16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System

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This chapter focuses on recent developments in one’s understanding of how different components of the cell envelope from virulent mycobacteria, in particular , interact with each stage of innate and adaptive immune responses. Human dendritic cells express an additional C-type lectin, dendritic cell-specific ICAM-3-grabbing nonintegrin (DC-SIGN), which is not present on macrophages but serves as a major receptor for on dendritic cells (DCs). Cell wall components of mycobacteria bind to these pathogen recognition receptors on DCs and macrophages, and initiate the host response to infection. The biological relevance of TLR activation by cell wall components has been examined by mycobacterial infection of gene-deficient mice. Inactivation of protein kinase G (PknG) by gene disruption or chemical inhibition resulted in delivery of pathogenic mycobacteria to lysosomes and mycobacterial killing, and conversely, expression of PknG in nonpathogenic prevented phagosomal maturation. The induction of adaptive immunity to mycobacteria and activation of infected macrophages by IFN-γ can overcome the maturation arrest of mycobacteria containing phagosomes. CD1 proteins, which are antigen presenting molecules encoded by genes located outside of the major histocompatibility complex (MHC), recognize nonpeptide lipid or glycolipid structures, including components of mycobacteria. The containment of mycobacterial infection requires the formation of granulomas (or tubercles), which are nodular aggregations of lymphocytes, macrophages, and epithelioid cells. In human infection, the propensity of trehalose dimycolate (TDM) and other cell wall components to promote granuloma formation in association with a chronic T-cell response leads to caseating granulomas, which may erode into airways.

Citation: Britton W, Triccas J. 2008. 16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System, p 249-270. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch16
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Image of Figure 1.
Figure 1.

T-cell immunity to mycobacteria. Professional antigen-presenting cells (APCs), such as dendritic cells, can present peptide fragments to classical CD8 and CD4 T cells through major histocompatibility (MHC) class I and II molecules, respectively. Mycobacterial lipids can also be presented through CD1 molecules to T-cell subsets including γδ T cells, natural killer (NK) T cells and other non classic T cells lacking expression of CD4 and CD8 surface molecules. Activated APCs release soluble meditators, such as the cytokines IL-12, IL-18, and IL-23, which act to enhance the effector function of mycobacteriaspecific T cells. Release of IFN-γ and TNF serve to activate macrophages infected with mycobacteria to promote bacterial killing. Perforin is cytolytic for infected cells, and granulysin is bactericidal for mycobacteria. Activated macrophages release cytokines and chemokines, which are required for granuloma formation in order to contain the infection effectively.

Citation: Britton W, Triccas J. 2008. 16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System, p 249-270. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch16
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Image of Figure 2.
Figure 2.

Inhibition of phagosome maturation by cell envelope components of . (A) Opsonized particles and extracellular bacteria are taken into phagosomes, which mature and fuse with lysosomes containing acid hydrolases necessary to digest the bacteria. The early phagosomes acquire the GTPase Rab5 and have access to transferring receptors (TfR) and a supply of iron from the early endosome (EE) compartment. Subunits of PI3 kinase (PI3K) are recruited and generate PI3P on the maturing phagosome, which acquires Rab7 and the early endosome antigen 1 (EEA1) which is essential for fusion with lysosomes. The late phagosome also recruits syntaxin 6, which is required for acquisition of the vacuolar proton ATPase (VATPase), necessary for acidification of the phagosome. (B) Phagosomes containing virulent mycobacteria, such as do not mature beyond the early phagosome stage characterized by Rab5. They fail to acquire markers of late phagosomes, fuse with lysosomes or undergo acidification. ManLAM inhibits PI3-kinase and prevents the generation of PI3P on the surface of the phagosome and the acquisition of the tethering proteins and the V-ATPase. ManLAM also blocks the Ca flux required for recruitment of PI3-kinase to the phagosome. also secretes the acid phosphatase SapM, which hydrolyzes PI3P and prevents PI3P accumulating on the surface of phagosomes containing live, virulent mycobacteria. The production of the serine-threonine kinase G (PknG) by virulent mycobacteria also inhibits phagolysosomal fusion. By contrast, lower order PIMs increase the fusion of early phagosomes with early endosomes, so they acquire syntaxin 4 and access to iron for mycobacterial replication.

Citation: Britton W, Triccas J. 2008. 16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System, p 249-270. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch16
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Image of Figure 3.
Figure 3.

Inhibition of macrophage activation by cell envelope components of . Infection with virulent inhibits the transcriptional response of macrophages to the activation by IFN-γ secreted by mycobacterium-specific CD4 T cells by disrupting the interaction of STAT1 with the transcriptional coactivators CREB-binding protein (CREB BP) and p300, as demonstrated by reduced MHC class II expression. This inhibition is dependent on activation of TLR2/MyD88 by lipoproteins, such as LpgH, and PIMS, and also on stimulation of TLR2 by the mycolyl-arabinogalactan peptidoglycan complex through an MyD88-independent pathway. LAM interferes with intracellular signaling by activating the Src homology containing tyrosine phosphatase SHP-1, which inactivates phosphorylated signaling kinases, such as protein kinase C (PKC) and MAP kinase. In addition, cell wall components, such as LAM and DIM, can act as scavengers for ROI and RNI, respectively, produced by phagocyte oxidase (Phox) and inducible nitric oxide synthase (iNOS).

Citation: Britton W, Triccas J. 2008. 16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System, p 249-270. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch16
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Table 1.

Classes of mycobacterial cell wall molecules recognized by the humoral immune response during mycobacterial infection

Citation: Britton W, Triccas J. 2008. 16 The Constituents of the Cell Envelope and Their Impact on the Host Immune System, p 249-270. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch16