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Chapter 3 : The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates

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Abstract:

This chapter focuses on how the essential components of the adaptive immune system-Ab, TcR, and MHC molecules-arose and began to interact. The major histocompatibility complex (MHC) molecules are loaded with their antigens by sophisticated pathways composed of various kinds of molecules, some of which are encoded by genes located in the MHC. In all jawed vertebrates examined thus far, the essential elements of the adaptive immune system are present. Despite years of functional experiments with invertebrates pointing to recognition of allo- and xenoantigens, none of the essential genetic components of the adaptive immune system in the jawed vertebrates were found in the first complete genomic sequences of invertebrates: an insect (the fruit fly ) and a nematode worm (). Therefore, the notion that invertebrates lack an adaptive immune system was strengthened, and the question became how invertebrates managed to survive without a system that is essential to jawed vertebrates. A key concept that has relevance no matter what the defense system might be is that pathogens that overcome all of their hosts may face a bleak evolutionary future, and so, in general, the virulence of pathogens is constrained and guided by the particular defenses that their host(s) evolve. Although there is little scope to observe the evolution of the immune system through fossils, it seems likely that the adaptive immune system of the jawed vertebrates also evolved in steps, none of which are separated between those organisms still living.

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3

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Cytotoxic T Cell
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Major Histocompatibility Complex
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Adaptive Immune System
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MHC Class I
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Figures

Image of FIGURE 1
FIGURE 1

An idealized tree, showing the relationships of the animals (and their defense systems). Phyla are indicated above the tree with thick lines; common names of species are indicated above the tree with thin lines; defense systems are indicated.

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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Image of FIGURE 2
FIGURE 2

A model for the evolution of the adaptive immune system of jawed vertebrates, from the primordial MHC (left) through two rounds of genome-wide duplication (middle) and subsequent silencing, deletion, and break up to give MHC paralogous regions (right). Black boxes indicate genes based on data from chickens; open boxes indicate genes based on data from other species. Gga and Hsa, chromosomes from chickens and humans, respectively.

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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Image of FIGURE 3
FIGURE 3

A model for the evolution of split variable region-containing antigen specific receptors by insertion of transposons (top), with cartoons indicating the location of the CDRs in a V domain (lower right) and the footprint of the CDRs on an MHC molecule (lower left). In the upper left, open circles indicate domains (Ig V type and C type), lines indicate transmembrane and cytoplasmic regions, filled circles indicate D and J segments of the protein, grey bars indicate membranes; one chain is gray to indicate that the molecule may or may not have been a dimer. In the upper right, boxes indicate genes or gene segments, and dotted lines indicate regions introduced by transposon insertion with the heavy black lines indicating RSS. In the cartoons, cylinders indicate α-helices, arrows indicate β-strands, thin lines indicate other conformations of the protein, the thick line indicates peptide bound to the MHC molecule, and the dotted ovals indicate the footprint of the CDRs from the α-chain and the β-chain of a TcR on a class I molecule.

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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Image of FIGURE 4
FIGURE 4

A model for the evolution of MHC molecules, from a class II β-chain-like homodimer to a class II heterodimer by duplication and divergence, and then to a class I chain with β2m by inversion. On the left, circles indicate domains (open for class II α-chain, gray-filled for class II β-chain, with SS for intrachain disulphide bond), lines indicate transmembrane and cytoplasmic regions, gray bars indicate membranes. On the right, boxes indicate exons (open for coding regions of class II α-chain, gray-filled for coding regions of class II β-chain, black-filled for 3′ untranslated region), P indicates promoter region with arrow showing direction of transcription, curved arrow around axis, and lightning bolts indicating an inversion around a central point with asymmetric breakpoints. Adapted from .

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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Image of FIGURE 5
FIGURE 5

A cartoon showing the relationship between coevolution of interacting genes and (recombinational) distance in the genome, as illustrated for the class I and TAP genes of the MHC. (Left) The TAP heterodimer and class I molecule(s) are embedded in a membrane. The number of well-expressed class I molecules ranges from three in humans to one in chickens. Similarly, the specificity of interaction with peptide (as indicated by the number and depth of indentations) increases for TAPs and may decrease for class I molecules from humans to chickens. (Right) Different regions of the MHC labelled in bold are separated by thin vertical lines, genes labeled in normal script are indicated by thick vertical lines, and distance between the TAP genes and the most distant class I gene is indicated by the horizontal arrow. Adapted from ; B. Walker et al., submitted.

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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Image of FIGURE 6
FIGURE 6

A cartoon showing that coevolution between the peptide-translocation specificity of TAP and the peptide-binding specificity of class I molecules leads to a single dominantly expressed class I molecule, as illustrated with the chicken MHC haplotype B4. Thin lines indicate peptides, a minus sign within a circle indicates negatively charged residue, a plus sign within a circle indicates positively charged residue, a circle indicates a hydrophobic residue. Adapted from .

Citation: Kaufman J. 2011. The Evolutionary Origins of the Adaptive Immune System of Jawed Vertebrates, p 41-55. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch3
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