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Chapter 1 : Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses

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Abstract:

This chapter discusses evolutionary factors regarding the emergence and phylogenetic distribution of the innate immune system and the combinatorial or adaptive immune system, as well as the interactions between the two. Naturally occurring IgM antibodies, as well as induced antibodies, can recognize lipopolysaccharide (LPS) epitopes and feed into the NF-κB activation and differentiation cascade with one result being production of immunoglobulin (Ig) by B lymphocytes. The mannose-binding lectins (C lectins) are effective in complement fixation even in lower chordates, including tunicates, and occur in groups as ancient as Cnidarians. Ancestral deuterostomes branched off from the ancestral protostomes before the two major branches of protostomes, namely, iophotrochozoans (annelids, platyhelminths, and mollusks) and ecdysozoans (arthropods and nematodes), emerged. The chapter talks about interplay between innate and combinatorial immunity, molecules of innate immunity, and the adaptive or combinatorial immune response of jawed vertebrates. With the exception of the molecules defining the combinatorial or adaptive system, cyclostomes have molecules appropriate for their phylogenetic position with the percentage of sequence identity expected from the rates of divergence with the jawed vertebrates. It is likely that in each individual species where co-option occurred, it was followed by a coevolution dependent on the stringency of the selective environment.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1

Key Concept Ranking

Complement System
0.59432584
Innate Immune System
0.52992445
Adaptive Immune System
0.5013429
Amino Acids
0.47153464
MHC Class I
0.44884458
0.59432584
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Image of FIGURE 1
FIGURE 1

Overview of mechanisms of recognition and activation used in defense and differentiation by organisms ranging from insects to vertebrates. (A) Pathways of cell activation that are mediated by NF-κB. Signal pathways are activated by receptors anchored at the cell surface by transmembrane domains. NF-κB in the cytoplasm is induced to enter the nucleus and activate gene expression. The Toll and Toll-related receptors (Toll/TLR) and the B-cell receptor (BCR) recognize LPS on the surface of gram-negative bacteria (Gram-). IL-1R, which contains IgG C2-type domains, is activated by the cytokine IL-1.Toll/TLR and IL-1R have signaling domains in the cytoplasm termed TIR domains. The recognition unit of BCR is Ig and contains V and C1 domains. (B) Humoral defense pathways that rely on the activation of complement for the effector phase. C-reactive protein (CRP) and antibody recognize PC on gram-positive bacteria (Gram+).

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 2
FIGURE 2

Summary of metazoan phylogeny. This scheme is based on recent molecular and morphological data.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 3
FIGURE 3

Birth and death scheme for the evolution of multigene families. Gene families are formed by gene duplication and mutation. Gene death occurs by mutation leading to pseudogenes (ψ) or by deletion from the genome. *, derived from pervious precursor.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 4
FIGURE 4

Formation and evolution of the IgSF domains. This scheme proposes that the I-type domain was the ancestral Ig domain type.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 5
FIGURE 5

Comparative alignments of sequences around the crucial cysteine (C) and tryptophan (W) residues of Ig C1 domains (Igs, TCR, and MHC) and C2 domains of the NCAM group.The positions of the β strands and intervening loop are shown above the alignment. The number of residues identical with the sandbar shark λ light-chain sequence are shown on the right. Sandbar shark (SbS), human (Hu), bullfrog, goldfish, chicken (chick), nurse shark (NuShark), moth, and tunicate (Ciona) sequences were obtained from the databases at http://www.ncbi.nlm.nih.gov. The shark TCR and β2M sequences are from I. Jensen, S. F. Schluter, and J. J. Marchalonis (unpublished data).

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 6
FIGURE 6

Phylogenetic tree of deuterostomes based on molecular data and paleontological considerations.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 7
FIGURE 7

Cladogram of putative VDR orthologs. Chordate receptors were aligned, and percent identities with human VDR were computed with the BLAST alignment tool at http://www.ncbi.nlm.nih. gov/gorf/bl2.html. Alignment for fruit fly and nematode receptors was further refined in Clustal W. The lamprey sequence (lampVDR) is from . Pufferfish and tunicate sequences are available from http://genome.jgi-psf.org/cgi-bin/searchGM2. cgi?db=ciona4 and from http://scrappy.fugu-sg. org/Fugu_rubripes. Other sequences were obtained from the databases at http://www.ncbi.nlm.nih.gov. Frog, ; pufferfish, ; tunicate, ; fruit fly, ecdysone receptor (EcR); daf-12, nematode () daf-12 protein. The latter two are the best matches for VDR in the fruit fly and nematode genomes.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 8
FIGURE 8

Representation of Ig recognition elements found in the combinatorial immune system of jawed vertebrates. Examples shown here are the IgM isotype and the α/β TCR.The membrane receptor on B lymphocytes consists of membrane-associated IgM monomer (IgM). The circulating form shown here is the pentamer. The antigen receptor on T lymphocytes is the α/β heterodimer depicted here recognizing peptide antigen presented by an MHC class I molecule on an antigen-presenting cell. All the variable (V) regions and constant (C) domains as well as the MHC C1 and the associated β2M are Ig C1 domains. The α1 and α2 MHC domains presenting peptides are unrelated to Igs. Adapted from with permission.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 9
FIGURE 9

Schematic diagram summarizing the evolution and properties of the RAG genes. The genomic organization is shown in the boxes and line diagram, with the direction of transcription indicated by the arrows on the boxes. Domains identified in the proteins are indicated.“ RING” is the ring zinc finger domain; NBD is the nonamer-binding domain. Adapted from with permission.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 10
FIGURE 10

Phylogenetic distribution of the ring finger motif found in RAG1. Sequences were obtained from the databases at; http://www.ncbi.nlm.nih.gov. Human (Hu); mouse (Mu); chicken (Ch); trout (Tr); tunicate (); (Ara); RAD, nucleotide excision repair protein; EP, C3HC4-type ring finger; BRCA, breast cancer.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 11
FIGURE 11

Phylogenetic distribution of the RAG1 NBD.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 12
FIGURE 12

Comparative alignment of sandbar shark λ (cDNA clone 5.1) ( ) sequence with human λ light-chain Mcg (Vλ5) ( ).The structural features depicted, including extended chain (β band), reverse turn, and other structures, are those of human λ light chain as determined by X-ray crystallography. Shortened structures are indicated by gaps and insertions are designated by placement of the residues above the corresponding segment. Identities between sequences are shaded. Residues conserved in all light chains are indicated by stars above the sequence. Adapted from with permission.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 13
FIGURE 13

Comparative alignment of two sandbar shark Vµ ( ) sequences with that of a human VH3 (HuV3) monoclonal IgM autoantibody ( ).The CDR segments shown are those defined by for human sequences. Residues shared with the human sequence are shaded. Universally conserved residues are denoted by a star. Adapted from with permission.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Image of FIGURE 14
FIGURE 14

Comparative alignments of human VJλ (Mcg),TCR VDJβ ( ), and TCR VJλ ( ) and sandbar shark VJλ,TCR VDJβ, TCR VJλ.The shark TCR sequences are from Jensen, Schluter, and Marchalonis (unpublished data).The shading indicates positions with at least four matches. Adapted from with permission.

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1
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Tables

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TABLE 1

Distribution in phylogeny of molecules functioning in innate immunity

Citation: Marchalonis J, Schluter S, Whitfield G. 2004. Evolutionary Emergence and Interactions among Elements of the Innate and Combinatorial Responses, p 1-30. In Kaufmann S, Medzhitov R, Gordon S (ed), The Innate Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555817671.ch1

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