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Toxins
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Toxins and Virulence Factors of Listeria monocytogenes
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Toxins and Virulence Factors of Listeria monocytogenes

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Bacterial Toxins".

Deadline for manuscript submissions: closed (15 April 2020) | Viewed by 49896

Special Issue Editors

Dr. Didier Cabanes

E-Mail Website
Guest Editor
Group of Molecular Microbiology, i3S-Instituto de Investigação e Inovação em Saúde, IBMC, Universidade do Porto, 4200-135 Porto, Portugal
Interests: host-pathogen interactions; bacterial virulence factors; bacterial pore forming toxins; Listeria monocytogenes
Dr. Sandra Sousa

E-Mail Website
Guest Editor
Group of Cell Biology of Bacterial Infections, i3S-Instituto de Investigação e Inovação em Saúde, IBMC, Universidade do Porto, 4200-135 Porto, Portugal
Interests: pore-forming toxins; host cytoskeleton; Listeria monocytogenes; host–pathogen interactions

Special Issue Information

Dear Colleagues,

Listeria monocytogenes is a major intracellular foodborne bacterial pathogen which causes listeriosis, a human systemic infection. Among zoonotic diseases under EU-surveillance, listeriosis is the most severe. L. monocytogenes can grow under temperatures ranging from 0 to 45°C, in acidic medium and at high osmolarity; conditions that it may encounter in nature, in the food chain, as well as during infection. L. monocytogenes has the capacity to colonize various niches, from inert and organic matrixes to the intestinal lumen where it competes with resident microbiota, translocates across the epithelium, multiplies in phagocytic and non-phagocytic cells, and disseminates via the blood. To adapt and resist to this diversity of environments, L. monocytogenes evolved an arsenal of virulence mechanisms spatially and timely regulated.

Toxins are essential determinants of bacterial virulence. The cholesterol-dependent cytotoxin Listeriolysin O (LLO) is a major L. monocytogenes virulence factor that mediates the escape of bacteria from internalization vacuoles, allowing replication in the cytosol. Other L. monocytogenes toxins have been described to date, including phospholipases (PlcA, PlcB) that contribute to the escape from the endocytic and secondary vacuoles, the thiazole/oxazole-modified toxin Listeriolysin S (LLS) that behaves as a bacteriocin favoring intestinal colonization, or the toxin/antitoxin MazEF involved in growth and survival under stress. In addition, several L. monocytogenes secreted or surface-associated proteins play major roles in virulence.

The L. monocytogenes genome encodes a large number of proteins of still unknown functions; some of them are probably undiscovered virulence factors. This Special Issue focuses on the role of known or new L. monocytogenes determinants acting as offensive or defensive factors but providing benefits to bacterial virulence, with a special emphasis on toxins and secreted or surface proteins. Original research manuscripts, methods, opinions, reviews, and mini reviews are welcome.

Dr. Didier Cabanes
Dr. Sandra Sousa
Guest Editors

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Listeria monocytogenes
  • Toxins
  • Virulence factors
  • Surface proteins
  • Secreted proteins
  • Host-pathogen interactions

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Published Papers (10 papers)

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Research

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14 pages, 2109 KiB  
Article
Listeria monocytogenes Interferes with Host Cell Mitosis through Its Virulence Factors InlC and ActA
by Ana Catarina Costa, Jorge Pinheiro, Sandra A. Reis, Didier Cabanes and Sandra Sousa
Toxins 2020, 12(6), 411; https://doi.org/10.3390/toxins12060411 - 20 Jun 2020
Cited by 8 | Viewed by 4948
Abstract
Listeria monocytogenes is among the best-characterized intracellular pathogens. Its virulence factors, and the way they interfere with host cells to hijack host functions and promote the establishment and dissemination of the infection, have been the focus of multiple studies over the last 30 [...] Read more.
Listeria monocytogenes is among the best-characterized intracellular pathogens. Its virulence factors, and the way they interfere with host cells to hijack host functions and promote the establishment and dissemination of the infection, have been the focus of multiple studies over the last 30 years. During cellular infection, L. monocytogenes was shown to induce host DNA damage and delay the host cell cycle to its own benefit. However, whether the cell cycle stage would interfere with the capacity of Listeria to infect human cultured cell lines was never assessed. We found here that L. monocytogenes preferentially infects cultured cells in G2/M phases. Inside G2/M cells, the bacteria lead to an increase in the overall mitosis duration by delaying the mitotic exit. We showed that L. monocytogenes infection causes a sustained activation of the spindle assembly checkpoint, which we correlated with the increase in the percentage of misaligned chromosomes detected in infected cells. Moreover, we demonstrated that chromosome misalignment in Listeria-infected cells required the function of two Listeria virulence factors, ActA and InlC. Our findings show the pleiotropic role of Listeria virulence factors and their cooperative action in successfully establishing the cellular infection. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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23 pages, 2460 KiB  
Article
The Production of Listeriolysin O and Subsequent Intracellular Infections by Listeria monocytogenes Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
by Erica Rinehart, Julia Chapman and Yvonne Sun
Toxins 2020, 12(4), 218; https://doi.org/10.3390/toxins12040218 - 30 Mar 2020
Cited by 4 | Viewed by 2972
Abstract
Listeria monocytogenes is a foodborne pathogen capable of secreting listeriolysin O (LLO), a pore-forming toxin encoded by the hly gene. While the functions of LLO have been studied extensively, how the production of LLO is modulated by the intestinal environment, devoid of oxygen [...] Read more.
Listeria monocytogenes is a foodborne pathogen capable of secreting listeriolysin O (LLO), a pore-forming toxin encoded by the hly gene. While the functions of LLO have been studied extensively, how the production of LLO is modulated by the intestinal environment, devoid of oxygen and enriched in short chain fatty acids (SCFAs), is not completely understood. Using L. monocytogenes strain 10403s, we found that hly transcription was moderately decreased by aerobic SCFA exposures but significantly increased by anaerobic SCFA exposures. Moreover, aerobic, but not anaerobic, exposure to low levels of SCFAs resulted in a significantly higher LLO activity. These results demonstrated that transcriptional and post-transcriptional regulations of LLO production were separately modulated by SCFAs and were responsive to oxygen levels. Examining isogenic mutants revealed that PrfA and SigB play a role in regulating LLO production in response to SCFAs. Effects of SCFAs were also present in the cardiotropic strain 07PF0776 but distinctly different from those in strain 10403s. For both strains, prior exposures to SCFAs altered intracellular infections in Caco-2 and RAW264.7 cells and the plaque sizes in L fibroblasts, a result confirming the ability of L. monocytogenes to adapt to SCFAs in ways that impact its subsequent infection outcomes. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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11 pages, 2084 KiB  
Article
A Structural Study on the Listeria Monocytogenes Internalin A—Human E-cadherin Interaction: A Molecular Tool to Investigate the Effects of Missense Mutations
by Luca Dellafiora, Virginia Filipello, Chiara Dall’Asta, Guido Finazzi, Gianni Galaverna and Marina Nadia Losio
Toxins 2020, 12(1), 60; https://doi.org/10.3390/toxins12010060 - 20 Jan 2020
Cited by 8 | Viewed by 4320
Abstract
Listeria monocytogenes is a widespread foodborne pathogen of high concern and internalin A is an important virulence factor that mediates cell invasion upon the interaction with the host protein E-cadherin. Nonsense mutations of internalin A are known to reduce virulence. Although missense mutations [...] Read more.
Listeria monocytogenes is a widespread foodborne pathogen of high concern and internalin A is an important virulence factor that mediates cell invasion upon the interaction with the host protein E-cadherin. Nonsense mutations of internalin A are known to reduce virulence. Although missense mutations are largely overlooked, they need to be investigated in respect to their effects in cell invasion processes. This work presented a computational workflow to early characterize internalin A missense mutations. The method reliably estimated the effects of a set of engineered missense mutations in terms of their effects on internalin A–E-cadherin interaction. Then, the effects of mutations of an internalin A variant from a L. monocytogenes isolate were calculated. Mutations showed impairing effects on complex stability providing a mechanistic explanation of the low cells invasion capacity previously observed. Overall, our results provided a rational approach to explain the effects of internalin A missense mutations. Moreover, our findings highlighted that the strength of interaction may not directly relate to the cell invasion capacity reflecting the non-exclusive role of internalin A in determining the virulence of L. monocytogenes. The workflow could be extended to other virulence factors providing a promising platform to support a better molecular understanding of L. monocytogenes epidemiology. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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14 pages, 1553 KiB  
Article
An Inducible Cre-lox System to Analyze the Role of LLO in Listeria monocytogenes Pathogenesis
by Brittney N. Nguyen and Daniel A. Portnoy
Toxins 2020, 12(1), 38; https://doi.org/10.3390/toxins12010038 - 7 Jan 2020
Cited by 11 | Viewed by 4236
Abstract
Listeriolysin O (LLO) is a pore-forming cytolysin that allows Listeria monocytogenes to escape from phagocytic vacuoles and enter the host cell cytosol. LLO is expressed continuously during infection, but it has been a challenge to evaluate the importance of LLO secreted in the [...] Read more.
Listeriolysin O (LLO) is a pore-forming cytolysin that allows Listeria monocytogenes to escape from phagocytic vacuoles and enter the host cell cytosol. LLO is expressed continuously during infection, but it has been a challenge to evaluate the importance of LLO secreted in the host cell cytosol because deletion of the gene encoding LLO (hly) prevents localization of L. monocytogenes to the cytosol. Here, we describe a L. monocytogenes strain (hlyfl) in which hly is flanked by loxP sites and Cre recombinase is under the transcriptional control of the L. monocytogenes actA promoter, which is highly induced in the host cell cytosol. In less than 2 h after infection of bone marrow-derived macrophages (BMMs), bacteria were 100% non-hemolytic. hlyfl grew intracellularly to levels 10-fold greater than wildtype L. monocytogenes and was less cytotoxic. In an intravenous mouse model, 90% of bacteria were non-hemolytic within three hours in the spleen and eight hours in the liver. The loss of LLO led to a 2-log virulence defect in the spleen and a 4-log virulence defect in the liver compared to WT L. monocytogenes. Thus, the production of LLO in the cytosol has significant impact on the pathogenicity of L. monocytogenes. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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14 pages, 4507 KiB  
Article
Large-Scale Comparison of Toxin and Antitoxins in Listeria monocytogenes
by José Antonio Agüero, Hatice Akarsu, Lisandra Aguilar-Bultet, Anna Oevermann and Laurent Falquet
Toxins 2020, 12(1), 29; https://doi.org/10.3390/toxins12010029 - 2 Jan 2020
Cited by 5 | Viewed by 3466
Abstract
Toxin–antitoxin systems (TASs) are widely distributed in prokaryotes and encode pairs of genes involved in many bacterial biological processes and mechanisms, including pathogenesis. The TASs have not been extensively studied in Listeria monocytogenes (Lm), a pathogenic bacterium of the Firmicutes phylum [...] Read more.
Toxin–antitoxin systems (TASs) are widely distributed in prokaryotes and encode pairs of genes involved in many bacterial biological processes and mechanisms, including pathogenesis. The TASs have not been extensively studied in Listeria monocytogenes (Lm), a pathogenic bacterium of the Firmicutes phylum causing infections in animals and humans. Using our recently published TASmania database, we focused on the known and new putative TASs in 352 Listeria monocytogenes genomes and identified the putative core gene TASs (cgTASs) with the Pasteur BIGSdb-Lm database and, by complementarity, the putative accessory gene TAS (acTASs). We combined the cgTASs with those of an additional 227 L. monocytogenes isolates from our previous studies containing metadata information. We discovered that the differences in 14 cgTAS alleles are sufficient to separate the four main lineages of Listeria monocytogenes. Analyzing these differences in more details, we uncovered potentially co-evolving residues in some pairs of proteins in cgTASs, probably essential for protein–protein interactions within the TAS complex. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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18 pages, 1110 KiB  
Article
Validation of Predicted Virulence Factors in Listeria monocytogenes Identified Using Comparative Genomics
by Hossam Abdelhamed, Mark L. Lawrence, Reshma Ramachandran and Attila Karsi
Toxins 2019, 11(9), 508; https://doi.org/10.3390/toxins11090508 - 30 Aug 2019
Cited by 6 | Viewed by 5127
Abstract
Listeria monocytogenes is an intracellular facultative pathogen that causes listeriosis, a foodborne zoonotic infection. There are differences in the pathogenic potential of L. monocytogenes subtypes and strains. Comparison of the genome sequences among L. monocytogenes pathogenic strains EGD-e and F2365 with nonpathogenic L. [...] Read more.
Listeria monocytogenes is an intracellular facultative pathogen that causes listeriosis, a foodborne zoonotic infection. There are differences in the pathogenic potential of L. monocytogenes subtypes and strains. Comparison of the genome sequences among L. monocytogenes pathogenic strains EGD-e and F2365 with nonpathogenic L. innocua CLIP1182 and L. monocytogenes strain HCC23 revealed a set of proteins that were present in pathogenic strains and had no orthologs among the nonpathogenic strains. Among the candidate virulence factors are five proteins: putrescine carbamoyltransferase; InlH/InlC2 family class 1 internalin; phosphotransferase system (PTS) fructose transporter subunit EIIC; putative transketolase; and transcription antiterminator BglG family. To determine if these proteins have a role in adherence and invasion of intestinal epithelial Caco-2 cells and/or contribute to virulence, five mutant strains were constructed. F2365ΔinlC2, F2365Δeiic, and F2365Δtkt exhibited a significant (p < 0.05) reduction in adhesion to Caco-2 cells compared to parent F2365 strain. The invasion of F2365ΔaguB, F2365ΔinlC2, and F2365ΔbglG decreased significantly (p < 0.05) compared with the parent strain. Bacterial loads in mouse liver and spleen infected by F2365 was significantly (p < 0.05) higher than it was for F2365ΔaguB, F2365ΔinlC2, F2365Δeiic, F2365Δtkt, and F2365ΔbglG strains. This study demonstrates that aguB, inlC2, eiic, tkt, and bglG play a role in L. monocytogenes pathogenicity. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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Review

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18 pages, 1223 KiB  
Review
Potential Roles and Functions of Listerial Virulence Factors during Brain Entry
by Franjo Banović, Horst Schroten and Christian Schwerk
Toxins 2020, 12(5), 297; https://doi.org/10.3390/toxins12050297 - 5 May 2020
Cited by 9 | Viewed by 3568
Abstract
Although it rarely induces disease in humans, Listeria monocytogenes (Lm) is important due to the frequency of serious pathological conditions—such as sepsis and meningitis—it causes in those few people that do get infected. Virulence factors (VF) of Lm—especially those involved [...] Read more.
Although it rarely induces disease in humans, Listeria monocytogenes (Lm) is important due to the frequency of serious pathological conditions—such as sepsis and meningitis—it causes in those few people that do get infected. Virulence factors (VF) of Lm—especially those involved in the passage through multiple cellular barriers of the body, including internalin (Inl) family members and listeriolysin O (LLO)—have been investigated both in vitro and in vivo, but the majority of work was focused on the mechanisms utilized during penetration of the gut and fetoplacental barriers. The role of listerial VF during entry into other organs remain as only partially solved puzzles. Here, we review the current knowledge on the entry of Lm into one of its more significant destinations, the brain, with a specific focus on the role of various VF in cellular adhesion and invasion. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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21 pages, 4780 KiB  
Review
Pathogenic Biohacking: Induction, Modulation and Subversion of Host Transcriptional Responses by Listeria monocytogenes
by Matthew J. G. Eldridge, Pascale Cossart and Mélanie A. Hamon
Toxins 2020, 12(5), 294; https://doi.org/10.3390/toxins12050294 - 5 May 2020
Cited by 6 | Viewed by 4640
Abstract
During infection, the foodborne bacterial pathogen Listeria monocytogenes dynamically influences the gene expression profile of host cells. Infection-induced transcriptional changes are a typical feature of the host-response to bacteria and contribute to the activation of protective genes such as inflammatory cytokines. However, by [...] Read more.
During infection, the foodborne bacterial pathogen Listeria monocytogenes dynamically influences the gene expression profile of host cells. Infection-induced transcriptional changes are a typical feature of the host-response to bacteria and contribute to the activation of protective genes such as inflammatory cytokines. However, by using specialized virulence factors, bacterial pathogens can target signaling pathways, transcription factors, and epigenetic mechanisms to alter host gene expression, thereby reprogramming the response to infection. Therefore, the transcriptional profile that is established in the host is delicately balanced between antibacterial responses and pathogenesis, where any change in host gene expression might significantly influence the outcome of infection. In this review, we discuss the known transcriptional and epigenetic processes that are engaged during Listeria monocytogenes infection, the virulence factors that can remodel them, and the impact these processes have on the outcome of infection. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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19 pages, 1356 KiB  
Review
Bacterial Factors Targeting the Nucleus: The Growing Family of Nucleomodulins
by Hélène Bierne and Renaud Pourpre
Toxins 2020, 12(4), 220; https://doi.org/10.3390/toxins12040220 - 31 Mar 2020
Cited by 37 | Viewed by 7273
Abstract
Pathogenic bacteria secrete a variety of proteins that manipulate host cell function by targeting components of the plasma membrane, cytosol, or organelles. In the last decade, several studies identified bacterial factors acting within the nucleus on gene expression or other nuclear processes, which [...] Read more.
Pathogenic bacteria secrete a variety of proteins that manipulate host cell function by targeting components of the plasma membrane, cytosol, or organelles. In the last decade, several studies identified bacterial factors acting within the nucleus on gene expression or other nuclear processes, which has led to the emergence of a new family of effectors called “nucleomodulins”. In human and animal pathogens, Listeria monocytogenes for Gram-positive bacteria and Anaplasma phagocytophilum, Ehrlichia chaffeensis, Chlamydia trachomatis, Legionella pneumophila, Shigella flexneri, and Escherichia coli for Gram-negative bacteria, have led to pioneering discoveries. In this review, we present these paradigms and detail various mechanisms and core elements (e.g., DNA, histones, epigenetic regulators, transcription or splicing factors, signaling proteins) targeted by nucleomodulins. We particularly focus on nucleomodulins interacting with epifactors, such as LntA of Listeria and ankyrin repeat- or tandem repeat-containing effectors of Rickettsiales, and nucleomodulins from various bacterial species acting as post-translational modification enzymes. The study of bacterial nucleomodulins not only generates important knowledge about the control of host responses by microbes but also creates new tools to decipher the dynamic regulations that occur in the nucleus. This research also has potential applications in the field of biotechnology. Finally, this raises questions about the epigenetic effects of infectious diseases. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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Other

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13 pages, 5782 KiB  
Perspective
Bacteriocins of Listeria monocytogenes and Their Potential as a Virulence Factor
by Sangmi Lee
Toxins 2020, 12(2), 103; https://doi.org/10.3390/toxins12020103 - 5 Feb 2020
Cited by 14 | Viewed by 4077
Abstract
Intestinal microbiota exerts protective effects against the infection of various bacterial pathogens, including Listeria monocytogenes, a major foodborne pathogen whose infection can lead to a disease (listeriosis) with a high fatality rate. As a strategy to mitigate the action of the intestinal [...] Read more.
Intestinal microbiota exerts protective effects against the infection of various bacterial pathogens, including Listeria monocytogenes, a major foodborne pathogen whose infection can lead to a disease (listeriosis) with a high fatality rate. As a strategy to mitigate the action of the intestinal microbiota, pathogens often produce antimicrobial proteinaceous compounds such as bacteriocins. In this review, we summarize the information currently available for the well-characterized L. monocytogenes bacteriocin listeriolysin S, with the emphasis on its intriguing mode of action as a virulence factor, which promotes the infection of L. monocytogenes by changing the composition of the intestinal microbiota. We then discuss another intriguing L. monocytogenes bacteriocin Lmo2776 that specifically inhibits the inflammogenic species, Prevotella copri, in the intestinal microbiota, reducing superfluous inflammation while weakening virulence. In addition, we describe relatively less studied phage tail-like Listeria bacteriocins (monocins) and elaborate on the possibility that these monocins could be involved in enhancing pathogenicity. In spite of the burgeoning interest in the roles played by the intestinal microbiota against the L. monocytogenes infection, our understanding on the virulence factors affecting the intestinal microbiota is still lacking, calling for further studies on bacteriocins that could function as novel virulence factors. Full article
(This article belongs to the Special Issue Toxins and Virulence Factors of Listeria monocytogenes)
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