Chapter 30 : CD1 and Tuberculosis

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This chapter reviews the immunobiology of CD1 and its potentially important role in the immune response to infection. Importantly, CD1 is expressed on dendritic cell (DC) within granulomas from patients with both and infections, although the role of DC in granuloma formation and maintenance is unclear. One of the hallmarks of bacteria is the capacity to survive within the intracellular environment. A significant increase in CD1c-restricted Tcell proliferation was observed in the tuberculosis group compared to the purified protein derivative (PPD)-negative control group. Interestingly, patients with clinically active pulmonary tuberculosis showed no significant response to lipid antigens or whole bacterial sonicates. Lipid-immunized guinea pigs challenged with virulent via aerosol administration exhibit reduced pulmonary pathology compared to negative control animals. bacilli possess one of the more unusual cell walls in the bacterial kingdom, with many of the lipid molecules being unique to this genus. A more thorough understanding of how CD1 antigen presentation fits into the overall host immune response to infection may lead to novel interventional therapies and improved vaccine formulations for tuberculosis and other infectious diseases.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Figure 1

Hypothetical evolution of CD1 and the MHC. There are five distinct CD1 genes in humans that are unlinked to the MHC locus. These are divided into two groups based on sequence homology. Analysis of protein sequence data shows that CD1 diverged from the MHC family early in vertebrate evolution. The divergence of MHC I and MHC II is estimated at approximately 250 million to 300 million years ago. CD1 and MHC I share many structural features and thus probably have a common ancestor. However, the exact time of the divergence of CD1 and MHC I is difficult to estimate since both gene families are under strong selective pressure. So far, CD1 genes have been found only in placental mammals.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Figure 2

Structure of the human CD1b protein-lipid complex. (a and b) Two orthogonal views of the human CD1b structure from the side (a) and from the top (b) of the structure with bound phosphatidylinositol in the antigen binding pocket. The internal cavity that forms the antigen binding pocket is shown as a transparent surface, and the various channels are indicated as A′, C′, F′, and T′. (c) Structure of human HLA-A2, with the human T-cell leukemia virus type 1 Tax peptide (space filling) in the antigen binding groove shown for comparison to CD1b ( ). (d) Structure of mycolic acid with the meromycolate chain (dark) and the shorter alpha chain (light) and carboxylate groups. (e) Hypothetical model of mycolic acid as it would appear folded into the CD1b protein. The left-hand orthogonal view corresponds to the orientation of the CD1b protein in panel a, and the right hand view corresponds to the orientation in b. In this model, the C long meromycolate chain (dark) is fully contained within channels A′, T′ and F′, a superchannel of ca. 70 Å. The shorter C alkyl chain (light) is lodged in the C? channel. The crystal structure provides no guidance to how to model the end of the C chain in the mycolic acid, and this part of the model is therefore indicated by an extended gray chain. Panels a, b, and e reprinted from reference with permission from the authors and publisher. © 2002 Nature Publishing Group.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Figure 3

Structures of known CD1 lipid antigens. The first six lipid molecules are derived from species and are presented by either CD1a, CD1b, or CD1c. The αGC (far right) is derived from the marine sponge . All of the molecules have a common structural motif, which is a hydrophobic acyl chain linked to a hydrophilic head group such as a simple sugar or carboxylate group. Both structural and functional data support a model in which the hydrophobic acyl chain is anchored into the CD1 binding groove and the hydrophilic head group is exposed to the aqueous environment and interacts with the TCR. While the αGC is not known to exist in bacteria or mammalian tissues, it is a ligand for CD1d and a potent stimulator of CD1d-restricted NK T cells. Lipid structures courtesy of Branch Moody, Brigham and Women's Hospital.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Figure 4

T-cell adaptive immunity. Multiple antigen presentation pathways are available to the host immune system for stimulation of T cells. A model antigen-presenting cell, such as a DC, is able to take up pathogens or pathogen-derived molecules from the surrounding extracellular environment. Live organisms are able to prevent maturation of the phagosome and hence prevent interaction with lysosomes and subsequent killing. The bacilli may survive and grow within the phagosome environment and thus evade immune surveillance. Some evidence exists for secretion of proteins into the cytosol, where they could be processed for presentation by MHC I. Lipid antigens with different structures may partition into different intracellular compartments. For example, short-chain lipids may traffic to recycling endosomes, where they would be accessible to CD1a, while long-chain lipids may traffic to lysosomes for loading and presentation by CD1b. Dashed lines represent the main-line sequence of endosomal maturation. Lipids may be transported out of the phagosome containing live organisms to then enter the antigen presentation pathway for CD1 and MHC II. Likewise, secreted antigens or lipids shed from extracellular bacteria are taken up by endocytosis and enter the endosomal network. Each of the CD1 molecules traffics through the endocytic system in a unique pattern. The CD1a isoform samples recycling endosomes, while CD1b samples late endosomes and lysosomes. The CD1c isoform samples both of these compartments. Together, the CD1 antigen presentation system is able to survey most of the intracellular environment for potential antigenic lipid molecules and to transport these to the cell surface for T-cell recognition.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Figure 5

Effector functions of CD1-restricted T cells. T cells reactive to lipids presented by CD1 on the cell surface secrete high levels of proinflammatory cytokines including IFN-γ and tumor necrosis factor alpha (TNF-α), both critical for containment of infections and granuloma formation. Furthermore, activation of macrophages increases the killing of ingested bacilli. The CD1-restricted T cells release perforin and granulysin, which have direct bactericidal effects on . The CD1-restricted T cells are also cytolytic and have the capacity to kill infected host cells in a CD1-dependent manner.

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30
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Table 1

Antigen-presenting pathways for T cells

Citation: Dascher C, Brenner M. 2005. CD1 and Tuberculosis, p 475-488. In Cole S, Eisenach K, McMurray D, Jacobs, Jr. W (ed), Tuberculosis and the Tubercle Bacillus. ASM Press, Washington, DC. doi: 10.1128/9781555817657.ch30

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