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Innate Response to MAP Infection

Upon transcytosis across the intestinal epithe­lium, MAP is taken up by macrophages and DCs in the subepithelium. In general, these cells will then traffic to the lamina propria of the small intestine, the mesenteric lymph nodes and the peripheral circulation, thereby initiating an im­mune response to clear or control the infection (Lugton, 1999).

Survivability of MAP within the macrophage is dependent upon the host, as MAP can thwart degradation by blocking matu­ration and preventing acidification of phago­somes (Sturgill-Koszycki et al., 1994; Hostetter et al., 2003). Hostetter et al. (2003) found that phagosomes within macrophages infected with live MAP expressed higher levels of transfer­rin, an early phagosome marker and lower lev­els of lysosome-associated membrane protein one, a late maturation marker, compared with phagosomes within macrophages infected with heat-killed MAP or M. avium subsp. avium. The arrestment of phagosome maturation has been correlated with inhibition of phagosome acidi­fication, a process that produces bactericidal agents such as nitric oxide, reactive oxygen spe­cies (H2O2 and OH-) and lysosomal hydrolases (Akaki et al., 199 7). The mechanism by which MAP is taken up by phagocytes can affect the subsequent ability of the phagocyte to effec­tively destroy the pathogen. The engagement of complement receptors (CR1, CR3 and CR4) for MAP uptake can limit macrophage activa­tion (Hostetter et al., 2005). Blocking bovine CR3 receptor by incubating activated mac­rophages with anti-CD18∕CD11b reduced up­take of opsonized MAP (Hostetter et al., 2005). Opsonization of MAP with heat-treated serum limited uptake, further demonstrating that CR is a primary means of MAP entry into mac­rophage. Perhaps even more interesting was the observation that opsonization of MAP lowered levels of phagosome acidification, suggestive of decreased ability to kill the pathogen (Hostetter et al., 2005).
More recently, pre-incubation of bovine monocyte-derived macrophages with mannosylated-lipoarabinomannan (Man-LAM) derived from MAP was shown to reduce kill­ing of live M. avium subsp. avium (Souza et al., 2013). Reduced killing was directly associated with lower phagosome acidification and fusion of the phagosome-lysosome, along with in­creased IL-10 expression. IL-10 is induced via a MAPK-p38 pathway in macrophages, a sig­nalling pathway that has been shown to nega­tively impact acidification of the phagosome and killing of MAP within the macrophage (Souza et al., 2006). Activation of the MAPK path­way in bovine monocytes upon infection with MAP is mediated through TLR 2 (Weiss et al., 2008). Blocking TLR2 on bovine monocytes resulted in increased phagosome acidification, phagosome-lysosome fusion and MAP survival, suggesting that TLR2 signalling is critical to macrophage bactericidal activities (Weiss et al., 2008). It is clear that IL-10 plays a substantial role in the ability of the macrophages to arrest the infectious process (Hussain et al., 2016). IL-10 is a negative regulator of IL-12 produc­tion by antigen-presenting cells, thereby influ­encing the cross-talk between macrophages and T cells and retarding the amplification of the adaptive immune response (Rahim et al., 2005). Although IL-10 plays an essential role in controlling inflammatory responses of the host during infection, one contrary aspect may be a weaponization by the intracellular patho­gen to defeat the macrophage. A recent review outlines a critical role for regulation of IL-10 by mycobacteria, suggesting that it is a key effec­tor in survival of the pathogen (Abdalla et al.,

2016). Another cytokine that controls mac­rophage responses to intracellular infection is IL-1β (Lamont et al., 2012). The infection of MAC-T-bovine monocyte-derived macrophages with live MAP demonstrated that phagosome acidification was calcium-dependent and linked to IL-1β processing by the cells. It was suggested that IL-1β plays a critical role in the recruit­ment of other monocyte-derived macrophages to the site of infection and that MAP has the ability to exploit this by inducing calcium influx in the cell. A comprehensive RNA-seq analysis of genes expressed by monocyte-derived mac­rophages infected with MAP complemented those results as they found upregulation of IL-1 and other proinflammatory genes in early infec­tion, concomitant with expression of IL-10 and other proinflammatory mediators (Casey et al., 2015). It is clear that macrophage-mycobac­teria interactions have to be balanced between protection and pathology and this is not always successful in the infected host (Divangahi et al., 2018). Participation of other cell types involved in adaptive immunity may be required to skew the host response to a more protective nature.

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Source: Behr Marcel A., Stevenson K., Kapur V. (eds.). Paratuberculosis: Organism, Disease, Control. 2nd edition. — CAB International,2020. — 439 p.. 2020
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