 2 https://doi.org/10.1128/jb.165.2.443-447.1986	journal	January 1986
Temperature sensing in Yersinia pestis: regulation of yopE transcription by lcrF. Hoe, N. P.; Minion, F. C.; Goguen, J. D. Journal of Bacteriology, Vol. 174, Issue 13 https://doi.org/10.1128/jb.174.13.4275-4286.1992	journal	January 1992
Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. Hoe, N. P.; Goguen, J. D. Journal of Bacteriology, Vol. 175, Issue 24 https://doi.org/10.1128/jb.175.24.7901-7909.1993	journal	January 1993
Identification of DNA sequences recognized by VirF, the transcriptional activator of the Yersinia yop regulon. Wattiau, P.; Cornelis, G. R. Journal of Bacteriology, Vol. 176, Issue 13 https://doi.org/10.1128/jb.176.13.3878-3884.1994	journal	January 1994
The V Antigen of Yersinia pestisRegulates Yop Vectorial Targeting as Well as Yop Secretion through Effects on YopB and LcrG Nilles, Matthew L.; Fields, Kenneth A.; Straley, Susan C. Journal of Bacteriology, Vol. 180, Issue 13 https://doi.org/10.1128/jb.180.13.3410-3420.1998	journal	July 1998
YscB of Yersinia pestis Functions as a Specific Chaperone for YopN Jackson, Michael W.; Day, James B.; Plano, Gregory V. Journal of Bacteriology, Vol. 180, Issue 18 https://doi.org/10.1128/jb.180.18.4912-4921.1998	journal	September 1998
Structural Organization of Virulence-Associated Plasmids of Yersinia pestis Hu, Ping; Elliott, Jeffrey; McCready, Paula Journal of Bacteriology, Vol. 180, Issue 19 https://doi.org/10.1128/jb.180.19.5192-5202.1998	journal	October 1998
Yersinia enterocolitica TyeA, an Intracellular Regulator of the Type III Machinery, Is Required for Specific Targeting of YopE, YopH, YopM, and YopN into the Cytosol of Eukaryotic Cells Cheng, Luisa W.; Schneewind, Olaf Journal of Bacteriology, Vol. 182, Issue 11 https://doi.org/10.1128/jb.182.11.3183-3190.2000	journal	June 2000
Roles of LcrG and LcrV during Type III Targeting of Effector Yops by Yersinia enterocolitica DeBord, Kristin L.; Lee, Vincent T.; Schneewind, Olaf Journal of Bacteriology, Vol. 183, Issue 15 https://doi.org/10.1128/jb.183.15.4588-4598.2001	journal	August 2001
A Program of Yersinia enterocolitica Type III Secretion Reactions Is Activated by Specific Signals Lee, V. T.; Mazmanian, S. K.; Schneewind, O. Journal of Bacteriology, Vol. 183, Issue 17 https://doi.org/10.1128/jb.183.17.4970-4978.2001	journal	September 2001
Regulated Secretion of YopN by the Type III Machinery of Yersinia enterocolitica Cheng, Luisa W.; Kay, Olga; Schneewind, Olaf Journal of Bacteriology, Vol. 183, Issue 18 https://doi.org/10.1128/jb.183.18.5293-5301.2001	journal	September 2001
Role of the Pilot Protein YscW in the Biogenesis of the YscC Secretin in Yersinia enterocolitica Burghout, Peter; Beckers, Frank; de Wit, Emmie Journal of Bacteriology, Vol. 186, Issue 16 https://doi.org/10.1128/jb.186.16.5366-5375.2004	journal	August 2004
Cationic Antimicrobial Peptide Resistance in Neisseria meningitidis Tzeng, Yih-Ling; Ambrose, Karita D.; Zughaier, Susu Journal of Bacteriology, Vol. 187, Issue 15 https://doi.org/10.1128/jb.187.15.5387-5396.2005	journal	August 2005
Studies on the Nutrition and Physiology of Pasteurella Pestis Higuchi, K.; Kupferberg, L. L.; Smith, J. L. Journal of Bacteriology, Vol. 77, Issue 3 https://doi.org/10.1128/jb.77.3.317-321.1959	journal	January 1959
Glucose-6-Phosphate Dehydrogenase and 6-Phosphogluconate Dehydrogenase Activities of Pasteurella Pestis and Pasteurella Pseudotuberculosis Mortlock, R. P.; Brubaker, R. R. Journal of Bacteriology, Vol. 84, Issue 5 https://doi.org/10.1128/jb.84.5.1122-1123.1962	journal	January 1962
The Virulence Plasmid of Yersinia, an Antihost Genome Cornelis, Guy R.; Boland, Anne; Boyd, Aoife P. Microbiology and Molecular Biology Reviews, Vol. 62, Issue 4 https://doi.org/10.1128/mmbr.62.4.1315-1352.1998	journal	December 1998
Genetics of lipopolysaccharide biosynthesis in enteric bacteria Schnaitman, C. A.; Klena, J. D. Microbiological Reviews, Vol. 57, Issue 3 https://doi.org/10.1128/mr.57.3.655-682.1993	journal	September 1993
MOLECULAR BASIS FOR MEMBRANE PHOSPHOLIPID DIVERSITY:Why Are There So Many Lipids? Dowhan, W. Annual Review of Biochemistry, Vol. 66, Issue 1 https://doi.org/10.1146/annurev.biochem.66.1.199	journal	June 1997
A complex of N5,N10-methylenetetrahydrofolate dehydrogenase and N5,N10-methenyltetrahydrofolate cyclohydrolase in Escherichia coli. Purification, subunit structure, and allosteric inhibition by N10-formyltetrahydrofolate. Dev, I. K.; Harvey, R. J. Journal of Biological Chemistry, Vol. 253, Issue 12 https://doi.org/10.1016/S0021-9258(17)34711-7	journal	June 1978
Biosynthesis of enterobacterial common antigen in Escherichia coli. Biochemical characterization of Tn10 insertion mutants defective in enterobacterial common antigen synthesis. Meier-Dieter, U.; Starman, R.; Barr, K. Journal of Biological Chemistry, Vol. 265, Issue 23 https://doi.org/10.1016/S0021-9258(18)77373-0	journal	August 1990
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
A database for post-genome analysis Kanehisa, Minoru Trends in Genetics, Vol. 13, Issue 9 https://doi.org/10.1016/S0168-9525(97)01223-7	journal	September 1997
A specific polysaccharide of Pasteurella pestis Davies, D. A. L. Biochemical Journal, Vol. 63, Issue 1 https://doi.org/10.1042/bj0630105	journal	May 1956
Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism Maden, B. Edward H. Biochemical Journal, Vol. 350, Issue 3 https://doi.org/10.1042/bj3500609	journal	September 2000
Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system: Y. pestis LOS characterization and regulation of expression by PhoPQ Hitchen, Paul G.; Prior, Joann L.; Oyston, Petra C. F. Molecular Microbiology, Vol. 44, Issue 6 https://doi.org/10.1046/j.1365-2958.2002.02990.x	journal	June 2002
Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies: Translocation of YopE and YopN Day, James B.; Ferracci, Franco; Plano, Gregory V. Molecular Microbiology, Vol. 47, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03343.x	journal	January 2003
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM Kolodziejek, Anna M.; Sinclair, Dylan J.; Seo, Keun S. Microbiology, Vol. 153, Issue 9 https://doi.org/10.1099/mic.0.2006/005694-0	journal	September 2007
PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B: Resistance to antimicrobial peptides Shi, Yixin; Cromie, Michael J.; Hsu, Fong-Fu Molecular Microbiology, Vol. 53, Issue 1 https://doi.org/10.1111/j.1365-2958.2004.04107.x	journal	May 2004
An in vivo inducible gene of Pseudomonas aeruginosa encodes an anti-ExsA to suppress the type III secretion system: PtrA inhibits type III secretion system Ha, Un-Hwan; Kim, Jaewha; Badrane, Hassan Molecular Microbiology, Vol. 54, Issue 2 https://doi.org/10.1111/j.1365-2958.2004.04282.x	journal	September 2004
Selection and characterization of Yersinia pestis YopN mutants that constitutively block Yop secretion: Y. pestis YopN mutants that constitutively block secretion Ferracci, Franco; Schubot, Florian D.; Waugh, David S. Molecular Microbiology, Vol. 57, Issue 4 https://doi.org/10.1111/j.1365-2958.2005.04738.x	journal	June 2005
The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion: Role of YscF in the regulation of Yop secretion Torruellas, Julie; Jackson, Michael W.; Pennock, Jeffry W. Molecular Microbiology, Vol. 57, Issue 6 https://doi.org/10.1111/j.1365-2958.2005.04790.x	journal	July 2005
YopK regulates the Yersinia pestis type III secretion system from within host cells: Regulation of the Y. pestis TTSS by YopK Dewoody, Rebecca; Merritt, Peter M.; Houppert, Andrew S. Molecular Microbiology, Vol. 79, Issue 6 https://doi.org/10.1111/j.1365-2958.2011.07534.x	journal	January 2011
Plague Bacteria Target Immune Cells During Infection Marketon, M. M. Science, Vol. 309, Issue 5741 https://doi.org/10.1126/science.1114580	journal	September 2005
A mRNA Signal for the Type III Secretion of Yop Proteins by Yersinia enterocolitica Anderson, D. M. Science, Vol. 278, Issue 5340 https://doi.org/10.1126/science.278.5340.1140	journal	November 1997
Yersinia pestis--etiologic agent of plague. Perry, R. D.; Fetherston, J. D. Clinical Microbiology Reviews, Vol. 10, Issue 1 https://doi.org/10.1128/CMR.10.1.35	journal	January 1997
Transcriptional Induction of the Pseudomonas aeruginosa Type III Secretion System by Low Ca2+ and Host Cell Contact Proceeds through Two Distinct Signaling Pathways Dasgupta, Nandini; Ashare, Alix; Hunninghake, Gary W. Infection and Immunity, Vol. 74, Issue 6 https://doi.org/10.1128/IAI.00090-06	journal	June 2006
Resistance of Yersinia pestis to Complement-Dependent Killing Is Mediated by the Ail Outer Membrane Protein Bartra, Sara Schesser; Styer, Katie L.; O'Bryant, Deanna M. Infection and Immunity, Vol. 76, Issue 2 https://doi.org/10.1128/IAI.01125-07	journal	November 2007
Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Portnoy, D. A.; Moseley, S. L.; Falkow, S. Infection and Immunity, Vol. 31, Issue 2 https://doi.org/10.1128/IAI.31.2.775-782.1981	journal	January 1981
Genetically manipulated virulence of Yersinia enterocolitica. Heesemann, J.; Algermissen, B.; Laufs, R. Infection and Immunity, Vol. 46, Issue 1 https://doi.org/10.1128/IAI.46.1.105-110.1984	journal	January 1984
Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Sodeinde, O. A.; Goguen, J. D. Infection and Immunity, Vol. 56, Issue 10 https://doi.org/10.1128/IAI.56.10.2743-2748.1988	journal	January 1988
Plasminogen activator/coagulase gene of Yersinia pestis is responsible for degradation of plasmid-encoded outer membrane proteins. Sodeinde, O. A.; Sample, A. K.; Brubaker, R. R. Infection and Immunity, Vol. 56, Issue 10 https://doi.org/10.1128/IAI.56.10.2749-2752.1988	journal	January 1988
Secretion of Yop proteins by Yersiniae. Michiels, T.; Wattiau, P.; Brasseur, R. Infection and Immunity, Vol. 58, Issue 9 https://doi.org/10.1128/IAI.58.9.2840-2849.1990	journal	January 1990
Expression of the soxR Gene ofPseudomonas aeruginosa Is Inducible during Infection of Burn Wounds in Mice and Is Required To Cause Efficient Bacteremia Ha, Unhwan; Jin, Shouguang Infection and Immunity, Vol. 67, Issue 10 https://doi.org/10.1128/IAI.67.10.5324-5331.1999	journal	October 1999
Virulence Role of V Antigen of Yersinia pestis at the Bacterial Surface Fields, Kenneth A.; Nilles, Matthew L.; Cowan, Clarissa Infection and Immunity, Vol. 67, Issue 10 https://doi.org/10.1128/IAI.67.10.5395-5408.1999	journal	October 1999
Identification of Attenuated Yersinia pseudotuberculosis Strains and Characterization of an Orogastric Infection in BALB/c Mice on Day 5 Postinfection by Signature-Tagged Mutagenesis Mecsas, Joan; Bilis, Inna; Falkow, Stanley Infection and Immunity, Vol. 69, Issue 5 https://doi.org/10.1128/IAI.67.5.2779-2787.2001	journal	May 2001
Application of High-Density Array-Based Signature-Tagged Mutagenesis To Discover Novel YersiniaVirulence-Associated Genes Karlyshev, A. V.; Oyston, P. C. F.; Williams, K. Infection and Immunity, Vol. 69, Issue 12 https://doi.org/10.1128/IAI.69.12.7810-7819.2001	journal	December 2001
Activation of the Pseudomonas aeruginosa Type III Secretion System Requires an Intact Pyruvate Dehydrogenase aceAB Operon Dacheux, Denis; Epaulard, Olivier; de Groot, Arjan Infection and Immunity, Vol. 70, Issue 7 https://doi.org/10.1128/IAI.70.7.3973-3977.2002	journal	July 2002
Role of Yops and Adhesins in Resistance of Yersinia enterocolitica to Phagocytosis Grosdent, Nadine; Maridonneau-Parini, Isabelle; Sory, Marie-Paule Infection and Immunity, Vol. 70, Issue 8 https://doi.org/10.1128/IAI.70.8.4165-4176.2002	journal	August 2002
Generation of Yersinia pestis Attenuated Strains by Signature-Tagged Mutagenesis in Search of Novel Vaccine Candidates Flashner, Yehuda; Mamroud, Emanuelle; Tidhar, Avital Infection and Immunity, Vol. 72, Issue 2 https://doi.org/10.1128/IAI.72.2.908-915.2004	journal	February 2004
Effect of Metabolic Imbalance on Expression of Type III Secretion Genes in Pseudomonas aeruginosa Rietsch, Arne; Wolfgang, Matthew C.; Mekalanos, John J. Infection and Immunity, Vol. 72, Issue 3 https://doi.org/10.1128/IAI.72.3.1383-1390.2004	journal	March 2004
Influence of Na+, Dicarboxylic Amino Acids, and pH in Modulating the Low-Calcium Response of Yersinia pestis Brubaker, Robert R. Infection and Immunity, Vol. 73, Issue 8 https://doi.org/10.1128/IAI.73.8.4743-4752.2005	journal	August 2005
Calcium-Regulated Type III Secretion of Yop Proteins by an Escherichia coli hha Mutant Carrying a Yersinia pestis pCD1 Virulence Plasmid Bartra, Sara Schesser; Jackson, Michael W.; Ross, Julia A. Infection and Immunity, Vol. 74, Issue 2 https://doi.org/10.1128/IAI.74.2.1381-1386.2006	journal	February 2006
Temperature Sensitivity and Cell Division Defects in an Escherichia coli Strain with Mutations in yghB and yqjA, Encoding Related and Conserved Inner Membrane Proteins Thompkins, Kandi; Chattopadhyay, Ballari; Xiao, Ying Journal of Bacteriology, Vol. 190, Issue 13 https://doi.org/10.1128/JB.00414-08	journal	May 2008
Consequences of aspartase deficiency in Yersinia pestis. Dreyfus, L. A.; Brubaker, R. R. Journal of Bacteriology, Vol. 136, Issue 2 https://doi.org/10.1128/JB.136.2.757-764.1978	journal	January 1978
Construction of a mobilizable Yersinia enterocolitica virulence plasmid. Heesemann, J.; Laufs, R. Journal of Bacteriology, Vol. 155, Issue 2 https://doi.org/10.1128/JB.155.2.761-767.1983	journal	January 1983
Genetic analysis of the low calcium response in Yersinia pestis mu d1(Ap lac) insertion mutants. Goguen, J. D.; Yother, J.; Straley, S. C. Journal of Bacteriology, Vol. 160, Issue 3 https://doi.org/10.1128/JB.160.3.842-848.1984	journal	January 1984
The V Antigen of Yersinia pestisRegulates Yop Vectorial Targeting as Well as Yop Secretion through Effects on YopB and LcrG Nilles, Matthew L.; Fields, Kenneth A.; Straley, Susan C. Journal of Bacteriology, Vol. 180, Issue 13 https://doi.org/10.1128/JB.180.13.3410-3420.1998	journal	July 1998
YscB of Yersinia pestis Functions as a Specific Chaperone for YopN Jackson, Michael W.; Day, James B.; Plano, Gregory V. Journal of Bacteriology, Vol. 180, Issue 18 https://doi.org/10.1128/JB.180.18.4912-4921.1998	journal	September 1998
Structural Organization of Virulence-Associated Plasmids of Yersinia pestis Hu, Ping; Elliott, Jeffrey; McCready, Paula Journal of Bacteriology, Vol. 180, Issue 19 https://doi.org/10.1128/JB.180.19.5192-5202.1998	journal	October 1998
Yersinia enterocolitica TyeA, an Intracellular Regulator of the Type III Machinery, Is Required for Specific Targeting of YopE, YopH, YopM, and YopN into the Cytosol of Eukaryotic Cells Cheng, Luisa W.; Schneewind, Olaf Journal of Bacteriology, Vol. 182, Issue 11 https://doi.org/10.1128/JB.182.11.3183-3190.2000	journal	June 2000
Roles of LcrG and LcrV during Type III Targeting of Effector Yops by Yersinia enterocolitica DeBord, Kristin L.; Lee, Vincent T.; Schneewind, Olaf Journal of Bacteriology, Vol. 183, Issue 15 https://doi.org/10.1128/JB.183.15.4588-4598.2001	journal	August 2001
A Program of Yersinia enterocolitica Type III Secretion Reactions Is Activated by Specific Signals Lee, V. T.; Mazmanian, S. K.; Schneewind, O. Journal of Bacteriology, Vol. 183, Issue 17 https://doi.org/10.1128/JB.183.17.4970-4978.2001	journal	September 2001
Regulated Secretion of YopN by the Type III Machinery of Yersinia enterocolitica Cheng, Luisa W.; Kay, Olga; Schneewind, Olaf Journal of Bacteriology, Vol. 183, Issue 18 https://doi.org/10.1128/JB.183.18.5293-5301.2001	journal	September 2001
Yersinia enterocolitica Type III Secretion: Mutational Analysis of the yopQ Secretion Signal Ramamurthi, Kumaran S.; Schneewind, Olaf Journal of Bacteriology, Vol. 184, Issue 12 https://doi.org/10.1128/JB.184.12.3321-3328.2002	journal	June 2002
Genome Sequence of Yersinia pestis KIM Deng, W.; Burland, V.; Plunkett III, G. Journal of Bacteriology, Vol. 184, Issue 16 https://doi.org/10.1128/JB.184.16.4601-4611.2002	journal	August 2002
Role of the Pilot Protein YscW in the Biogenesis of the YscC Secretin in Yersinia enterocolitica Burghout, Peter; Beckers, Frank; de Wit, Emmie Journal of Bacteriology, Vol. 186, Issue 16 https://doi.org/10.1128/JB.186.16.5366-5375.2004	journal	August 2004
Cationic Antimicrobial Peptide Resistance in Neisseria meningitidis Tzeng, Yih-Ling; Ambrose, Karita D.; Zughaier, Susu Journal of Bacteriology, Vol. 187, Issue 15 https://doi.org/10.1128/JB.187.15.5387-5396.2005	journal	August 2005
Studies on the Nutrition and Physiology of Pasteurella Pestis Higuchi, K.; Kupferberg, L. L.; Smith, J. L. Journal of Bacteriology, Vol. 77, Issue 3 https://doi.org/10.1128/JB.77.3.317-321.1959	journal	January 1959
Glucose-6-Phosphate Dehydrogenase and 6-Phosphogluconate Dehydrogenase Activities of Pasteurella Pestis and Pasteurella Pseudotuberculosis Mortlock, R. P.; Brubaker, R. R. Journal of Bacteriology, Vol. 84, Issue 5 https://doi.org/10.1128/JB.84.5.1122-1123.1962	journal	January 1962
Mutation rate to nonpigmentation in Pasteurella pestis. Brubaker, R. R. Journal of Bacteriology, Vol. 98, Issue 3 https://doi.org/10.1128/JB.98.3.1404-1406.1969	journal	January 1969
Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Schnaitman, C. A.; Klena, J. D. Microbiological Reviews, Vol. 57, Issue 3 https://doi.org/10.1128/MMBR.57.3.655-682.1993	journal	January 1993
The Virulence Plasmid of Yersinia, an Antihost Genome Cornelis, Guy R.; Boland, Anne; Boyd, Aoife P. Microbiology and Molecular Biology Reviews, Vol. 62, Issue 4 https://doi.org/10.1128/MMBR.62.4.1315-1352.1998	journal	December 1998
Pseudomonas aeruginosa transposable bacteriophages D3112 and B3 require pili and surface growth for adsorption. Roncero, C.; Darzins, A.; Casadaban, M. J. Journal of Bacteriology, Vol. 172, Issue 4 https://doi.org/10.1128/jb.172.4.1899-1904.1990	journal	January 1990
LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis. Skryzpek, E.; Straley, S. C. Journal of Bacteriology, Vol. 175, Issue 11 https://doi.org/10.1128/jb.175.11.3520-3528.1993	journal	January 1993
VirG, a Yersinia enterocolitica lipoprotein involved in Ca2+ dependency, is related to exsB of Pseudomonas aeruginosa. Allaoui, A.; Scheen, R.; Lambert de Rouvroit, C. Journal of bacteriology, Vol. 177, Issue 15 https://doi.org/10.1128/jb.177.15.4230-4237.1995	journal	January 1995
Yersinia pestis LcrV forms a stable complex with LcrG and may have a secretion-related regulatory role in the low-Ca2+ response. Nilles, M. L.; Williams, A. W.; Skrzypek, E. Journal of bacteriology, Vol. 179, Issue 4 https://doi.org/10.1128/jb.179.4.1307-1316.1997	journal	January 1997

Cited By (4)

Resistance to Innate Immunity Contributes to Colonization of the Insect Gut by Yersinia pestis Earl, Shaun C.; Rogers, Miles T.; Keen, Jennifer PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0133318	journal	July 2015
Illuminating Targets of Bacterial Secretion Pechous, Roger D.; Goldman, William E. PLOS Pathogens, Vol. 11, Issue 8 https://doi.org/10.1371/journal.ppat.1004981	journal	August 2015
Regulation of the Yersinia type III secretion system: traffic control Dewoody, Rebecca S.; Merritt, Peter M.; Marketon, Melanie M. Frontiers in Cellular and Infection Microbiology, Vol. 3 https://doi.org/10.3389/fcimb.2013.00004	journal	January 2013
YopK controls both rate and fidelity of Yop translocation: Control of translocation by YopK Dewoody, Rebecca; Merritt, Peter M.; Marketon, Melanie M. Molecular Microbiology, Vol. 87, Issue 2 https://doi.org/10.1111/mmi.12099	journal	December 2012

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
immunoblotting
mouse models
outer membrane proteins
phenotypes
secretion
transposable elements
yersinia
yersinia pestis