The Yersinia enterocolitica Ysa type III secretion system is expressed during infections both in vitro and in vivo

Bent, Zachary W.; Branda, Steven S.; Young, Glenn M.

doi:10.1002/mbo3.136

The Yersinia enterocolitica Ysa type III secretion system is expressed during infections both in vitro and in vivo

Journal Article · Sun Dec 01 00:00:00 EST 2013 · MicrobiologyOpen

DOI:https://doi.org/10.1002/mbo3.136· OSTI ID:1623571

Bent, Zachary W. ^[1]; Branda, Steven S. ^[2]; Young, Glenn M. ^[3]

Univ. of California, Davis, CA (United States). Microbiology Graduate Group; Sandia National Lab. (SNL-CA), Livermore, CA (United States). Systems Biology; DOE/OSTI
Sandia National Lab. (SNL-CA), Livermore, CA (United States). Biotechnology and Bioengineering
Univ. of California, Davis, CA (United States). Microbiology Graduate Group; Univ. of California, Davis, CA (United States). Dept. of Food Science and Technology

Yersinia enterocolitica biovar 1B maintains two type III secretion systems (T3SS) that are involved in pathogenesis, the plasmid encoded Ysc T3SS and the chromosomally encoded Ysa T3SS. In vitro, the Ysa T3SS has been shown to be expressed only at 26°C in a high-nutrient medium containing an exceptionally high concentration of salt – an artificial condition that provides no clear insight on the nature of signal that Y. enterocolitica responds to in a host. However, previous research has indicated that the Ysa system plays a role in the colonization of gastrointestinal tissues of mice. In this study, a series of Ysa promoter fusions to green fluorescent protein gene (gƒp) were created to analyze the expression of this T3SS during infection. Using reporter strains, infections were carried out in vitro using HeLa cells and in vivo using the mouse model of yersiniosis. Expression of green fluorescent protein (GFP) was measured from the promoters of yspP (encoding a secreted effector protein) and orƒ6 (encoding a structural component of the T3SS apparatus) in vitro and in vivo. During the infection of HeLa cells GFP intensity was measured by fluorescence microscopy, while during murine infections GFP expression in tissues was measured by flow cytometry. These approaches, combined with quantification of yspP mRNA transcripts by quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR), demonstrate that the Ysa system is expressed in vitro in a contactdependent manner, and is expressed in vivo during infection of mice.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL-CA), Livermore, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: NA0003525

OSTI ID:: 1623571

Journal Information:: MicrobiologyOpen, Journal Name: MicrobiologyOpen Journal Issue: 6 Vol. 2; ISSN 2045-8827

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

Characterization of the ysa Pathogenicity Locus in the Chromosome of Yersinia enterocolitica and Phylogeny Analysis of Type III Secretion Systems Foultier, Boris; Troisfontaines, Paul; Müller, Simone Journal of Molecular Evolution, Vol. 55, Issue 1 https://doi.org/10.1007/s00239-001-0089-7	journal	July 2002
Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R−M+ mutant Kinder, Susan A.; Badger, Julie L.; Bryant, Gene O. Gene, Vol. 136, Issue 1-2 https://doi.org/10.1016/0378-1119(93)90478-l	journal	December 1993
Yersinia enterocolitica: overview and epidemiologic correlates Bottone, Edward J. Microbes and Infection, Vol. 1, Issue 4 https://doi.org/10.1016/s1286-4579(99)80028-8	journal	April 1999
The Yersinia Ysc–Yop 'Type III' weaponry Cornelis, Guy R. Nature Reviews Molecular Cell Biology, Vol. 3, Issue 10 https://doi.org/10.1038/nrm932	journal	October 2002
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
Co-ordinate, temperature-sensitive regulation of the three Yersinia enterocolitica flagellin genes Kapatral, Vinayak; Minnich, Scott A. Molecular Microbiology, Vol. 17, Issue 1 https://doi.org/10.1111/j.1365-2958.1995.mmi_17010049.x	journal	July 1995
Molecular genetic bases of Salmonella entry into host cells Galán, Jorge E. Molecular Microbiology, Vol. 20, Issue 2 https://doi.org/10.1111/j.1365-2958.1996.tb02615.x	journal	April 1996
In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted Cummings, Lisa A.; Wilkerson, W. David; Bergsbaken, Tessa Molecular Microbiology, Vol. 61, Issue 3 https://doi.org/10.1111/j.1365-2958.2006.05271.x	journal	August 2006
Contribution of BlaA and BlaB -Lactamases to Antibiotic Susceptibility of Yersinia enterocolitica Biovar 1B Bent, Z. W.; Young, G. M. Antimicrobial Agents and Chemotherapy, Vol. 54, Issue 9 https://doi.org/10.1128/aac.01754-09	journal	June 2010
Pathogenecity of Yersinia enterocolitica for mice. Carter, P. B. Infection and Immunity, Vol. 11, Issue 1 https://doi.org/10.1128/iai.11.1.164-170.1975	journal	January 1975
Characteristics of virulence in human isolates of Yersinia enterocolitica. Schiemann, D. A.; Devenish, J. A.; Toma, S. Infection and Immunity, Vol. 32, Issue 1 https://doi.org/10.1128/iai.32.1.400-403.1981	journal	January 1981
HeLa cell infection by Yersinia enterocolitica: evidence for lack of intracellular multiplication and development of a new procedure for quantitative expression of infectivity. Devenish, J. A.; Schiemann, D. A. Infection and Immunity, Vol. 32, Issue 1 https://doi.org/10.1128/iai.32.1.48-55.1981	journal	January 1981
Secretion of Shigella flexneri Ipa invasins on contact with epithelial cells and subsequent entry of the bacterium into cells are growth stage dependent. Mounier, J.; Bahrani, F. K.; Sansonetti, P. J. Infection and immunity, Vol. 65, Issue 2 https://doi.org/10.1128/iai.65.2.774-782.1997	journal	January 1997
Novel Virulence-Associated Type II Secretion System Unique to High-Pathogenicity Yersinia enterocolitica Iwobi, A.; Heesemann, J.; Garcia, E. Infection and Immunity, Vol. 71, Issue 4 https://doi.org/10.1128/iai.71.4.1872-1879.2003	journal	April 2003
Environmental Regulation and Virulence Attributes of the Ysa Type III Secretion System of Yersinia enterocolitica Biovar 1B Venecia, K.; Young, G. M. Infection and Immunity, Vol. 73, Issue 9 https://doi.org/10.1128/iai.73.9.5961-5977.2005	journal	August 2005
Synchronous Gene Expression of the Yersinia enterocolitica Ysa Type III Secretion System and Its Effectors Walker, Kimberly A.; Miller, Virginia L. Journal of Bacteriology, Vol. 191, Issue 6 https://doi.org/10.1128/jb.01402-08	journal	January 2009
The Yersinia enterocolitica pYV Virulence Plasmid Contains Multiple Intrinsic DNA Bends Which Melt at 37°C Rohde, John R.; Luan, Xing-she; Rohde, Harold Journal of Bacteriology, Vol. 181, Issue 14 https://doi.org/10.1128/jb.181.14.4198-4204.1999	journal	July 1999
Ferric Enterochelin Transport in Yersinia enterocolitica: Molecular and Evolutionary Aspects Schubert, S.; Fischer, D.; Heesemann, J. Journal of Bacteriology, Vol. 181, Issue 20 https://doi.org/10.1128/jb.181.20.6387-6395.1999	journal	October 1999
The Yersinia enterocoliticaPhospholipase Gene yplA Is Part of the Flagellar Regulon Schmiel, Deborah H.; Young, Glenn M.; Miller, Virginia L. Journal of Bacteriology, Vol. 182, Issue 8 https://doi.org/10.1128/jb.182.8.2314-2320.2000	journal	April 2000
Regulation of the Ysa Type III Secretion System of Yersinia enterocolitica by YsaE/SycB and YsrS/YsrR Walker, Kimberly A.; Miller, Virginia L. Journal of Bacteriology, Vol. 186, Issue 13 https://doi.org/10.1128/jb.186.13.4056-4066.2004	journal	July 2004
Application of Comparative Phylogenomics To Study the Evolution of Yersinia enterocolitica and To Identify Genetic Differences Relating to Pathogenicity Howard, S. L.; Gaunt, M. W.; Hinds, J. Journal of Bacteriology, Vol. 188, Issue 10 https://doi.org/10.1128/jb.188.10.3645-3653.2006	journal	May 2006
The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia enterocolitica Strain 8081 Thomson, Nicholas R.; Howard, Sarah; Wren, Brendan W. PLoS Genetics, Vol. 2, Issue 12 https://doi.org/10.1371/journal.pgen.0020206	journal	January 2006
Yersinia Has a Tropism for B and T Cell Zones of Lymph Nodes That Is Independent of the Type III Secretion System Balada-Llasat, Joan-Miquel; Mecsas, Joan PLoS Pathogens, Vol. 2, Issue 9 https://doi.org/10.1371/journal.ppat.0020086	journal	September 2006
Concerted Actions of a Thermo-labile Regulator and a Unique Intergenic RNA Thermosensor Control Yersinia Virulence Böhme, Katja; Steinmann, Rebekka; Kortmann, Jens PLoS Pathogens, Vol. 8, Issue 2 https://doi.org/10.1371/journal.ppat.1002518	journal	February 2012
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Environmental Stimuli Affecting Expression of the Ysa Type Three Secretion Locus Mildiner-Earley, Shirly; Miller, Virginia L.; Walker, Kimberly A. Advances In Experimental Medicine And Biology https://doi.org/10.1007/978-0-387-72124-8_18	book	January 2007
Yersinia enterocolitica No authors listed Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz https://doi.org/10.1007/978-3-662-38283-7_108	book	January 1999
Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R−M+ mutant Kinder, Susan A.; Badger, Julie L.; Bryant, Gene O. Gene, Vol. 136, Issue 1-2 https://doi.org/10.1016/0378-1119(93)90478-L	journal	December 1993
Yersinia enterocolitica: overview and epidemiologic correlates Bottone, Edward J. Microbes and Infection, Vol. 1, Issue 4 https://doi.org/10.1016/S1286-4579(99)80028-8	journal	April 1999
Yersinia enterocolitica Fredriksson-Ahomaa, M. Foodborne Diseases https://doi.org/10.1016/b978-0-12-385007-2.00009-7	book	February 2017
Yersinia enterocolitica Marsicano, Elizabeth; Jani, Bhairvi; Narayanan, Mey Encyclopedia of Gastroenterology https://doi.org/10.1016/b978-0-12-801238-3.65974-3	book	November 2019
Identification of host-induced pathogen genes by differential fluorescence induction reporter systems Bumann, Dirk; Valdivia, Raphael H. Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.78	journal	April 2007
A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence: Yersinia enterocolitica chromosomal type III secretion Haller, Jon C.; Carlson, Sharon; Pederson, Kristin J. Molecular Microbiology, Vol. 36, Issue 6 https://doi.org/10.1046/j.1365-2958.2000.01964.x	journal	June 2000
Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry: Salmonella gene expression in a mammalian host Bumann, Dirk Molecular Microbiology, Vol. 43, Issue 5 https://doi.org/10.1046/j.1365-2958.2002.02821.x	journal	March 2002
A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence Haller, Jon C.; Carlson, Sharon; Pederson, Kristin J. Molecular Microbiology, Vol. 44, Issue 2 https://doi.org/10.1046/j.1365-2958.2002.02893.x	journal	April 2002
Yersinia Enterocolitica Cover, Timothy L.; Aber, Robert C. New England Journal of Medicine, Vol. 321, Issue 1 https://doi.org/10.1056/NEJM198907063210104	journal	July 1989
Population-Based Incidence of Infection With Selected Bacterial Enteric Pathogens in Children Younger Than Five Years of Age, 1996???1998 Koehler, Kathleen M.; Lasky, Tamar; Fein, Sara B. The Pediatric Infectious Disease Journal, Vol. 25, Issue 2 https://doi.org/10.1097/01.inf.0000199289.62733.d5	journal	January 2006
Proteomic and functional analysis of the suite of Ysp proteins exported by the Ysa type III secretion system of Yersinia enterocolitica Biovar 1B: Ysps secreted by the Ysa type III secretion system Matsumoto, Hiroyuki; Young, Glenn M. Molecular Microbiology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1365-2958.2005.04973.x	journal	November 2005
Contribution of BlaA and BlaB -Lactamases to Antibiotic Susceptibility of Yersinia enterocolitica Biovar 1B Bent, Z. W.; Young, G. M. Antimicrobial Agents and Chemotherapy, Vol. 54, Issue 9 https://doi.org/10.1128/AAC.01754-09	journal	June 2010
A Phenotype at Last: Essential Role for the Yersinia enterocolitica Ysa Type III Secretion System in a Drosophila melanogaster S2 Cell Model Walker, Kimberly A.; Maltez, Vivien I.; Hall, Joshua D. Infection and Immunity, Vol. 81, Issue 7 https://doi.org/10.1128/IAI.01454-12	journal	April 2013
Pathogenecity of Yersinia enterocolitica for mice. Carter, P. B. Infection and Immunity, Vol. 11, Issue 1 https://doi.org/10.1128/IAI.11.1.164-170.1975	journal	January 1975
Characteristics of virulence in human isolates of Yersinia enterocolitica. Schiemann, D. A.; Devenish, J. A.; Toma, S. Infection and Immunity, Vol. 32, Issue 1 https://doi.org/10.1128/IAI.32.1.400-403.1981	journal	January 1981
HeLa cell infection by Yersinia enterocolitica: evidence for lack of intracellular multiplication and development of a new procedure for quantitative expression of infectivity. Devenish, J. A.; Schiemann, D. A. Infection and Immunity, Vol. 32, Issue 1 https://doi.org/10.1128/IAI.32.1.48-55.1981	journal	January 1981
Secretion of Shigella flexneri Ipa invasins on contact with epithelial cells and subsequent entry of the bacterium into cells are growth stage dependent. Mounier, J.; Bahrani, F. K.; Sansonetti, P. J. Infection and immunity, Vol. 65, Issue 2 https://doi.org/10.1128/IAI.65.2.774-782.1997	journal	January 1997
Novel Virulence-Associated Type II Secretion System Unique to High-Pathogenicity Yersinia enterocolitica Iwobi, A.; Heesemann, J.; Garcia, E. Infection and Immunity, Vol. 71, Issue 4 https://doi.org/10.1128/IAI.71.4.1872-1879.2003	journal	April 2003
YAPI, a New Yersinia pseudotuberculosis Pathogenicity Island Collyn, F.; Billault, A.; Mullet, C. Infection and Immunity, Vol. 72, Issue 8 https://doi.org/10.1128/IAI.72.8.4784-4790.2004	journal	July 2004
Environmental Regulation and Virulence Attributes of the Ysa Type III Secretion System of Yersinia enterocolitica Biovar 1B Venecia, K.; Young, G. M. Infection and Immunity, Vol. 73, Issue 9 https://doi.org/10.1128/IAI.73.9.5961-5977.2005	journal	August 2005
Identification of YsrT and Evidence that YsrRST Constitute a Unique Phosphorelay System in Yersinia enterocolitica Walker, Kimberly A.; Obrist, Markus W.; Mildiner-Earley, Shirly Journal of Bacteriology, Vol. 192, Issue 22 https://doi.org/10.1128/JB.00745-10	journal	September 2010
Synchronous Gene Expression of the Yersinia enterocolitica Ysa Type III Secretion System and Its Effectors Walker, Kimberly A.; Miller, Virginia L. Journal of Bacteriology, Vol. 191, Issue 6 https://doi.org/10.1128/JB.01402-08	journal	January 2009
The Yersinia enterocolitica pYV Virulence Plasmid Contains Multiple Intrinsic DNA Bends Which Melt at 37°C Rohde, John R.; Luan, Xing-she; Rohde, Harold Journal of Bacteriology, Vol. 181, Issue 14 https://doi.org/10.1128/JB.181.14.4198-4204.1999	journal	July 1999
Ferric Enterochelin Transport in Yersinia enterocolitica: Molecular and Evolutionary Aspects Schubert, S.; Fischer, D.; Heesemann, J. Journal of Bacteriology, Vol. 181, Issue 20 https://doi.org/10.1128/JB.181.20.6387-6395.1999	journal	October 1999
The Yersinia enterocoliticaPhospholipase Gene yplA Is Part of the Flagellar Regulon Schmiel, Deborah H.; Young, Glenn M.; Miller, Virginia L. Journal of Bacteriology, Vol. 182, Issue 8 https://doi.org/10.1128/JB.182.8.2314-2320.2000	journal	April 2000
YplA Is Exported by the Ysc, Ysa, and Flagellar Type III Secretion Systems of Yersinia enterocolitica Young, B. M.; Young, G. M. Journal of Bacteriology, Vol. 184, Issue 5 https://doi.org/10.1128/JB.184.5.1324-1334.2002	journal	March 2002
Regulation of the Ysa Type III Secretion System of Yersinia enterocolitica by YsaE/SycB and YsrS/YsrR Walker, Kimberly A.; Miller, Virginia L. Journal of Bacteriology, Vol. 186, Issue 13 https://doi.org/10.1128/JB.186.13.4056-4066.2004	journal	July 2004
Application of Comparative Phylogenomics To Study the Evolution of Yersinia enterocolitica and To Identify Genetic Differences Relating to Pathogenicity Howard, S. L.; Gaunt, M. W.; Hinds, J. Journal of Bacteriology, Vol. 188, Issue 10 https://doi.org/10.1128/JB.188.10.3645-3653.2006	journal	May 2006
Yersinia enterocolitica Bottone, Edward J. https://doi.org/10.1201/9781351077804	book	January 1981
A Phenotype at Last: Essential Role for the Yersinia enterocolitica Ysa Type III Secretion System in a Drosophila melanogaster S2 Cell Model D., Hall, Joshua; I., Maltez, Vivien; A., Walker, Kimberly The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/f1sv-8w77	text	January 2013
Клинический случай генерализованной инфекции, вызванной Yersinia enterocolitica, у подростка Романовская, О. Ф.; Адамович, О. Л.; Романова, О. Н. Клиническая инфектология и паразитология https://doi.org/10.34883/pi.2020.9.1.010	text	January 2020

Cited By (1)

Applications of Flow Cytometry to Characterize Bacterial Physiological Responses Ambriz-Aviña, Verónica; Contreras-Garduño, Jorge A.; Pedraza-Reyes, Mario BioMed Research International, Vol. 2014 https://doi.org/10.1155/2014/461941	journal	January 2014

Similar Records

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

Journal Article · Sun Apr 19 20:00:00 EDT 2015 · Infection and Immunity · OSTI ID:1235333

Crystal structure of the Yersinia type III secretion protein YscE

Journal Article · Sun Dec 05 23:00:00 EST 2010 · Protein Sci. · OSTI ID:1008636

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

Journal Article · Thu Mar 29 20:00:00 EDT 2012 · PLoS ONE · OSTI ID:1627507

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
In vivo expression
Microbiology
T3SS
Y. enterocolitica
Ysa
Ysp

The Yersinia enterocolitica Ysa type III secretion system is expressed during infections both in vitro and in vivo

Citation Formats

References (58)

Cited By (1)

Similar Records

Related Subjects