Evolution of chick type I procollagen genes

Benveniste-Schrode, Kathy; Doering, Jeffrey L.; Schrode, James; Kendra, Kari; Drexler, Bonnie K.

doi:10.1007/bf02099750

Cited by 6 publications

(3 citation statements)

References 30 publications

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“…The average fibril diameter for control and patient specimens is 110 nm and 70 nm, respectively evolved by sequential duplication of an ancestral 54-bp sequence from which all helix-encoding exons are derived (Yamada et al 1980). Although there is debate regarding the role and timing of the appearance of introns in this evolutionary process (Benveniste-Schrode et al 1985;Tate et al 1983;Ramirez et al 1985;Vuorio and de Crombrugge 1990), it is evident that unequal recombination involving intronic sequences ensures that the translational reading frame is maintained. Our demonstration of a large multi-exon duplication that causes only mild phenotypic manifestations appears to support the notion that recombination events that lead to gene expansion may have been important in collagen evolution and need not be associated with severe disease.…”

Section: Discussionmentioning

confidence: 98%

Partial COL1A2 gene duplication produces features of osteogenesis imperfecta and Ehlers-Danlos syndrome type VII

Raff¹,

Craigen²,

Smith³

et al. 2000

Human Genetics

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Type I collagen is the most abundant structural protein in the mammalian body. It exists as a heterotrimer of two subunits in the form [alpha1(I)]2alpha2(I). Pathogenic mutations in COL1A1 and COL1A2, the genes that encode the two subunits, cause a range of phenotypes including mild to lethal forms of osteogenesis imperfecta and a restricted set of Ehlers-Danlos syndrome phenotypes. Lethal mutations usually result from missense mutations that disrupt the normal triple helical structure of the molecule. Multi-exon duplication or deletion in type I collagen genes has rarely been observed and has generally resulted in a lethal or severe phenotype. We report a partial duplication in the COLIA2 gene that causes a relatively mild phenotype, despite the addition of 477 amino acids to the triple helical domain of the proalpha2(I) chain. The abnormal molecule is synthesized and secreted by cultured dermal fibroblasts in a normal fashion. Electron microscopy of dermal tissue reveals small but otherwise near normal collagen fibrils. The gene duplication occurred by mitotic sister chromatid exchange in the mother who is mosaic for the duplication allele. Examination of the abnormal sequence suggests a means by which the duplicated molecule could be processed and properly incorporated into mature collagen fibrils.

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Section: Discussionmentioning

confidence: 98%

Partial COL1A2 gene duplication produces features of osteogenesis imperfecta and Ehlers-Danlos syndrome type VII

Raff¹,

Craigen²,

Smith³

et al. 2000

Human Genetics

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“…It is worth noting that other exons that are multiples of 18 bp (36 and 72 bp) have been described in COL9A2, COLJJA2, COLM2AJ, and COLJ3AI genes (8,(10)(11)(12)(13). It is generally admitted that the 54-bp unit is itself the result of amplification events (9) of a primordial unit such as a 9-mer GGN CCN CCN oligonucleotide, coding for the triplet Gly-Pro-Pro (44,45). Interestingly, the 18-bp sponge exon encodes the sequence Gly-Pro-Pro-Gly-Pro-Thr.…”

Section: Discussionmentioning

confidence: 99%

Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families.

Exposito¹,

Garrone²

1990

Proc. Natl. Acad. Sci. U.S.A.

131

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We have characterized cDNA and genomic clones coding for a sponge collagen. The partial cDNA has an open reading frame encoding 547 amino acid residues. The conceptual translation product contains a probably incomplete triple-helical domain (307 amino acids) with one Gly-Xaa-YaaZaa imperfection in the otherwise perfect Gly-Xaa-Yaa repeats and a carboxyl propeptide (240 amino acids) that includes 7 cysteine residues. Amino acid sequence comparisons indicate that this sponge collagen is homologous to vertebrate and sea urchin fibrillar coliagens. Partial characterization of the corresponding gene reveals an intron-exon organization clearly related to the fibrillar collagen gene family. The exons coding for the triple-helical domain are 54 base pairs (bp) or multiples thereof, except for a 57-bp exon containing the Gly-Xaa-YaaZaa coding sequence and for two unusual exons of 126 and 18 bp, respectively. This latter 18-bp exon marks the end of the triple-helical domain, contrary to the other known ribriflar collagen genes that contain exons coding for the junction between the triple-helical domain and the carboxyl propeptide. Compared to other fibrillar collagen genes, the introns are remarkably small. Hybridization to blotted RNAs established that the gene transcript is 4.9 kilobases. Together with previous results that showed the existence of a nonfibrillar collagen in the same species, these data demonstrate that at least two collagen gene families are represented in the most primitive metazoa.Collagens are multidomain, interactive proteins that constitute the main extracellular component of all multicellular animals (1). So far, 13 different collagen types have been described in vertebrates, most of them forming polymeric structures or being closely associated with other collagenous polymers. Collagen molecules are made of three a chains, which may or may not be identical. They are characterized by the presence of triple-helical domains, which contain GlyXaa-Yaa repeats, that are essential for helix formation (2). More than 20 genes encode the different a chains. With the exception of the gene coding for type X collagen (3, 4), the described collagen coding genes have a complex exon-intron organization. Among them, the genes coding for the fibrilforming collagens (types I, II, III, V, and XI) have a homologous organization (5-8) with, in particular, triple-helix coding exons related to a 54-base-pair (bp) unit. These exons are believed to have evolved from an ancestral unit of 54 bp encoding six Gly-Xaa-Yaa repeats (9). The nonfibrillar collagen genes examined so far have more variable structures even though a few 54-bp exon units have been described (10-13).Very few data have been reported on the collagen gene organization in invertebrates. Variable exon sizes have been found in the nonfibrillar collagen genes, either in Drosophila melanogaster (14)(15)(16) or in Caenorhabditis elegans (17, 18), contrary to the multiple 54-bp motif described recently in a fibrillar collagen gene of the sea urchin Paracen...

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“…It has been hypothesized that this structure arose by tandem duplication ofan ancestral 54-bp exon (36). The internally repetitive nature of fibrillar collagen gene exons has suggested that recombination between Gly-Xaa-Yaa-encoding sequences may have been responsible for the generation of the 54-bp ancestral exon from a 9-bp precursor (38) as well as exon sizes different from the 54-base-pair unit (36). Surprisingly, the deletions described to date in the type I and type III collagen genes have their endpoints within introns (10,31,32).…”

Section: Resultsmentioning

confidence: 99%

Tandem duplication within a type II collagen gene (COL2A1) exon in an individual with spondyloepiphyseal dysplasia.

Tiller

Rimoin

Murray

et al. 1990

Proc. Natl. Acad. Sci. U.S.A.

116

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We have characterized a mutation in the type II collagen gene (COL2AJ) that produces a form of spondyloepiphyseal dysplasia. The mutation is an internal tandem duplication of 45 base pairs within exon 48 and results in the addition of 15 amino acids to the triple-helical domain of the al chains of type II collagen derived from the abnormal allele.Although the repeating (Gly-Xaa-Yaa)1. motif that characterizes the triple-helical domain is preserved, type H collagen derived from cartilage of the affected individual contains a population with excessive posttranslational modification, consistent with a disruption in triple-helix structure. The mutation is not carried by either parent, indicating that the phenotype in the affected individual is due to a new dominant mutation. DNA sequence homology in the area of the duplication suggests that the mutation may have arisen by unequal crossover between related sequences, a proposed mechanism in the evolution and diversification of the collagen gene family.The spondyloepiphyseal dysplasias (SEDs) are a heterogeneous subgroup of the skeletal dysplasias whose cardinal features include abnormal epiphyses, flattened vertebral bodies, and ocular involvement that ranges from myopia to vitreo-retinal degeneration (1). Since type II collagen is found in a restricted set of tissues that includes articular cartilage, the nucleus pulposus of the spine, and the vitreous of the eye (2), the concordance between the clinical findings and the distribution of the protein suggests that a primary defect of type II collagen may be responsible for some of these disorders. Structurally abnormal type II collagen has been isolated from cartilage ofindividuals with SED (3, 4), spondyloepimetaphyseal dysplasia (3,4), and achondrogenesishypochondrogenesis (5). Combined with the demonstration of linkage of markers in the COL2AJ gene with a form of familial osteoarthritis (6) and with Stickler syndrome (7,8), these studies have suggested that mutations in the type II collagen gene may underlie a spectrum of disorders that span a broad range of clinical severity.Type II collagen is a fibrillar collagen that in its mature form is a homotrimer ofal(II) chains (9). Biochemical studies have shown that cartilage from individuals with either SED (3, 4) or achondrogenesis-hypochondrogenesis (5) contains type II collagen with both slowly migrating and normally migrating al(II) chains. Amino acid analyses of the abnormal type II collagen from the affected individuals have shown that there is increased lysyl hydroxylation (3-5), suggesting that the more slowly migrating population is derived from molecules containing a chain with a defect that affects triple-helix structure and/or assembly. These results are conceptually homologous to the consequences of defects in type I collagen that produce osteogenesis imperfecta, in which mutations that alter triple-helix structure result in excessive posttranslational modification of all chains in molecules that incorporate at least one abnormal chain (10, 11). Th...

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Evolution of chick type I procollagen genes

Cited by 6 publications

References 30 publications

Partial COL1A2 gene duplication produces features of osteogenesis imperfecta and Ehlers-Danlos syndrome type VII

Partial COL1A2 gene duplication produces features of osteogenesis imperfecta and Ehlers-Danlos syndrome type VII

Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families.

Tandem duplication within a type II collagen gene (COL2A1) exon in an individual with spondyloepiphyseal dysplasia.

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