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Int J Mol Sci
2010 Jan 28;112:407-26. doi: 10.3390/ijms11020407.
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The fibrillar collagen family.
Exposito JY
,
Valcourt U
,
Cluzel C
,
Lethias C
.
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Collagens, or more precisely collagen-based extracellular matrices, are often considered as a metazoan hallmark. Among the collagens, fibrillar collagens are present from sponges to humans, and are involved in the formation of the well-known striated fibrils. In this review we discuss the different steps in the evolution of this protein family, from the formation of an ancestral fibrillar collagen gene to the formation of different clades. Genomic data from the choanoflagellate (sister group of Metazoa) Monosiga brevicollis, and from diploblast animals, have suggested that the formation of an ancestral alpha chain occurred before the metazoan radiation. Phylogenetic studies have suggested an early emergence of the three clades that were first described in mammals. Hence the duplication events leading to the formation of the A, B and C clades occurred before the eumetazoan radiation. Another important event has been the two rounds of "whole genome duplication" leading to the amplification of fibrillar collagen gene numbers, and the importance of this diversification in developmental processes. We will also discuss some other aspects of fibrillar collagen evolution such as the development of the molecular mechanisms involved in the formation of procollagen molecules and of striated fibrils.
Figure 1. Fibrillar collagen characteristics. (A) From fibrillar α chains to the striated fibrils. To illustrate the different steps leading to the formation of collagen fibrils, we have chosen human type I collagen. After the selection of appropriate α chains, the C-propeptides play a fundamental role in alignment and registration of α chains, permitting nucleation of the triple helix and its elongation in a C- to a N-terminal direction. Then, the procollagens are processed by N- and C-proteinases, and the resultant collagen molecules aggregate to form the fibrils. (B) Modular structures of human fibrillar collagen chains. Dashed lines are used to illustrate the three different N-propeptide modular configurations found in human types I–III, V and XI. (C) Different N-propeptide architectures of metazoan fibrillar collagen chains. (+) indicates that at least one α chain presents this type of N-propeptide. In the case of cnidarian data, (+?a) signifies that these N-propeptide modular structures have not been characterized to date, but are present either in hydra or in sea anemone. (?b) indicates that phylogenetic analysis has indicated that the sea urchin 7α chain is related to vertebrate types XXIV and XXVII, but that the N-propeptide of this fibrillar collagen is still unknown [12].
Figure 2. Multiple alignments of C-propeptide (COLF1) domains. (A) Selected human (Hsa) and choanoflagellate (Mbr, Monosiga brevicolis) COLF1 domains are aligned. Residues that are perfectly conserved among these proteins are shaded in yellow. Cysteine residues are colored in red and numbered. The grey boxes represent the chain selectivity recognition domains identified by Lees et al. [24]. (B) Chain recognition sequences in Metazoa. This sequence alignment is based on previous studies [12,25].
Figure 3. The sea urchin 1α fibrillar collagen chain. (A) Modular structure of the 1α chain. Domains are illustrated as in Figure 1. (B) the exon/intron structure of COLP1α, the gene encoding the S. purpuratus 1α chain. The COLP1α sequence is available using a sea urchin server (http://genome.ucsc.edu/cgi-bin/hgGateway; Scaffold69286:454253-495522 bp). Exons are represented by closed boxes. Below the COLP1α gene, the short and putative long mRNA isoforms are schematized. The four ESTs specific to the long 1α mRNA isoform are indicated with their accession number. (C) Northern-blot analysis of 1α mRNA. A short-exposure time of this Northern-blot was shown previously [34]. Here, we present different times of autoradiography, from 2 h to 72 h.
Figure 4. Hypothetical steps leading to the formation of an ancestral fibrillar collagen gene.
Figure 5. Phylogenetic analysis of some metazoan fibrillar collagen chains. This unrooted tree was modified from a previous study [30]. The illustration was drawn using the TreeDyn program [49]. Gray boxes indicate the ascidian fibrillar collagen chains.
Figure 6. Evolution of the fibrillar collagen family. This model was modified from a previous study [30]. It should be followed from the bottom to the top. In this model, we suggest that the steps leading to the formation of an ancestral α chain occurred before the metazoan radiation and the divergence of the three clades predated the Parazoa-Eumetazoa split. The different steps (emergence of the different clades, module or chain selection sequence acquisition) are presented. We have two major hypotheses concerning the B/C clades. In the H1 scenario, sponges possess fibrillar collagen chains containing a TSPN module and the related genes have duplicated before the divergence of the B and the C clades from an ancestral B/C clade gene. In this hypothesis, the emergence of the B and C clades occurred between Parazoa-Eumetazoa and Cnidaria-Bilateria split. In hypothesis H2, B and C clade genes are present in demosponges and their emergence predated metazoan cladogenesis.
Figure 7. Simplified Eukarya tree of life with a special focus on the kingdom Animalia. Most of the animals discussed in the text are represented. This tree is based on several studies [51–58]. Sponges are presented as a monophyletic group [57].
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