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Microbial Virulence Factors 2.0

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 63083

Special Issue Editor

Special Issue Information

Dear Colleagues,

Microbial virulence factors can be defined as a wide range of molecules produced by pathogenic microbes that enhance their ability to evade their host defenses and cause disease. This broad definition encompasses secreted products such as toxins, enzymes, and exopolysaccharides, but also cell surface structures like capsules, lipopolysaccharides, glyco- and lipoproteins, and intracellular changes in metabolic regulatory networks governed by protein sensors/regulators and noncoding regulatory RNAs. The knowledge, at a molecular level, of the biology of microbial pathogens and their virulence factors is central in the development of novel therapeutic molecules and strategies to combat microbial infections. This is of particular importance in the present days with the worldwide emergence of microbes resistant to available antimicrobials. Advances in recent years in molecular biology, genomic technologies, and bioinformatics have contributed to the molecular identification and functional analyses of microbial virulence factors. This Special Issue of IJMS will be focused on virulence factors and their regulatory networks from microbes such as bacteria, viruses, fungi, and parasites, as well as on the description of innovative experimental techniques to characterize microbial virulence factors. Research papers, up-to-date review articles, and commentaries are all welcome.

Prof. Jorge H. Leitão
Guest Editor

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Keywords

  • Pathogenic bacteria
  • Toxins
  • Bacterial capsules
  • Fungal virulence factors
  • Virus virulence factors
  • Host defense evasion
  • Intracellular survival
  • Virulence determinants
  • Human microbial parasites

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Published Papers (12 papers)

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Research

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15 pages, 5218 KiB  
Article
A Comprehensive Virulence and Resistance Characteristics of Listeria monocytogenes Isolated from Fish and the Fish Industry Environment
by Arkadiusz Józef Zakrzewski, Monika Kurpas, Anna Zadernowska, Wioleta Chajęcka-Wierzchowska and Maria João Fraqueza
Int. J. Mol. Sci. 2023, 24(4), 3581; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24043581 - 10 Feb 2023
Cited by 7 | Viewed by 2510
Abstract
Listeria monocytogenes is an important pathogen, often associated with fish, that can adapt and survive in products and food processing plants, where it can persist for many years. It is a species characterized by diverse genotypic and phenotypic characteristics. Therefore, in this study, [...] Read more.
Listeria monocytogenes is an important pathogen, often associated with fish, that can adapt and survive in products and food processing plants, where it can persist for many years. It is a species characterized by diverse genotypic and phenotypic characteristics. Therefore, in this study, a total of 17 L. monocytogenes strains from fish and fish-processing environments in Poland were characterized for their relatedness, virulence profiles, and resistance genes. The Core Genome Multilocus Sequence Typing (cgMLST) analysis revealed that the most frequent serogroups were IIa and IIb; sequence types (ST) were ST6 and ST121; and clonal complexes (CC) were CC6 and CC121. Core genome multilocus sequence typing (cgMLST) analysis was applied to compare the present isolates with the publicly available genomes of L. monocytogenes strains recovered in Europe from humans with listeriosis. Despite differential genotypic subtypes, most strains had similar antimicrobial resistance profiles; however, some of genes were located on mobile genetic elements that could be transferred to commensal or pathogenic bacteria. The results of this study showed that molecular clones of tested strains were characteristic for L. monocytogenes isolated from similar sources. Nevertheless, it is worth emphasizing that they could present a major public health risk due to their close relation with strains isolated from human listeriosis. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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19 pages, 3988 KiB  
Article
Role of Iron-Containing Alcohol Dehydrogenases in Acinetobacter baumannii ATCC 19606 Stress Resistance and Virulence
by Guang-Huey Lin, Ming-Chuan Hsieh and Hung-Yu Shu
Int. J. Mol. Sci. 2021, 22(18), 9921; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22189921 - 14 Sep 2021
Cited by 13 | Viewed by 3370
Abstract
Most bacteria possess alcohol dehydrogenase (ADH) genes (Adh genes) to mitigate alcohol toxicity, but these genes have functions beyond alcohol degradation. Previous research has shown that ADH can modulate quorum sensing in Acinetobacter baumannii, a rising opportunistic pathogen. However, the number [...] Read more.
Most bacteria possess alcohol dehydrogenase (ADH) genes (Adh genes) to mitigate alcohol toxicity, but these genes have functions beyond alcohol degradation. Previous research has shown that ADH can modulate quorum sensing in Acinetobacter baumannii, a rising opportunistic pathogen. However, the number and nature of Adh genes in A. baumannii have not yet been fully characterized. We identified seven alcohol dehydrogenases (NAD+-ADHs) from A. baumannii ATCC 19606, and examined the roles of three iron-containing ADHs, ADH3, ADH4, and ADH6. Marker-less mutation was used to generate Adh3, Adh4, and Adh6 single, double, and triple mutants. Disrupted Adh4 mutants failed to grow in ethanol-, 1-butanol-, or 1-propanol-containing mediums, and recombinant ADH4 exhibited strongest activity against ethanol. Stress resistance assays with inorganic and organic hydroperoxides showed that Adh3 and Adh6 were key to oxidative stress resistance. Virulence assays performed on the Galleria mellonella model organism revealed that Adh4 mutants had comparable virulence to wild-type, while Adh3 and Adh6 mutants had reduced virulence. The results suggest that ADH4 is primarily involved in alcohol metabolism, while ADH3 and ADH6 are key to stress resistance and virulence. Further investigation into the roles of other ADHs in A. baumannii is warranted. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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18 pages, 2847 KiB  
Article
Omics Analysis of Blood-Responsive Regulon in Bordetella pertussis Identifies a Novel Essential T3SS Substrate
by Jakub Drzmisek, Daniel Stipl, Denisa Petrackova, Branislav Vecerek and Ana Dienstbier
Int. J. Mol. Sci. 2021, 22(2), 736; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22020736 - 13 Jan 2021
Cited by 2 | Viewed by 2099
Abstract
Bacterial pathogens sense specific cues associated with different host niches and integrate these signals to appropriately adjust the global gene expression. Bordetella pertussis is a Gram-negative, strictly human pathogen of the respiratory tract and the etiological agent of whooping cough (pertussis). Though B. [...] Read more.
Bacterial pathogens sense specific cues associated with different host niches and integrate these signals to appropriately adjust the global gene expression. Bordetella pertussis is a Gram-negative, strictly human pathogen of the respiratory tract and the etiological agent of whooping cough (pertussis). Though B. pertussis does not cause invasive infections, previous results indicated that this reemerging pathogen responds to blood exposure. Here, omics RNA-seq and LC–MS/MS techniques were applied to determine the blood-responsive regulon of B. pertussis. These analyses revealed that direct contact with blood rewired global gene expression profiles in B. pertussis as the expression of almost 20% of all genes was significantly modulated. However, upon loss of contact with blood, the majority of blood-specific effects vanished, with the exception of several genes encoding the T3SS-secreted substrates. For the first time, the T3SS regulator BtrA was identified in culture supernatants of B. pertussis. Furthermore, proteomic analysis identified BP2259 protein as a novel secreted T3SS substrate, which is required for T3SS functionality. Collectively, presented data indicate that contact with blood represents an important cue for B. pertussis cells. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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18 pages, 1304 KiB  
Article
Molecular Epidemiology of Enteroaggregative Escherichia coli (EAEC) Isolates of Hospitalized Children from Bolivia Reveal High Heterogeneity and Multidrug-Resistance
by Enrique Joffré and Volga Iñiguez Rojas
Int. J. Mol. Sci. 2020, 21(24), 9543; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21249543 - 15 Dec 2020
Cited by 9 | Viewed by 3487
Abstract
Enteroaggregative Escherichia coli (EAEC) is an emerging pathogen frequently associated with acute diarrhea in children and travelers to endemic regions. EAEC was found the most prevalent bacterial diarrheal pathogen from hospitalized Bolivian children less than five years of age with acute diarrhea from [...] Read more.
Enteroaggregative Escherichia coli (EAEC) is an emerging pathogen frequently associated with acute diarrhea in children and travelers to endemic regions. EAEC was found the most prevalent bacterial diarrheal pathogen from hospitalized Bolivian children less than five years of age with acute diarrhea from 2007 to 2010. Here, we further characterized the epidemiology of EAEC infection, virulence genes, and antimicrobial susceptibility of EAEC isolated from 414 diarrheal and 74 non-diarrheal cases. EAEC isolates were collected and subjected to a PCR-based virulence gene screening of seven virulence genes and a phenotypic resistance test to nine different antimicrobials. Our results showed that atypical EAEC (a-EAEC, AggR-negative) was significantly associated with diarrhea (OR, 1.62, 95% CI, 1.25 to 2.09, p < 0.001) in contrast to typical EAEC (t-EAEC, AggR-positive). EAEC infection was most prevalent among children between 7–12 months of age. The number of cases exhibited a biannual cycle with a major peak during the transition from warm to cold (April–June). Both typical and a-EAEC infections were graded as equally severe; however, t-EAEC harbored more virulence genes. aap, irp2 and pic were the most prevalent genes. Surprisingly, we detected 60% and 52.6% of multidrug resistance (MDR) EAEC among diarrheal and non-diarrheal cases. Resistance to ampicillin, sulfonamides, and tetracyclines was most common, being the corresponding antibiotics, the ones that are frequently used in Bolivia. Our work is the first study that provides comprehensive information on the high heterogenicity of virulence genes in t-EAEC and a- EAEC and the large prevalence of MDR EAEC in Bolivia. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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15 pages, 1380 KiB  
Article
Whole-Genome Sequencing-Based Characterization of Listeria monocytogenes from Fish and Fish Production Environments in Poland
by Kinga Wieczorek, Arkadiusz Bomba and Jacek Osek
Int. J. Mol. Sci. 2020, 21(24), 9419; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21249419 - 10 Dec 2020
Cited by 18 | Viewed by 2407
Abstract
Listeria monocytogenes, an important foodborne pathogen, may be present in different kinds of food and in food processing environments where it can persist for a long time. In this study, 28 L. monocytogenes isolates from fish and fish manufactures were characterized by [...] Read more.
Listeria monocytogenes, an important foodborne pathogen, may be present in different kinds of food and in food processing environments where it can persist for a long time. In this study, 28 L. monocytogenes isolates from fish and fish manufactures were characterized by whole genome sequencing (WGS). Core genome multilocus sequence typing (cgMLST) analysis was applied to compare the present isolates with publicly available genomes of L. monocytogenes strains recovered worldwide from food and from humans with listeriosis. All but one (96.4%) of the examined isolates belonged to molecular serogroup IIa, and one isolate (3.6%) was classified to serogroup IVb. The isolates of group IIa were mainly of MLST sequence types ST121 (13 strains) and ST8 (four strains) whereas the isolate of serogroup IVb was classified to ST1. Strains of serogroup IIa were further subtyped into eight different sublineages with the most numerous being SL121 (13; 48.1% strains) which belonged to six cgMLST types. The majority of strains, irrespective of the genotypic subtype, had the same antimicrobial resistance profile. The cluster analysis identified several molecular clones typical for L. monocytogenes isolated from similar sources in other countries; however, novel molecular cgMLST types not present in the Listeria database were also identified. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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15 pages, 3407 KiB  
Article
Genomic Analysis of Natural Rough Brucella melitensis Rev.1 Vaccine Strains: Identification and Characterization of Mutations in Key Genes Associated with Bacterial LPS Biosynthesis and Virulence
by David Kornspan, Regina Lubkovskaia, Shubham Mathur, Adva Yeheskel and Mali Salmon-Divon
Int. J. Mol. Sci. 2020, 21(24), 9341; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21249341 - 08 Dec 2020
Cited by 5 | Viewed by 2198
Abstract
Brucella species are facultative intracellular bacteria that cause brucellosis, a zoonotic world-wide disease. The live attenuated B. melitensis Rev.1 vaccine strain is widely used for the control of brucellosis in the small ruminant population. However, Rev.1 induces antibodies against the O-polysaccharide (O-PS) of [...] Read more.
Brucella species are facultative intracellular bacteria that cause brucellosis, a zoonotic world-wide disease. The live attenuated B. melitensis Rev.1 vaccine strain is widely used for the control of brucellosis in the small ruminant population. However, Rev.1 induces antibodies against the O-polysaccharide (O-PS) of the smooth lipopolysaccharide thus, it is difficult to differentiate between infected and vaccinated animals. Hence, rough Brucella strains lacking the O-PS have been introduced. In the current study, we conducted a comprehensive comparative analysis of the genome sequence of two natural Rev.1 rough strains, isolated from sheep, against that of 24 Rev.1 smooth strains and the virulent reference strain B. melitensis 16M. We identified and characterized eight vital mutations within highly important genes associated with Brucella lipopolysaccharide (LPS) biosynthesis and virulence, which may explain the mechanisms underlying the formation of the Rev.1 rough phenotype and may be used to determine the mechanism underlying virulence attenuation. Further complementation studies aimed to estimate the specific role of these mutations in affecting Brucella morphology and virulence will serve as a basis for the design of new attenuated vaccines for animal immunization against brucellosis. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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14 pages, 2677 KiB  
Article
Binding of Kingella kingae RtxA Toxin Depends on Cell Surface Oligosaccharides, but Not on β2 Integrins
by Waheed Ur Rahman, Adriana Osickova, Nela Klimova, Jinery Lora, Nataliya Balashova and Radim Osicka
Int. J. Mol. Sci. 2020, 21(23), 9092; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21239092 - 29 Nov 2020
Cited by 9 | Viewed by 2181
Abstract
The Gram-negative coccobacillus Kingella kingae is increasingly recognized as an important invasive pediatric pathogen that causes mostly bacteremia and skeletal system infections. K. kingae secretes an RtxA toxin that belongs to a broad family of the RTX (Repeats in ToXin) cytotoxins produced by [...] Read more.
The Gram-negative coccobacillus Kingella kingae is increasingly recognized as an important invasive pediatric pathogen that causes mostly bacteremia and skeletal system infections. K. kingae secretes an RtxA toxin that belongs to a broad family of the RTX (Repeats in ToXin) cytotoxins produced by bacterial pathogens. Recently, we demonstrated that membrane cholesterol facilitates interaction of RtxA with target cells, but other cell surface structures potentially involved in toxin binding to cells remain unknown. We show that deglycosylation of cell surface structures by glycosidase treatment, or inhibition of protein N- and O-glycosylation by chemical inhibitors substantially reduces RtxA binding to target cells. Consequently, the deglycosylated cells were more resistant to cytotoxic activity of RtxA. Moreover, experiments on cells expressing or lacking cell surface integrins of the β2 family revealed that, unlike some other cytotoxins of the RTX family, K. kingae RtxA does not bind target cells via the β2 integrins. Our results, hence, show that RtxA binds cell surface oligosaccharides present on all mammalian cells but not the leukocyte-restricted β2 integrins. This explains the previously observed interaction of the toxin with a broad range of cell types of various mammalian species and reveals that RtxA belongs to the group of broadly cytolytic RTX hemolysins. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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14 pages, 3809 KiB  
Article
AvrA Exerts Inhibition of NF-κB Pathway in Its Naïve Salmonella Serotype through Suppression of p-JNK and Beclin-1 Molecules
by Chao Yin, Zijian Liu, Honghong Xian, Yang Jiao, Yu Yuan, Yang Li, Qiuchun Li and Xinan Jiao
Int. J. Mol. Sci. 2020, 21(17), 6063; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21176063 - 23 Aug 2020
Cited by 13 | Viewed by 2032
Abstract
Avian salmonellosis caused by Salmonella enterica serovar Enteritidis (S. Enteritidis) and Pullorum (S. Pullorum) remains a big threat to the poultry industry and public hygiene. AvrA is an effector involved in inhibiting inflammation. Compared to AvrA from S. Enteritidis [...] Read more.
Avian salmonellosis caused by Salmonella enterica serovar Enteritidis (S. Enteritidis) and Pullorum (S. Pullorum) remains a big threat to the poultry industry and public hygiene. AvrA is an effector involved in inhibiting inflammation. Compared to AvrA from S. Enteritidis (SE-AvrA), the AvrA from S. Pullorum (SP-AvrA) lacks ten amino acids at the C-terminal. In this study, we compared the anti-inflammatory response induced by SP-AvrA to that of SE-AvrA. Transient expression of SP-AvrA in epithelial cells resulted in significantly weaker inhibition of NF-κB pathway activation when treated with TNF-α compared to the inhibition by SE-AvrA. SP-AvrA expression in the S. Enteritidis resulted in weaker suppression of NF-κB pathway in infected HeLa cells compared to SE-AvrA expression in the cells, while SP-AvrA expressed in S. Pullorum C79-13 suppressed NF-κB activation in infected HeLa and Caco 2 BBE cells to a greater extent than did SE-AvrA because of the higher expression of SP-AvrA than SE-AvrA in S. Pullorum. Further analysis demonstrated that the inhibition of NF-κB pathway in Salmonella-infected cells corresponded to the downregulation of the p-JNK and Beclin-1 protein molecules. Our study reveals that AvrA modifies the anti-inflammatory response in a manner dependent on the Salmonella serotype through inhibition of NF-κB pathway. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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Review

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35 pages, 2163 KiB  
Review
Pseudomonas aeruginosa: An Audacious Pathogen with an Adaptable Arsenal of Virulence Factors
by Irene Jurado-Martín, Maite Sainz-Mejías and Siobhán McClean
Int. J. Mol. Sci. 2021, 22(6), 3128; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22063128 - 18 Mar 2021
Cited by 218 | Viewed by 26185
Abstract
Pseudomonas aeruginosa is a dominant pathogen in people with cystic fibrosis (CF) contributing to morbidity and mortality. Its tremendous ability to adapt greatly facilitates its capacity to cause chronic infections. The adaptability and flexibility of the pathogen are afforded by the extensive number [...] Read more.
Pseudomonas aeruginosa is a dominant pathogen in people with cystic fibrosis (CF) contributing to morbidity and mortality. Its tremendous ability to adapt greatly facilitates its capacity to cause chronic infections. The adaptability and flexibility of the pathogen are afforded by the extensive number of virulence factors it has at its disposal, providing P. aeruginosa with the facility to tailor its response against the different stressors in the environment. A deep understanding of these virulence mechanisms is crucial for the design of therapeutic strategies and vaccines against this multi-resistant pathogen. Therefore, this review describes the main virulence factors of P. aeruginosa and the adaptations it undergoes to persist in hostile environments such as the CF respiratory tract. The very large P. aeruginosa genome (5 to 7 MB) contributes considerably to its adaptive capacity; consequently, genomic studies have provided significant insights into elucidating P. aeruginosa evolution and its interactions with the host throughout the course of infection. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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21 pages, 1399 KiB  
Review
Extracellular RNAs in Bacterial Infections: From Emerging Key Players on Host-Pathogen Interactions to Exploitable Biomarkers and Therapeutic Targets
by Tiago Pita, Joana R. Feliciano and Jorge H. Leitão
Int. J. Mol. Sci. 2020, 21(24), 9634; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21249634 - 17 Dec 2020
Cited by 11 | Viewed by 2868
Abstract
Non-coding RNAs (ncRNAs) are key regulators of post-transcriptional gene expression in prokaryotic and eukaryotic organisms. These molecules can interact with mRNAs or proteins, affecting a variety of cellular functions. Emerging evidence shows that intra/inter-species and trans-kingdom regulation can also be achieved with exogenous [...] Read more.
Non-coding RNAs (ncRNAs) are key regulators of post-transcriptional gene expression in prokaryotic and eukaryotic organisms. These molecules can interact with mRNAs or proteins, affecting a variety of cellular functions. Emerging evidence shows that intra/inter-species and trans-kingdom regulation can also be achieved with exogenous RNAs, which are exported to the extracellular medium, mainly through vesicles. In bacteria, membrane vesicles (MVs) seem to be the more common way of extracellular communication. In several bacterial pathogens, MVs have been described as a delivery system of ncRNAs that upon entry into the host cell, regulate their immune response. The aim of the present work is to review this recently described mode of host-pathogen communication and to foster further research on this topic envisaging their exploitation in the design of novel therapeutic and diagnostic strategies to fight bacterial infections. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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16 pages, 1153 KiB  
Review
Helicobacter pylori Virulence Factor Cytotoxin-Associated Gene A (CagA)-Mediated Gastric Pathogenicity
by Shamshul Ansari and Yoshio Yamaoka
Int. J. Mol. Sci. 2020, 21(19), 7430; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21197430 - 08 Oct 2020
Cited by 52 | Viewed by 5960
Abstract
Helicobacter pylori causes persistent infection in the gastric epithelium of more than half of the world’s population, leading to the development of severe complications such as peptic ulcer diseases, gastric cancer, and gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Several virulence factors, including cytotoxin-associated [...] Read more.
Helicobacter pylori causes persistent infection in the gastric epithelium of more than half of the world’s population, leading to the development of severe complications such as peptic ulcer diseases, gastric cancer, and gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Several virulence factors, including cytotoxin-associated gene A (CagA), which is translocated into the gastric epithelium via the type 4 secretory system (T4SS), have been indicated to play a vital role in disease development. Although infection with strains harboring the East Asian type of CagA possessing the EPIYA-A, -B, and -D sequences has been found to potentiate cell proliferation and disease pathogenicity, the exact mechanism of CagA involvement in disease severity still remains to be elucidated. Therefore, we discuss the possible role of CagA in gastric pathogenicity. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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14 pages, 1741 KiB  
Review
Mycobacterial Virulence Factors: Surface-Exposed Lipids and Secreted Proteins
by Angel Ly and Jun Liu
Int. J. Mol. Sci. 2020, 21(11), 3985; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21113985 - 02 Jun 2020
Cited by 20 | Viewed by 6310
Abstract
The clinically important Mycobacterium tuberculosis (M. tb) and related mycobacterial pathogens use various virulence mechanisms to survive and cause disease in their hosts. Several well-established virulence factors include the surface-exposed lipids in the mycobacterial outer membrane, as well as the Esx [...] Read more.
The clinically important Mycobacterium tuberculosis (M. tb) and related mycobacterial pathogens use various virulence mechanisms to survive and cause disease in their hosts. Several well-established virulence factors include the surface-exposed lipids in the mycobacterial outer membrane, as well as the Esx family proteins and the Pro-Glu (PE)/ Pro-Pro-Glu (PPE) family proteins secreted by type VII secretion systems (T7SS). Five ESX T7SS exist in M. tb and three—EsxA secretion system-1 (ESX-1), ESX-3, and ESX-5—have been implicated in virulence, yet only the structures of ESX-3 and ESX-5 have been solved to date. Here, we summarize the current research on three outer membrane lipids—phthiocerol dimycocerosates, phenolic glycolipids, and sulfolipids—as well as the secretion machinery and substrates of three mycobacterial T7SS—ESX-1, ESX-3, and ESX-5. We propose a structural model of the M. tb ESX-1 system based on the latest structural findings of the ESX-3 and ESX-5 secretion apparatuses to gain insight into the transport mechanism of ESX-associated virulence factors. Full article
(This article belongs to the Special Issue Microbial Virulence Factors 2.0)
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