Unusual, Virulence Plasmid-Dependent Growth Behavior of Yersinia enterocolitica in Three-Dimensional Collagen Gels
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As a first approach to establishing a three-dimensional culture infection model, we studied the growth behavior of the extracellular pathogen Yersinia enterocolitica in three-dimensional collagen gels (3D-CoG). Surprisingly, we observed that plasmidless Y. enterocolitica was motile in the 3D-CoG in contrast to its growth in traditional motility agar at 37 degrees C. Motility at 37 degrees C was abrogated in the presence of the virulence plasmid pYV or the exclusive expression of the pYV-located Yersinia adhesion gene yadA. YadA-producing yersiniae formed densely packed (dp) microcolonies, whereas pYVDelta yadA-carrying yersiniae formed loosely packed microcolonies at 37 degrees C in 3D-CoG. Furthermore, we demonstrated that the packing density of the microcolonies was dependent on the head domain of YadA. Moreover, dp microcolony formation did not depend on the capacity of YadA to bind to collagen fibers, as demonstrated by the use of yersiniae producing collagen nonbinding YadA. By using a yopE-gfp reporter, we demonstrated Ca(2+)-dependent expression of this pYV-localized virulence gene by yersiniae in 3D-CoG. In conclusion, this study revealed unique plasmid-dependent growth behavior of yersiniae in a three-dimensional matrix environment that resembles the behavior of yersiniae (e.g., formation of microcolonies) in infected mouse tissue. Thus, this 3D-CoG model may be a first step to a more complex level of in vitro infection models that mimic living tissue, enabling us to study the dynamics of pathogen-host cell interactions.
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YadA is crucial for packing density of microcolonies observed in Y. enterocolitica in collagen gels.
“The Yersinia adhesin YadA is involved in autoaggregation [9] and is crucial for the packing density of microcolonies observed in Y. enterocolitica in collagen gels [145].”
From Bacterial autoaggregation (2018) · cites this paper as [145]
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Cites
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko, K., & Wanner, B. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.120163297 · Cited by 15,902 · see citing works
The biology of cell locomotion within three-dimensional extracellular matrix
Friedl, P., & Br�cker, E.-B. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050498 · Cited by 651 · see citing works
YERSINIA OUTER PROTEINS: Role in Modulation of Host Cell Signaling Responses and Pathogenesis
Viboud, G. I., & Bliska, J. B. (2005) · Annual Review of Microbiology · doi:10.1146/annurev.micro.59.030804.121320 · Cited by 600 · see citing works
The Yersinia Ysc–Yop 'Type III' weaponry
Cornelis, G. R. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm932 · Cited by 426 · see citing works
Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A., & Heesemann, J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.22.5989 · Cited by 359 · see citing works
Self-citationDavis, G. E., & Camarillo, C. W. (1996) · Experimental Cell Research · doi:10.1006/excr.1996.0109 · Cited by 355 · see citing works
Bölin, I., Norlander, L., & Wolf‐Watz, H. (1982) · Infection and Immunity · doi:10.1128/iai.37.2.506-512.1982 · Cited by 299 · see citing works
Grützkau, A., HANSKI, C., Hahn, H. H., & Riecken, E. O. (1990) · Gut · doi:10.1136/gut.31.9.1011 · Cited by 265 · see citing works
YadA, the multifaceted adhesin
ELTAHIR, Y. (2001) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00119 · Cited by 259 · see citing works
Friedl, P., Maaser, K., Klein, C. E., Niggemann, B., Krohne, G., & Zänker, K. S. (1997) · PubMed · Cited by 237 · see citing works
Simonet, M., Richard, S., & Berche, P. (1990) · Infection and Immunity · doi:10.1128/iai.58.3.841-845.1990 · Cited by 220 · see citing works
Molecular Analysis of Transport and Oligomerization of the Yersinia enterocolitica Adhesin YadA
Roggenkamp, A., Ackermann, N., Jacobi, C. A., Trülzsch, K., Hoffmann, H., & Heesemann, J. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.13.3735-3744.2003 · Cited by 209 · see citing works
Self-citationde Rouvroit, C. L., Sluiters, C., & Cornelis, G. R. (1992) · Molecular Microbiology · doi:10.1111/j.1365-2958.1992.tb01483.x · Cited by 202 · see citing works
Heesemann, J., Groß, U., Schmidt, N., & Laufs, R. (1986) · Infection and Immunity · doi:10.1128/iai.54.2.561-567.1986 · Cited by 173 · see citing works
Self-citationTrülzsch, K., Sporleder, T., Igwe, E. I., Rüssmann, H., & Heesemann, J. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5227-5234.2004 · Cited by 172 · see citing works
Self-citationVirulence plasmid-associated autoagglutination in Yersinia spp
Skurnik, M., Bölin, I., Heikkinen, H., Piha, S., & Wolf-Watz, H. (1984) · Journal of Bacteriology · doi:10.1128/jb.158.3.1033-1036.1984 · Cited by 160 · see citing works
Construction of a mobilizable Yersinia enterocolitica virulence plasmid
Heesemann, J., & Laufs, R. (1983) · Journal of Bacteriology · doi:10.1128/jb.155.2.761-767.1983 · Cited by 159 · see citing works
Self-citationRuckdeschel, K., Roggenkamp, A., Schubert, S., & Heesemann, J. (1996) · Infection and Immunity · doi:10.1128/iai.64.3.724-733.1996 · Cited by 156 · see citing works
Self-citationQuorum Sensing inYersinia enterocoliticaControls Swimming and Swarming Motility
Atkinson, S., Chang, C., Sockett, R. E., Cámara, M., & Williams, P. M. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.4.1451-1461.2006 · Cited by 149 · see citing works
Eitel, J., & Dersch, P. (2002) · Infection and Immunity · doi:10.1128/iai.70.9.4880-4891.2002 · Cited by 145 · see citing works
Cornelis, G. R., Vanootegem, J.-C., & Sluiters, C. (1987) · Microbial Pathogenesis · doi:10.1016/0882-4010(87)90078-7 · Cited by 140 · see citing works
Straley, S. C., & Brubaker, R. R. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.2.1224 · Cited by 130 · see citing works
Roggenkamp, A., NEUBERGER, H., Flügel, A., Schmoll, T., & Heesemann, J. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02343.x · Cited by 124 · see citing works
Self-citationYersinia's stratagem: targeting innate and adaptive immune defense
Heesemann, J., Sing, A., & Trülzsch, K. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.10.018 · Cited by 115 · see citing works
Self-citationThe Yersinia high-pathogenicity island (HPI): evolutionary and functional aspects
Schubert, S., Rakin, A., & Heesemann, J. (2004) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2004.06.026 · Cited by 112 · see citing works
Self-citationBehnsen, J., Narang, P., Hasenberg, M., Gunzer, F., Bilitewski, U., Klippel, N., Rohde, M., Brock, M., Brakhage, A. A., & Gunzer, M. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030013 · Cited by 110 · see citing works
Wilharm, G., Lehmann, V., Krauss, K., Lehnert, B., Susanna, R., Ruckdeschel, K., Heesemann, J., & Trülzsch, K. (2004) · Infection and Immunity · doi:10.1128/iai.72.7.4004-4009.2004 · Cited by 108 · see citing works
Self-citationThe Myf fibrillae of Yersinia enterocolitica
Iriarte, M., Vanooteghem, J. ‐., Delor, I., Díaz, R., Knutton, S., & Cornelis, G. R. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01712.x · Cited by 99 · see citing works
Jacobi, C. A., Roggenkamp, A., Rakin, A., Zumbihl, R., Leitritz, L., & Heesemann, J. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01128.x · Cited by 98 · see citing works
Self-citationMechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3
Pilz, D., Vocke, T., Heesemann, J., & Brade, V. (1992) · Infection and Immunity · doi:10.1128/iai.60.1.189-195.1992 · Cited by 96 · see citing works
Self-citationGunzer, M., Friedl, P., Niggemann, B., Bröcker, E., Kämpgen, E., & Zänker, K. S. (2000) · Journal of Leukocyte Biology · doi:10.1002/jlb.67.5.622 · Cited by 83 · see citing works
Yersinia enterocolitica Infection of Mice Reveals Clonal Invasion and Abscess Formation
Oellerich, M. F., Jacobi, C. A., Freund, S., Niedung, K., Bach, A., Heesemann, J., & Trülzsch, K. (2007) · Infection and Immunity · doi:10.1128/iai.00419-07 · Cited by 76 · see citing works
Self-citationCo‐ordinate, temperature‐sensitive regulation of the three Yersinia enterocolitica flagellin genes
Kapatral, V., & Minnich, S. A. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_17010049.x · Cited by 64 · see citing works
Eitel, J., Heise, T., Thiesen, U., & Dersch, P. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00434.x · Cited by 63 · see citing works
Bleves, S., Marenne, M.-N., Detry, G., & Cornelis, G. R. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.12.3214-3223.2002 · Cited by 60 · see citing works
Roggenkamp, A., Ruckdeschel, K., Leitritz, L., Schmitt, R., & Heesemann, J. (1996) · Infection and Immunity · doi:10.1128/iai.64.7.2506-2514.1996 · Cited by 59 · see citing works
Self-citationModulation of Rho GTPases and the actin cytoskeleton by Yersinia outer proteins (Yops)
Aepfelbacher, M., & Heesemann, J. (2001) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00130 · Cited by 49 · see citing works
Self-citationHudson, K. J., Bliska, J. B., & Bouton, A. H. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00571.x · Cited by 47 · see citing works
Visser, L. G., Hiemstra, P. S., van den Barselaar, M. T., Ballieux, P. A., & van Furth, R. (1996) · Infection and Immunity · doi:10.1128/iai.64.5.1653-1658.1996 · Cited by 47 · see citing works
Jacobi, C. A., Gregor, S., Rakin, A., & Heesemann, J. (2001) · Infection and Immunity · doi:10.1128/iai.69.12.7772-7782.2001 · Cited by 35 · see citing works
Self-citationBalkovetz, D. F. (1998) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19981201)43:5 · Cited by 27 · see citing works
Pérez-Gutiérrez, C., Llompart, C. M., Skurnik, M., & Bengoechea, J. A. (2006) · Infection and Immunity · doi:10.1128/iai.00942-06 · Cited by 24 · see citing works
Roggenkamp, A., Schubert, S., Jacobi, C. A., & Heesemann, J. (1995) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1995.tb07916.x · Cited by 22 · see citing works
Self-citationJacobi, C. A. (2006) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.4807 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [2]Atkinson, S., C. Y. Chang, R. E. Sockett, M. Camara, and P. Williams. 2006. Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J. Bacteriol. 1881451-1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [4]Bleves, S., M. N. Marenne, G. Detry, and G. R. Cornelis. 2002. Up-regulation of the Yersinia enterocolitica yop regulon by deletion of the flagellum master operon flhDC. J. Bacteriol. 1843214-3223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [15]Friedl, P., K. S. Zanker, and E. B. Brocker. 1998. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 43369-378. [DOI] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Trunk, T., Bacterial Cell Surface Group, S. F. G. A. E. B., S. Khalil, H., & C. Leo, J. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.140 · Cited by 444 · see citing works
Barrila, J., Radtke, A. L., Crabbé, A., Sarker, S. F., Herbst-Kralovetz, M. M., Ott, C. M., & Nickerson, C. A. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2423 · Cited by 302 · see citing works
An in vitro model of bacterial infections in wounds and other soft tissues
Werthén, M., Henriksson, L., Jensen, P. Ø., Sternberg, C., Givskov, M., & Bjarnsholt, T. (2010) · Apmis · doi:10.1111/j.1600-0463.2009.02580.x · Cited by 136 · see citing works
Guggenberger, C., Wolz, C., Morrissey, J. A., & Heesemann, J. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002434 · Cited by 100 · see citing works
Self-citationThe Most Important Virulence Markers of Yersinia enterocolitica and Their Role during Infection
Bancerz‐Kisiel, A., Pieczywek, M., Łada, P., & Szweda, W. (2018) · Genes · doi:10.3390/genes9050235 · Cited by 85 · see citing works
Evolution of Cryptosporidium in vitro culture
Karanis, P., & Aldeyarbi, H. M. (2011) · International Journal for Parasitology · doi:10.1016/j.ijpara.2011.08.001 · Cited by 78 · see citing works
Adhesins of Human Pathogens from the Genus Yersinia
Leo, J. C., & Skurnik, M. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-0940-9_1 · Cited by 72 · see citing works
Trimer Stability of YadA Is Critical for Virulence of Yersinia enterocolitica
Schütz, M. S., Weiss, E., Schindler, M. K. H., Hallström, T., Zipfel, P. F., Linke, D., & Autenrieth, I. B. (2010) · Infection and Immunity · doi:10.1128/iai.01350-09 · Cited by 44 · see citing works
Leo, J. C., Elovaara, H., Bihan, D. G., Pugh, N., Kilpinen, S. K., Raynal, N., Skurnik, M., Farndale, R. W., & Goldman, A. (2010) · Infection and Immunity · doi:10.1128/iai.01057-09 · Cited by 43 · see citing works
Yersinia enterocolitica: A Dangerous, But Often Ignored, Foodborne Pathogen
Zadernowska, A., Chajęcka‐Wierzchowska, W., & Łaniewska‐Trokenheim, Ł. (2013) · Food Reviews International · doi:10.1080/87559129.2013.853775 · Cited by 35 · see citing works
Kakoschke, T. K., Kakoschke, S. C., Zeuzem, C., Bouabe, H., Adler, K., Heesemann, J., & Rossier, O. (2016) · Scientific Reports · doi:10.1038/srep29275 · Cited by 31 · see citing works
Self-citationStrategies used by Yersinia enterocolitica to evade killing by the host: thinking beyond Yops
Dhar, M. S., & Virdi, J. S. (2013) · Microbes and Infection · doi:10.1016/j.micinf.2013.11.002 · Cited by 25 · see citing works
Whelan, R., McVicker, G., & Leo, J. C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114102 · Cited by 18 · see citing works
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Clark, S. A., Thibault, D. M., Shull, L. M., Davis, K. M., Aunins, E., van Opijnen, T., & Isberg, R. R. (2020) · eLife · doi:10.7554/elife.58106 · Cited by 5 · see citing works
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- Authors
- Freund, S., Czech, B., Trülzsch, K., Ackermann, N., & Heesemann, J.
- Affiliations
- Max-von-Pettenkofer-Institut für Hygiene und Medizinische Mikrobiologie (DE)
- Max von Pettenkofer Institute for Hygiene and Medical Microbiology, Ludwig Maximilians University, D-80336 Munich, Germany
- Corresponding author
- Freund, Sandra
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2008-06-15
- Volume
- 190
- Issue
- 12
- Pages
- 4111-4120
- ISSN
- 0021-9193 (ISSN-L)
- 1098-5530
- PMC
- PMC2446754
- OpenAlex
- W2109033272
- Cited by
- 31
- References
- 44
- Citations by year
- 2024: 9 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 1 · 2014: 2 · 2013: 2 · 2012: 1
- FWCI
- 1.90
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Bacteriology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Yersinia bacterium, plague, ectoparasites research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- Yersinia enterocolitica, YadA, three-dimensional collagen gel, microcolony formation, bacterial motility, YopE, collagen binding, infection model, host-pathogen interaction
- MeSH terms
- Bacterial Outer Membrane Proteins, Bacterial Proteins, Collagen, Electrophoresis, Polyacrylamide Gel, Gels, Plasmids, Virulence, Yersinia enterocolitica, Polymerase Chain Reaction, Adhesins, Bacterial, Microscopy, Electron, Transmission
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