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BACKGROUND: Proteomic studies of skeletal proteins have revealed large, complex mixtures of proteins occluded within the mineral. Many skeletal proteomes contain rapidly evolving proteins with repetitive domains, further complicating our understanding. In echinoderms, proteomic analysis of the skeletal proteomes of mineralized tissues of the sea urchin Strongylocentrotus purpuratus prominently featured spicule matrix proteins with repetitive sequences linked to a C-type lectin domain. A comparative study of the brittle star Ophiocoma wendtii skeletal proteome revealed an order of magnitude fewer proteins containing C-type lectin domains. A number of other proteins conserved in the skeletons of the two groups were identified. Here we report the complete skeletal proteome of the sea star Patiria miniata and compare it to that of the other echinoderm groups.
RESULTS: We have identified eighty-five proteins in the P. miniata skeletal proteome. Forty-two percent of the proteins were determined to be homologous to proteins found in the S. purpuratus skeletal proteomes. An additional 34 % were from similar functional classes as proteins in the urchin proteomes. Thirteen percent of the P. miniata proteins had homologues in the O. wendtii skeletal proteome with an additional 29% showing similarity to brittle star skeletal proteins. The P. miniata skeletal proteome did not contain any proteins with C-lectin domains or with acidic repetitive regions similar to the sea urchin or brittle star spicule matrix proteins. MSP130 proteins were also not found. We did identify a number of proteins homologous between the three groups. Some of the highly conserved proteins found in echinoderm skeletons have also been identified in vertebrate skeletons.
CONCLUSIONS: The presence of proteins conserved in the skeleton in three different echinoderm groups indicates these proteins are important in skeleton formation. That a number of these proteins are involved in skeleton formation in vertebrates suggests a common origin for some of the fundamental processes co-opted for skeleton formation in deuterostomes. The proteins we identify suggest transport of proteins and calcium via endosomes was co-opted to this function in a convergent fashion. Our data also indicate that modifications to the process of skeleton formation can occur through independent co-option of proteins following species divergence as well as through domain shuffling.
Fig. 1. SDS-PAGE gel of Patiria miniata skeletal proteins. Lane 1; Molecular weight markers, Lane 2: P. miniata proteins. Molecular weights of marker bands are indicated on the left of the gel. The position of gel fractions separated prior to LC/MS/MS are indicated on the right of the gel
Fig. 2. Functional classes of proteins identified in the skeletal proteomes of sea stars and sea urchins. a The functional classes of proteins in the Patiria miniata skeletal proteome. b The functional classes of proteins found in the Strongylocentrotus purpuratus test and spine skeletal proteome
Fig. 3. Phylogenetic relationship of echinoderm fibrinogen C domain containing proteins. A maximum likelihood tree was produced using proteins found in Patiria miniata = PMI, Ophiocoma wendtii = Ow and Strongylocentrotus purpuratus = Sp. PMI_010282 contains four domains which were separated into A, B, C and D for this analysis. All proteins used are found within the skeletal proteome except for the S. pupuratus proteins indicated by the box
Fig. 4. Domain structure and relationship to similar proteins of a novel protease conserved in echinoderm skeletal proteomes. a Domain organization of the S. purpuratus and P. miniata proteins. b A maximum likelihood tree showing related proteases in multiple species. PM = Patiria miniata, SP = Strongylocentrous purpuratus, Pm = Polyandrocarpa misakiensis, Cg = Crassostrea gigasI, Hs = Homo sapiens, Dp = Daphnia pulex, Cs = Caenorhabditus elegans
Fig. 5. Conserved structure of Frem/Fras proteins found in echinoderm skeletal proteomes. a Domain structure of the Patiria miniata Fras homologue. b The amino acid identity of echinoderm and human Fras proteins compared to the P. miniata protein
Fig. 6.
Patiria miniata (PM) Ldl-receptor-like proteins (Lrp). a Domain structure of the most prevalent Lrp-like proteins in Patiria miniata (PM) and Strongylocentrotus purpuratus (Sp). b A maximum likelihood tree of Lrp-like proteins found in skeletal proteomes compared to Human LRP proteins involved in bone formation. Hs = Homo sapiens
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