Collagen XXIV, a Vertebrate Fibrillar Collagen with Structural Features of Invertebrate Collagens: SELECTIVE EXPRESSION IN DEVELOPING CORNEA AND BONE*

Manuel Koch,Friedrich Laub,Peihong Zhou,Rita A Hahn,Shizuko Tanaka,Robert E Burgeson,Donald R Gerecke,Francesco Ramirez,Marion K Gordon

doi:10.1074/jbc.m302112200

Abstract

Tissue-specific assembly of fibers composed of the major collagen types I and II depends in part on the formation of heterotypic fibrils, using the quantitatively minor collagens V and XI. Here we report the identification of a new fibrillar-like collagen chain that is related to the fibrillar alpha1(V), alpha1(XI), and alpha2(XI) collagen polypeptides and which is coexpressed with type I collagen in the developing bone and eye. The new collagen was designated the alpha1(XXIV) chain and consists of a long triple helical domain flanked by typical propeptide-like sequences. The carboxyl propeptide is classic, with 8 conserved cysteine residues. The amino-terminal peptide contains a thrombospodin-N-terminal-like (TSP) motif and a highly charged segment interspersed with several tyrosine residues, like the fibril diameter-regulating collagen chains alpha1(V) and alpha1(XI). However, a short imperfection in the triple helix makes alpha1(XXIV) unique from other chains of the vertebrate fibrillar collagen family. The triple helical interruption and additional select features in both terminal peptides are common to the fibrillar chains of invertebrate organisms. Based on these data, we propose that collagen XXIV is an ancient molecule that may contribute to the regulation of type I collagen fibrillogenesis at specific anatomical locations during fetal development.

Highlights

Tissue-specific assembly of fibers composed of the major collagen types I and II depends in part on the formation of heterotypic fibrils, using the quantitatively minor collagens V and XI
Once it became clear from sequence analysis that the cDNAs did, represent novel collagens, they were designated as the ␣1 chains for the available numbers in the collagen family, i.e. types XXII, XXIII, and XXIV. (The structures of collagens XXV–XXVII have since been elucidated (6 –9).) The ␣1(XXII) collagen chain, composed of four triple helical domains,2 is related in sequence to FACIT-like collagens XVI and XIX [35,36,37]. ␣1(XXIII) collagen [38] is part of a transmembrane trimeric molecule similar to collagens XIII and XXV [6, 39, 40]
Together with the newly described chain of collagen XXVII [8, 9], collagen XXIV represents a separate clade within the fibrillar group of collagens

Summary

SELECTIVE EXPRESSION IN DEVELOPING CORNEA AND BONE*

The triple helical interruption and additional select features in both terminal peptides are common to the fibrillar chains of invertebrate organisms Based on these data, we propose that collagen XXIV is an ancient molecule that may contribute to the regulation of type I collagen fibrillogenesis at specific anatomical locations during fetal development. Fibers are organized into specific spatial arrays that are responsible for the properties of individual tissues It follows that the regulation of fibril diameter is an important determinant of connective tissue function. Types V and XI collagen most likely serve as fibril diameter regulators because they retain a bulky amino-terminal portion attached to the triple helix after their final extracellular processing [17, 19]. The ␣1(XXIV) chain displays structural features unique to invertebrate fibrillar collagens

EXPERIMENTAL PROCEDURES

RESULTS

DISCUSSION