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Chapter 25 : The Role of Phagocytic Cells during Invasion of the Colonic Mucosa

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Abstract:

In acute shigellosis, bacterial invasion of the colonic mucosa is characterized by the development of an intense inflammatory reaction that is responsible for tissue destruction. This chapter reviews the role of determinants with an emphasis on the role of phagocytic cells during the establishment of infection. There are no animal models that faithfully reproduce the disease, and consequently the sequence of events leading to bacterial invasion of the colonic mucosa and to the mounting of the inflammatory reaction in its natural host is not precisely known. Although the infected tissue is not related to the colonic mucosa, this model has proven very useful to decipher cytokine profiles and immune responses induced during infection and benefits from the availability of mice genetically impaired for specific pathways. In light of the importance in downregulating inflammation, and given the importance of phagocytic cells in the control of inflammation, it is possible that the function of some T3S effectors, in particular, the second-line subset of effectors, target-specific cell types. Paradoxically, extracellular release of ATP was shown to favor invasion and dissemination in neighboring epithelial cells.

Citation: Tran Van Nhieu G, Sansonetti P. 2009. The Role of Phagocytic Cells during Invasion of the Colonic Mucosa, p 405-418. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch25
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FIGURE 1

Phagocytic cells and invasion of the colonic epithelium. (1) invasion is not efficient at the apical side of enterocytes but may occur occasionally, leading to the release of IL-8, which acts as a chemoattractant for PMNs. These discrete events account for successful invasion or bacterial crossing of the epithelium. (2) invasions preferentially occur at the levels of M cells overlying solitary lymphoid follicles. Bacterial phagocytosis by macrophages results in cell death and the release of IL-1β and IL-18 which, in turn, trigger the recruitment of PMNs at the site of infection. The influx of incoming PMNs destabilizes the epithelium, favoring access to the enterocyte’s basal side, where invasion readily occurs. (3) Destruction of the epithelium following bacterial invasion, replication, and dissemination in enterocytes is determined by the proinflammatory action of PMNs and macrophages. DC, dendritic cell.

Citation: Tran Van Nhieu G, Sansonetti P. 2009. The Role of Phagocytic Cells during Invasion of the Colonic Mucosa, p 405-418. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch25
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Image of FIGURE 2
FIGURE 2

The arsenal of T3S effectors. (Inset) T3S effectors can be divided into (1) constitutively expressed early effectors that are injected following cell contact—among these, the IpaB and IpaC proteins insert into host cell membranes to form the “translocon”; (2) effectors that are upregulated after secretion; and (3) late effectors that are only expressed after T3S has been induced. (EARLY) T3S effectors that promote bacterial invasion include IpaC, which induces actin polymerization; IpgB1, which activates the Dock/ELMO pathway; and IpaA, which binds to vinculin and induces actin depolymerization. IpgB2 is a mimic of the GTPase Rho. IpgD hydrolyzes PI(4,5)P2 and activates the PI3-K/Akt pathway. VirA inhibits microtubule polymerization and favors intracellular actin-based motility. IcsB binds to Atg5 and prevents autophagy. The early stages of invasion are associated with proinflammatory signals since intracellular PG stimulates Nod1-dependent activation of NF-κB. invasion also induces Ca signaling and the release of extracellular ATP through hemichannels. (LATE) Late T3S effectors down-regulate inflammatory signals. OspG binds to UbcH5, a E2 ubiquitin-conjugating enzyme, and prevents degradation of I-κB by the proteasome. OspF inhibits the activation of the MAPKs Erk2 and p38. OspF also alters the histone code by inhibiting the phosphorylation of histone H3. IpaH9.8 is an E3 ubiquitin ligase that may target the degradation of a MAPK by the proteasome.

Citation: Tran Van Nhieu G, Sansonetti P. 2009. The Role of Phagocytic Cells during Invasion of the Colonic Mucosa, p 405-418. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch25
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FIGURE 3

and phagocytes: cell or bacterial killing. internalization by the macrophage leads to cell death. Bacterial-induced apoptosis dependent on caspase 1/IpaB leads to the release of IL-1β and IL-18. The ASC-containing IPAF inflammasome may be involved in this process. Alternatively, macrophages may die of caspase-1-independent necrosis linked to T3S-dependent plasma membrane permeabilization, potentially mediated by the targeting of mitochondria by invasive bacteria. Necrosis was also reported to result from the release of lipid A by intracellular bacteria. Neutrophils (PMNs) kill internalized through the fusion of elastase-containing granules with the phagocytic vacuole. The activation of the NADPH oxidase and the production of reactive oxygen species (ROS) trigger the formation of neutrophil extracellular traps with PMN postmortem bactericidal activity.

Citation: Tran Van Nhieu G, Sansonetti P. 2009. The Role of Phagocytic Cells during Invasion of the Colonic Mucosa, p 405-418. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch25
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