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Multifaceted Activity of Listeriolysin O, the Cholesterol-Dependent Cytolysin of Listeria monocytogenes

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MACPF/CDC Proteins - Agents of Defence, Attack and Invasion

Part of the book series: Subcellular Biochemistry ((SCBI,volume 80))

Abstract

The cholesterol-dependent cytolysins (CDCs) are a large family of pore-forming toxins that are produced by numerous Gram-positive bacterial pathogens. These toxins are released in the extracellular environment as water-soluble monomers or dimers that bind to cholesterol-rich membranes and assemble into large pore complexes. Depending upon their concentration, the nature of the host cell and membrane (cytoplasmic or intracellular) they target, the CDCs can elicit many different cellular responses. Among the CDCs, listeriolysin O (LLO), which is a major virulence factor of the facultative intracellular pathogen Listeria monocytogenes, is involved in several stages of the intracellular lifecycle of the bacterium and displays unique characteristics. It has long been known that following L. monocytogenes internalization into host cells, LLO disrupts the internalization vacuole, enabling the bacterium to replicate into the host cell cytosol. LLO is then used by cytosolic bacteria to spread from cell to cell, avoiding bacterial exposure to the extracellular environment. Although LLO is continuously produced during the intracellular lifecycle of L. monocytogenes, several processes limit its toxicity to ensure the survival of infected cells. It was previously thought that LLO activity was limited to mediating vacuolar escape during bacterial entry and cell to cell spreading. This concept has been challenged by compelling evidence suggesting that LLO secreted by extracellular L. monocytogenes perforates the host cell plasma membrane, triggering important host cell responses. This chapter provides an overview of the well-established intracellular activity of LLO and the multiple roles attributed to LLO secreted by extracellular L. monocytogenes.

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Abbreviations

ALO:

Anthrolysin O

ASM:

Acid sphingomyelinase

CDC:

Cholesterol-dependent cytolysin

CFTR:

Cystic fibrosis transmembrane conductance regulator

ER:

Endoplasmic reticulum

ERK:

Extracellular-signal-regulated kinase

GILT:

Gamma-interferon inducible lysosomal thiol reductase

HGF:

Hepatocyte growth factor receptor

HNP1:

Human neutrophil peptide

ILY:

Intermedilysin O

InlA:

Internalin A

InlB:

Internalin B

IPTG:

Isopropyl β-D-1-thiogalactopyranoside

JNK:

C-Jun N-terminal kinase

LIPI-1:

Listeria pathogenicity island

LLO:

Listeriolysin O

MAPK:

Mitogen-activated protein kinase

MHC:

Major histocompatibility complex

Mpl:

Metalloprotease

NLRs:

NOD-like receptors

PERK:

Double-stranded RNA activated protein kinase (PKR)-like ER kinase

PC-PLC:

Phosphatidylcholine-specific phospholipase

PI-PLC:

Phosphatidylinositol-specific phospholipase

PFO:

Perfringolysin O

PLY:

Pneumolysin

PrfA:

Positive regulatory factor A

ROS:

Reactive oxygen species

SLO:

Streptolysin O

SUMO:

Small ubiquitin-like modifier

UPR:

Unfolded protein response

UTR:

Untranslated region

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Acknowledgements

This work was made possible by Grant R01AI107250 (Stephanie Seveau) from the National Institutes of Health (NIAID) and its contents are solely the responsibility of the author and do not necessarily represent the official views of the NIAID.

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  1. Department of Microbiology, Department of Microbial Infection and Immunity, The Ohio State University, 484 West, 12th Avenue, Columbus, OH, 43210-1292, USA

    Stephanie Seveau

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  1. National Institute of Chemistry, Ljubljana, Slovenia, Laboratory for Molecular Biology and Nanobiotechnology, Ljubljana, Slovenia

    Gregor Anderluh

  2. Division of Structural Biology, University of Oxford Wellcome Trust Centre for Human Genetics, Oxford, United Kingdom

    Robert Gilbert

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Seveau, S. (2014). Multifaceted Activity of Listeriolysin O, the Cholesterol-Dependent Cytolysin of Listeria monocytogenes . In: Anderluh, G., Gilbert, R. (eds) MACPF/CDC Proteins - Agents of Defence, Attack and Invasion. Subcellular Biochemistry, vol 80. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8881-6_9

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