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Dynamic evolution of toll-like receptor multigene families in echinoderms.

Buckley KM, Rast JP - Front Immunol (2012)

Bottom Line: Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences).The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level.These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Department of Immunology, Sunnybrook Research Institute, University of Toronto Toronto, ON, Canada.

ABSTRACT
The genome sequence of the purple sea urchin, Strongylocentrotus purpuratus, a large and long-lived invertebrate, provides a new perspective on animal immunity. Analysis of this genome uncovered a highly complex immune system in which the gene families that encode homologs of the pattern recognition receptors that form the core of vertebrate innate immunity are encoded in large multigene families. The sea urchin genome contains 253 Toll-like receptor (TLR) sequences, more than 200 Nod-like receptors and 1095 scavenger receptor cysteine-rich domains, a 10-fold expansion relative to vertebrates. Given their stereotypic protein structure and simple intron-exon architecture, the TLRs are the most tractable of these families for more detailed analysis. A role for these receptors in immune defense is suggested by their similarity to TLRs in other organisms, sequence diversity, and expression in immunologically active tissues, including phagocytes. The complexity of the sea urchin TLR multigene families is largely derived from expansions independent of those in vertebrates and protostomes, although a small family of TLRs with structure similar to that of Drosophila Toll can be traced to an ancient eumetazoan ancestor. Several other echinoderm sequences are now available, including Lytechinus variegatus, as well as partial sequences from two other sea urchin species. Here, we present an analysis of the invertebrate deuterostome TLRs with emphasis on the echinoderms. Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences). The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level. These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

No MeSH data available.


The TLR subfamily in sea urchins. The protein domain structure for each of the TLR subfamilies is shown. Among the sccTLR sequences, the number of LRRs varies from 21 to 25. TLRs in subfamilies Ib and Ie vary in the total number of LRRs (LRRs that are not present in all sequences are shown in light gray). The divergent TIR sequences that are present in the mccTLRs, intron-containing, and short TLRs are shown in light blue (see Figure 2). The numbers of TIR domains from each group and subfamily that are present in the S. purpuratus and L. variegatus genomes are shown below the diagram structures.
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Figure 1: The TLR subfamily in sea urchins. The protein domain structure for each of the TLR subfamilies is shown. Among the sccTLR sequences, the number of LRRs varies from 21 to 25. TLRs in subfamilies Ib and Ie vary in the total number of LRRs (LRRs that are not present in all sequences are shown in light gray). The divergent TIR sequences that are present in the mccTLRs, intron-containing, and short TLRs are shown in light blue (see Figure 2). The numbers of TIR domains from each group and subfamily that are present in the S. purpuratus and L. variegatus genomes are shown below the diagram structures.

Mentions: Most of the sea urchin TLR proteins (240) are structurally similar to those of vertebrates (Figure 1). The LRRs in the ectodomains of these proteins are flanked by LRR-NT and LRR-CT domains. TLRs with this type of extracellular domain are structurally distinct from Drosophila Toll (Rock et al., 1998) and are known as single cysteine cluster TLRs (sccTLRs; Leulier and Lemaitre, 2008). The sea urchin sccTLRs have between 21 and 25 LRRs. This is the structure of the vertebrate TLRs as well as Drosophila Toll-9 (Table 1). In addition, the sea urchin genome contains 13 TLRs that differ from the sccTLRs both in the structure of the ectodomain and also in the sequence of the TIR domain. Five of these divergent TLRs are characterized by shortened ectodomains that are composed of nine LRRs, rather than the typical 21–25. The LRRs within the ectodomains of these short TLRs are flanked by LRR-NT and LRR-CT domains (Figure 1). Four of the divergent TLRs, which comprise a supported clade, resemble the sccTLRs with respect to domain architecture, but the coding sequence is interrupted by a single intron. Finally, the ectodomains of four of the sea urchin TLRs resemble those of Drosophila Toll, in which LRR-CT and LRR-NT domains interrupt the typical LRRs. This domain organization has been termed multiple cysteine cluster TLRs (mccTLRs; Figure 1; Leulier and Lemaitre, 2008) and is the predominant structure of the Drosophila Toll proteins (Table 1).


Dynamic evolution of toll-like receptor multigene families in echinoderms.

Buckley KM, Rast JP - Front Immunol (2012)

The TLR subfamily in sea urchins. The protein domain structure for each of the TLR subfamilies is shown. Among the sccTLR sequences, the number of LRRs varies from 21 to 25. TLRs in subfamilies Ib and Ie vary in the total number of LRRs (LRRs that are not present in all sequences are shown in light gray). The divergent TIR sequences that are present in the mccTLRs, intron-containing, and short TLRs are shown in light blue (see Figure 2). The numbers of TIR domains from each group and subfamily that are present in the S. purpuratus and L. variegatus genomes are shown below the diagram structures.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3367398&req=5

Figure 1: The TLR subfamily in sea urchins. The protein domain structure for each of the TLR subfamilies is shown. Among the sccTLR sequences, the number of LRRs varies from 21 to 25. TLRs in subfamilies Ib and Ie vary in the total number of LRRs (LRRs that are not present in all sequences are shown in light gray). The divergent TIR sequences that are present in the mccTLRs, intron-containing, and short TLRs are shown in light blue (see Figure 2). The numbers of TIR domains from each group and subfamily that are present in the S. purpuratus and L. variegatus genomes are shown below the diagram structures.
Mentions: Most of the sea urchin TLR proteins (240) are structurally similar to those of vertebrates (Figure 1). The LRRs in the ectodomains of these proteins are flanked by LRR-NT and LRR-CT domains. TLRs with this type of extracellular domain are structurally distinct from Drosophila Toll (Rock et al., 1998) and are known as single cysteine cluster TLRs (sccTLRs; Leulier and Lemaitre, 2008). The sea urchin sccTLRs have between 21 and 25 LRRs. This is the structure of the vertebrate TLRs as well as Drosophila Toll-9 (Table 1). In addition, the sea urchin genome contains 13 TLRs that differ from the sccTLRs both in the structure of the ectodomain and also in the sequence of the TIR domain. Five of these divergent TLRs are characterized by shortened ectodomains that are composed of nine LRRs, rather than the typical 21–25. The LRRs within the ectodomains of these short TLRs are flanked by LRR-NT and LRR-CT domains (Figure 1). Four of the divergent TLRs, which comprise a supported clade, resemble the sccTLRs with respect to domain architecture, but the coding sequence is interrupted by a single intron. Finally, the ectodomains of four of the sea urchin TLRs resemble those of Drosophila Toll, in which LRR-CT and LRR-NT domains interrupt the typical LRRs. This domain organization has been termed multiple cysteine cluster TLRs (mccTLRs; Figure 1; Leulier and Lemaitre, 2008) and is the predominant structure of the Drosophila Toll proteins (Table 1).

Bottom Line: Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences).The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level.These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Department of Immunology, Sunnybrook Research Institute, University of Toronto Toronto, ON, Canada.

ABSTRACT
The genome sequence of the purple sea urchin, Strongylocentrotus purpuratus, a large and long-lived invertebrate, provides a new perspective on animal immunity. Analysis of this genome uncovered a highly complex immune system in which the gene families that encode homologs of the pattern recognition receptors that form the core of vertebrate innate immunity are encoded in large multigene families. The sea urchin genome contains 253 Toll-like receptor (TLR) sequences, more than 200 Nod-like receptors and 1095 scavenger receptor cysteine-rich domains, a 10-fold expansion relative to vertebrates. Given their stereotypic protein structure and simple intron-exon architecture, the TLRs are the most tractable of these families for more detailed analysis. A role for these receptors in immune defense is suggested by their similarity to TLRs in other organisms, sequence diversity, and expression in immunologically active tissues, including phagocytes. The complexity of the sea urchin TLR multigene families is largely derived from expansions independent of those in vertebrates and protostomes, although a small family of TLRs with structure similar to that of Drosophila Toll can be traced to an ancient eumetazoan ancestor. Several other echinoderm sequences are now available, including Lytechinus variegatus, as well as partial sequences from two other sea urchin species. Here, we present an analysis of the invertebrate deuterostome TLRs with emphasis on the echinoderms. Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences). The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level. These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

No MeSH data available.