Elsevier

Microbial Pathogenesis

Volume 149, December 2020, 104575
Microbial Pathogenesis

Listeria monocytogens - Amended understanding of its pathogenesis with a complete picture of its membrane vesicles, quorum sensing, biofilm and invasion

https://doi.org/10.1016/j.micpath.2020.104575Get rights and content

Highlights

  • An up-to-date review on Listeria monocytogenes pathogenesis and its other virulence factors is presented.

  • The current review focuses to understand the role of membrane vesicles mediated pathogenesis biofilms, and delivers auxiliary impetus to understanding the potentials of virulence mediated invasion in Listeria monocytogenes.

Abstract

Listeria monocytogenes is a ubiquitous, intracellular foodborne pathogen that causes listeriosis in animals and humans. Pathogenic Listeria monocytogenes easily adapted to the conditions of human gastrointestinal tract and tolerate the counter changes such as acidity, bile, osmolarity, and antimicrobial peptides. They secrete specialized biologically active extra organ called membrane vesicles which comprises proteins, lipids, and lipopolysaccharides. Listerial vesicles possess functional versatility and play a significant role in pathogenesis by cell-free intercellular communication and toxin packaging. L. monocytogenes can attach promptly and decisively to inert substratum including intestinal mucosa, and forms biofilms and causes detrimental effects. Further, they invade the host cells through quorum sensing (QS) controlled virulence determinants and biofilms. The precise degree to which the bacterium retains the intracellular ambiance of host cells remains unknown. The machinery associated with intracellular survival, and the role of membrane vesicles, quorum sensing, and the Agr system in Listeria monocytogenes largely remains unclear. The current review focused to understand the role of membrane vesicles mediated pathogenesis biofilms, and delivers auxiliary impetus to understanding the potentials of virulence mediated invasion in Listeria monocytogenes.

Introduction

In recent times, problems caused by foodborne pathogens have become a crucial public health issue worldwide, developing a substantial level of morbidity and mortality [1]. As per a World Health Organization (WHO) report, foodborne illnesses are considered as an extremely complex community health-related issue in both technologically advanced and developing countries [2]. Listeria monocytogens is a Gram-positive, rod-shaped bacterium which causes listeriosis in human, an infrequent disease accompanying with high death rates through septicaemia, meningitis, miscarriage, and stillbirth [3,4]. It mainly pangs immune-compromised adults, aged people, pregnant women, and new-borns. The bacterium was first named as Listeria monocytogens by Murray et al., due to the distinguishing monocytosis observed in diseased rabbits and guinea pigs in the laboratory [5].

As a consequence of foodborne epidemics, concern in the bacterium kept growing across food manufacturers and government entities in the 1980s, with a consequent rise in the literature published. The biochemistry of the L. monocytogenes and further Listeria spp cellular framework was examined by Fiedler and he introduced a macromolecular model of the listerial cell wall association [6]. Several factors that influence the pathogenicity of L. monocytogenes have been proposed over the years such as, intracellular multiplication, iron substances, catalase, and superoxide dismutase, superficial constituents, and hemolysins [7].

The transmission of L. monocytogenes is facilitated through cell-to-cell penetration. The larger part of the virulence proteins is positioned on the cell surface or hidden to the extracellular locale [8]. L. monocytogenes comprises significantly specific secretion systems such as flagella export apparatus (FEA) systems and membrane vesicles to transport the proteins and to grasp definite targets [9].

The membrane surface protein actA plays a major role in the invasion of intracellular bacterium and mobilization of actin assembly inside host cells [10]. After the invasion of host cells, L. monocytogenes uses listriolysin O (LLO) and/or phospholipases (PlcA and PlcB) for the ingestion and to invade the human cell cytosol [11]. Subsequently, the L. monocytogenes develops successful biofilms and build its unique infection mechanisms which diverge from other enteropathogens [12]. The control of virulence in L. monocytogenes relies greatly on the transcription regulator called PrfA, which controls the expression of a complex array of genes, and thus it is known to be the master virulence regulator [13]. Despite this, numerous additional virulence regulators such as Hfq, MogR, DegU, VirR, GmaR, and SigB, substantially contributed to the virulence regulatory network of L. monocytogenes [14].

Section snippets

Biologically active outer membrane vesicles – a successive secreted virulence factor of Listeria monocytogenes

Extracellular vesicles (EVs) have been secreted in extracellular space components of the mammals and are identified in many microorganisms, suggesting that these structures are established in all domains of life [15]. Gram-negative EVs are called outer membrane vesicles (OMVs) since they secreted from the external membrane [16]. OMVs are dynamic in function, such as intercellular, cell-free interaction, environmental stress detoxification, rivalry killing, and move among bacteria or through the

Biofilm as a virulence factor in Listeria monocytogens

Bacterial cells are frequently established in multifaceted societies, named biofilms that deliver resources and defence to harsh environments (Fig. 2.) Listeria monocytogenes easily adopt a saprophytic way of life, and shift from commensalism to virulence stage leading to infections in some uncommon situations, especially in the persons with immunodeficiency [56].

Concerning the food chain, biofilm development enables to sustain the L. monocytogenes in the natural ecosystem and adds more to the

Invasion and intracellular survival of Listeria monocytogens

Listeria monocytogenes is an obligatory intracellular pathogen capable of deliberately invading and propagating in mammalian cells. In 1926, Murray and his colleagues published for the first time on this bacterial pathogen intracellular replication of L. monocytogenes within mononuclear cells [96]. In the 1960s, Mackaness's pioneering study, which established key players in cellular immunity contrary to bacterial intracellular pathogens, took benefit of intracellular L. monocytogenes as a

Conclusions

Collectively these review provide a clearer understanding of the role of membrane vesicles, with the mechanism of quorum sensing, biofilm, and invasion. The treatment of Listeria monocytogenes focal infections remains a major challenge in the healthcare community since they develop a large array of biofilm regulated virulence and quorum sensing factors that influence disease progression. Many promising recent advances in the research of L. monocytogenes as an intracellular pathogen have been

Declaration of competing interest

Authors do not have any conflict of interest.

Acknowledgments

The authors strongly acknowledge the Vinayaka mission research foundation (deemed to be University) and Vinayaka mission medical college, Karaikal for the facilities provided.

References (110)

  • R.J. Mrsny

    Lessons from nature: “Pathogen-Mimetic” systems for mucosal Nano-medicines

    Adv. Drug Deliv. Rev.

    (2009)
  • J.E. Galán et al.

    Cross-talk between bacterial pathogens and their host cells

    Annu. Rev. Cell Dev. Biol.

    (1996)
  • R.L.T. Churchill et al.

    Detection of Listeria monocytogenes and the toxin listeriolysin O in food

    J. Microbiol. Methods

    (2006)
  • L.K. Dygico et al.

    The ability of Listeria monocytogenes to form biofilm on surfaces relevant to the mushroom production environment

    Int. J. Food Microbiol.

    (2020)
  • S. Hansen et al.

    A novel growth-based selection strategy identifies new constitutively active variants of the major virulence regulator PrfA in Listeria monocytogenes

    J. Bacteriol.

    (2020)
  • H. Abdelhamed et al.

    Contributions of a LysR transcriptional regulator to Listeria monocytogenes virulence and identification of its regulons

    J. Bacteriol.

    (2020)
  • M. Colombo et al.

    Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles

    Annu. Rev. Cell Dev. Biol.

    (2014)
  • E.Y. Lee et al.

    Global Proteomic Profiling of Native Outer Membrane Vesicles Derived from Escherichia coli, Proteomics

    (2007)
  • A.J. McBroom et al.

    Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response

    Mol. Microbiol.

    (2007)
  • I.A. MacDonald et al.

    Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa

    J. Bacteriol.

    (2013)
  • S. Gill et al.

    Extracellular membrane vesicles in the three domains of life and beyond

    FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev.

    (2019)
  • V. Gujrati et al.

    Bioengineered bacterial vesicles as biological nano-heaters for optoacoustic imaging

    Nat. Commun.

    (2019)
  • S. Vdovikova et al.

    A novel role of Listeria monocytogenes membrane vesicles in inhibition of autophagy and cell death

    Front. Cell. Infect. Microbiol.

    (2017)
  • B.A. Haruna et al.

    Adaptive mechanisms of Listeria monocytogenes to stressors: an overview

    South Asian Journal of Research in Microbiology

    (2019)
  • R. Frantz et al.

    The secrnome of listeria monocytogenes harbors small noncoding rnas that are potent inducers of beta interferon

    mBio

    (2019)
  • P.N.M. Gerhardt et al.

    Osmotic and chill activation of glycine betaine porter II in Listeria monocytogenes membrane vesicles

    J. Bacteriol.

    (2000)
  • G.C. Dowd et al.

    Listeria monocytogenes exploits host exocytosis to promote cell-to-cell spread

    Proc. Natl. Acad. Sci. U. S. A

    (2020)
  • S. Kühn et al.

    The actin comet guides the way: how Listeria actin subversion has impacted cell biology, infection biology and structural biology

    Cell Microbiol.

    (2020 Apr)
  • M. Šrajer Gajdošik et al.

    Proteomic analysis of pyridoxal oxime derivatives treated Listeria monocytogenes reveals down-regulation of the main virulence factor, Listeriolysin O

    Food Res. Int.

    (2020)
  • M.F. Tan et al.

    Development of ListeriaBase and comparative analysis of Listeria monocytogenes

    BMC Genom.

    (2015)
  • C.J. Provoda et al.

    Bacterial pore-forming hemolysins and their use in the cytosolic delivery of macromolecules

    Adv. Drug Deliv. Rev.

    (2000)
  • J.H. Lee et al.

    Transcription factor σB plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes

    PloS One

    (2013)
  • P.N.M. Gerhardt et al.

    Osmotic and chill activation of glycine betaine porter II in Listeria monocytogenes membrane vesicles

    J. Bacteriol.

    (2000)
  • P.N.M. Gerhardt et al.

    Sodium-driven, osmotically activated glycine betaine transport in Listeria monocytogenes membrane vesicles

    J. Bacteriol.

    (1996)
  • B.K. Ghosh et al.

    Fractionation and characterization of the plasma and mesosome membrane of Listeria monocytogenes

    J. Bacteriol.

    (1969)
  • G.A. Smith et al.

    The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread

    Infect. Immun.

    (1995)
  • B.K. Ghosh et al.

    Fine structure of Listeria monocytogenes in relation to protoplast formation

    J. Bacteriol.

    (1967)
  • B.K. Ghosh et al.

    Isolation, composition, and structure of membrane of Listeria monocytogenes

    J. Bacteriol.

    (1968)
  • P.D. Cotter et al.

    Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes

    PLoS Pathog.

    (2008)
  • J.J. Quereda et al.

    Listeriolysin S is a streptolysin S-like virulence factor that targets exclusively prokaryotic cells in vivo

    mBio

    (2017)
  • N.O. Gekara et al.

    The multiple mechanisms of Ca2+ signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes

    Cell Microbiol.

    (2007)
  • S. Vadia et al.

    Fluxes of Ca2+ and K+ Are Required for the Listeriolysin O-dependent Internalization Pathway of Listeria Monocytogenes, Infection and Immunity

    (2014)
  • S. Seveau

    Multifaceted Activity of Listeriolysin O, the Cholesterol-dependent Cytolysin of Listeria Monocytogenes

    Sub Cell. Biochem.

    (2014)
  • N. Meyer-Morse et al.

    Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection

    PloS One

    (2010)
  • M. Puri et al.

    Listeriolysin O Regulates the Expression of Optineurin, an Autophagy Adaptor that Inhibits the Growth of Listeria Monocytogenes, Toxins

    (2017)
  • S.A. Dalrymple et al.

    Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia

    Infect. Immun.

    (1995)
  • Y. Zhang et al.

    Listeria hijacks host mitophagy through a novel mitophagy receptor to evade killing

    Nat. Immunol.

    (2019)
  • B.N. Nguyen et al.

    A phagosome-specific cytolysin revisited

    Cell Microbiol.

    (2019)
  • R. Karthikeyan et al.

    Comprehensive proteomic analysis and pathogenic role of membrane vesicles of Listeria monocytogenes serotype 4b reveals proteins associated with virulence and their possible interaction with host

    Int. J. Med. Microbiol.

    (2019)
  • E.Y. Lee et al.

    Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles

    Proteomics

    (2009)
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