Invasiveness is a variable and heterogeneous phenotype in Listeria monocytogenes serotype strains

Chatterjee, Som Subhra; Otten, Sonja; Hain, Torsten; Lingnau, Andreas; Carl, Uwe D.; Wehland, Jürgen; Domann, Eugen; Chakraborty, Trinad

doi:10.1016/j.ijmm.2005.10.001

Cited by 21 publications

(15 citation statements)

References 38 publications

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“…We plan to test this postulate by searching for protein complexes involving these surface proteins. Our findings are also consistent with studies demonstrating the requirement of other surface proteins besides InlA and InlB for efficient entry of L. monocytogenes into eukaryotic cells (56).…”

Section: Discussionsupporting

confidence: 92%

Association of ActA to Peptidoglycan Revealed by Cell Wall Proteomics of Intracellular Listeria monocytogenes

Portillo

Calvo

D'Orazio

et al. 2011

Journal of Biological Chemistry

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Listeria monocytogenes is a Gram-positive intracellular bacterial pathogen that colonizes the cytosol of eukaryotic cells. Recent transcriptomic studies have revealed that intracellular L. monocytogenes alter expression of genes encoding envelope components. However, no comparative global analysis of this cell wall remodeling process is yet known at the protein level. Here, we used high resolution mass spectrometry to define the cell wall proteome of L. monocytogenes growing inside epithelial cells. When compared with extracellular bacteria growing in a nutrient-rich medium, a major difference found in the proteome was the presence of the actin assembly-inducing protein ActA in peptidoglycan purified from intracellular bacteria. ActA was also identified in the peptidoglycan of extracellular bacteria growing in a chemically defined minimal medium. In this condition, ActA maintains its membrane anchoring domain and promotes efficient bacterial entry into nonphagocytic host cells. Unexpectedly, Internalin-A, which mediates entry of extracellular L. monocytogenes into eukaryotic cells, was identified at late infection times (6 h) as an abundant protein in the cell wall of intracellular bacteria. Other surface proteins covalently bound to the peptidoglycan, as Lmo0514 and Lmo2085, were detected exclusively in intracellular and extracellular bacteria, respectively. Altogether, these data provide the first insights into the changes occurring at the protein level in the L. monocytogenes cell wall as the pathogen transits from the extracellular environment to an intracytosolic lifestyle inside eukaryotic cells. Some of these changes include alterations in the relative amount and the mode of association of certain surface proteins.

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Section: Discussionsupporting

confidence: 92%

Association of ActA to Peptidoglycan Revealed by Cell Wall Proteomics of Intracellular Listeria monocytogenes

Portillo

Calvo

D'Orazio

et al. 2011

Journal of Biological Chemistry

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“…4). These results confirm and extend the findings of others who have also observed variation in inlA transcript levels among and within L. monocytogenes serotypes (11,61).…”

Section: Vol 75 2009 L Monocytogenes Outbreak Strain Virulence Chasupporting

confidence: 92%

“…Although it has been previously observed that L. monocytogenes isolates belonging to different serotypes, including serotype 4b isolates, exhibit heterogeneous abilities to invade human cells (11,61), to our knowledge, this is the first report showing that significant variability in invasion capabilities also exists within epidemic clone strains associated with listeriosis outbreaks. While it could be argued that the consistently low invasion efficiency observed for the four human clinical isolates from listeriosis outbreaks (i.e., CSUFSL N1-008, CSUFSL N1-009, CSUFSL N1-044, and CSUFSL N1-081) is an artifact of laboratory passage, there is no apparent correlation between the invasiveness of a strain and the time since the outbreak (Table 1).…”

Section: Vol 75 2009 L Monocytogenes Outbreak Strain Virulence Chamentioning

confidence: 75%

SomeListeria monocytogenesOutbreak Strains Demonstrate Significantly Reduced Invasion,inlATranscript Levels, and Swarming Motility In Vitro

Roberts

Williams

Wiedmann

et al. 2009

Appl Environ Microbiol

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Listeria monocytogenes can cause a severe invasive food-borne disease known as listeriosis, and large outbreaks of this disease occur occasionally. Based on molecular-subtype data, epidemic clone (EC) strains have been defined, including ECI and ECIa, which have caused listeriosis outbreaks on different continents. While a number of molecular-subtyping studies of outbreak strains have been reported, few comprehensive data sets of virulence-associated characteristics of these strains are available. We assembled a set of human clinical isolates from 15 outbreaks that occurred worldwide between 1975 and 2002. Initial characterization of these strains showed significant variation in the ability to invade human Caco-2 intestinal epithelial cells and HepG2 hepatic cells; four strains showed consistently reduced invasion in both cell lines. DNA sequencing of inlA, which encodes a protein required for efficient Caco-2 and HepG2 invasion, showed that none of the invasion-attenuated strains contained known virulence-attenuating mutations in inlA. Phylogenetic analyses of inlA sequences revealed a well-supported clade containing a fully invasive ECI strain and three invasionattenuated ECI strains, along with a fully invasive ECIa strain and an invasion-attenuated ECIa strain. Of the four invasion-attenuated strains, one strain showed both reduced inlA transcript levels and impaired swarming, one strain showed reduced inlA transcript levels, and two strains showed reduced swarming. Overall, our data show that (i) L. monocytogenes strains from outbreaks vary significantly in invasion efficiency and (ii) different mechanisms may contribute to reduced invasion efficiency. Association between EC strains and listeriosis outbreaks may involve characteristics other than virulence phenotypes, including survival and growth in food-associated environments.

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“…Several studies suggest that other members of the internalin family may modulate L. monocytogenes invasion (Chatterjee et al 2006) by behaving as adhesins, by indirectly affecting the surface exposure of InlA and/or InlB, or by directly interacting with putative novel cellular receptors. For example, expression of the LPXTG-anchored InlJ by L. innocua leads to bacterial adhesion (but no invasion) to human JEG-3 and HT29 polarized epithelial cells , but its potential cell ligand has not been identified yet.…”

Section: Modulation Of Inla-and Inlb-dependent Invasion Pathways By Omentioning

confidence: 99%

Entry of Listeria monocytogenes in Mammalian Epithelial Cells: An Updated View

Pizarro‐Cerdá

Kühbacher

Cossart

2012

Cold Spring Harbor Perspectives in Medicine

226

203

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Listeria monocytogenes is a bacterial pathogen that promotes its internalization into host epithelial cells. Interaction between the bacterial surface molecules InlA and InlB and their cellular receptors E-cadherin and Met, respectively, triggers the recruitment of endocytic effectors, the subversion of the phosphoinositide metabolism, and the remodeling of the actin cytoskeleton that lead to bacterial engulfment. Additional bacterial surface and secreted virulence factors also contribute to entry, albeit to a lesser extent. Here we review the increasing number of signaling effectors that are reported as being subverted by L. monocytogenes during invasion of cultured cell lines. We also update the current knowledge of the early steps of in vivo cellular infection, which, as shown recently, challenges previous concepts generated from in vitro data.

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Invasiveness is a variable and heterogeneous phenotype in Listeria monocytogenes serotype strains

Cited by 21 publications

References 38 publications

Association of ActA to Peptidoglycan Revealed by Cell Wall Proteomics of Intracellular Listeria monocytogenes

Association of ActA to Peptidoglycan Revealed by Cell Wall Proteomics of Intracellular Listeria monocytogenes

SomeListeria monocytogenesOutbreak Strains Demonstrate Significantly Reduced Invasion,inlATranscript Levels, and Swarming Motility In Vitro

Entry of Listeria monocytogenes in Mammalian Epithelial Cells: An Updated View

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