Chapter 53 : Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes

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It is recognized that grows in a broad variety of cell types in animal models and in cell culture systems. This chapter reviews the molecular mechanisms involved in host-cell invasion, intracellular growth, and cell-to-cell spread. The process of entry of into nonphagocytic cells has been examined by scanning and transmission electron microscopy. In the genome, 41 genes encoding LPXTG proteins are detected. Several lines of evidence indicate that internalin is sufficient for entry in cells expressing its receptor. Indeed, expression of , the gene encoding internalin, in and also in the more distantly related grampositive bacterium , confers invasiveness to these noninvasive species. Externally added InlB is also able to associate with and several other gram-positive bacteria. Several autolysins have been shown to contribute to infection, and it has been hypothesized that they could have functioned as primitive colonizing factors, allowing bacteria to interact with surfaces that express molecules analogous to their natural receptors. FbpA was identified through a signature-tagged mutagenesis screening designed to identify new virulence factors. A fusion molecule of the E-cadherin ecto-domain and of the a-catenin actin-binding site restores invasion, suggesting that exploits the same molecular scaffold as the one involved in adherens junctions function to induce its entry into target cells. Intracellular pathogens can be divided into those that reside within a host vacuole and those, like , that escape and grow directly in the host cytosol.

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 1

Model of the intracellular life cycle. Bacteria induce their internalization in a phagosome that is subsequently lysed; once in the host cell cytoplasm, proliferates and polymerizes the host cell actin (stippled regions) to propulse itself, invading neighboring cells and starting a new infectious cycle ( ). The main bacterial products implicated in each step are indicated.

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 2

Scanning (A) and transmission (B and C) electron microscopy of different steps of the intracellular life cycle in the human epithelial Caco-2 cell line. (A and B) is internalized in host cells by a zipper phagocytosis mechanism, without triggering dramatic actin cytoskeleton rearrangements ( ). (C) Bacteria are internalized in a phagosome ( ) that is lysed after entry; cytoplasmic bacteria proliferate ( ) and polymerize host cell actin ( ) to move in the host cell cytoplasm; reaching the host cell plasma membrane induces the formation of protrusions ( ) that can invade neighboring cells ( ); bacteria are then located in a double membrane secondary vacuole ( ) that is lysed ( ), and the bacteria start a new infectious cycle ( ).

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 3

Members of the internalin family. A total of 24 proteins have been recognized in the genome that possess LRRs and belong to the internalin family: 19 proteins present LPXTG motifs and are covalently linked to the bacterial cell wall (including InlA), 1 protein is loosely attached to the membrane through GW motifs (InlB), and 4 proteins do not present anchor motifs and are released as soluble proteins (including InlC) ( ).

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 4

Model of internalization pathways in host cells. (A) InlA internalization pathway. The bacterial protein InlA binds E-cadherin located in lipid rafts, which in turns interacts with p120-, β-, and α-catenins. α-Catenin would link the whole complex to the actin cytoskeleton and to vezatin, which recruits the unconventional myosin VIIa, generating the contractile force required for internalization. (B) InlB internalization pathway. Soluble InlB can interact with gC1qr, but the signaling cascades triggered by this interaction are unknown; soluble InlB (stabilized by GAGs) or bacterial-associated InlB can interact with Met located in lipid rafts, inducing the recruitment of adaptor proteins (Cbl, Gab1, or Shc) and of class I PI 3-kinase. Conversion of PI( )P (PIP2) into PI( )P (PIP3) leads to translocation to the plasma membrane of an unknown factor that activates Rac; in turn, Rac indirectly activates LIM kinase, controlling a cofilin phosphocycle (that implicates an unknown phosphatase) that regulates actin polymerizationdepolymerization. Rac is also implicated in the activation of the actin nucleating Arp2/3 complex, probably through a signaling cascade that includes Wave.

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 5

Fluorescence microscopy of Vero cells infected with wild-type (A) or ΔActA (B). Wild-type induces the formation of actin comet tails that propulse the bacteria in the host cell cytoplasm (A), while ΔActA proliferates in microcolonies that are unable to spread from the primary infected cell (B). DNA is labeled with DAPI (4′,6′-diamidino-2-phenylindole; blue), the bacterial cell wall is labeled with an anti- antibody (red), and actin is labeled with fluorescent phalloidin (green).

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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Image of FIGURE 6

Model of actin polymerization by in host cells. The bacterial protein ActA recruits the host cell molecule VASP, which in turn recruits profilin to the bacterial tail; actin monomers are captured by profilin and are transferred to the Arp2/3 complex, which nucleates the polymerization of host actin, leading to the formation of actin comet tails. A capping protein inhibits the polymerization of actin on barbed ends, cofilin promotes the depolymerization of actin from pointed ends, and α-actinin stabilizes actin polymers.

Citation: Pizarro-Cerdá J, Cossart P. 2006. Cell Biology of Invasion and Intracellular Growth by Listeria monocytogenes, p 646-656. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch53
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