Distinct expression of type XIII collagen in neuronal structures and other tissues during mouse development

Sund, Malin; Väisänen, Timo; Kaukinen, Sami; Ilves, Mika; Tu, Hongmin; Autio–Harmainen, Helena; Rauvala, Heikki; Pihlajaniemi, Taina

doi:10.1016/s0945-053x(01)00134-2

Cited by 67 publications

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“…Type XIII collagen has a wide tissue distribution and has been localized to many sites of cell-matrix interaction in tissues and organs such as the myotendinous junctions in skeletal muscle and at some cell-cell interaction sites such as the intercalated disc of heart muscle (12)(13)(14)(15). Type XIII collagen has been localized to focal adhesions in cultured fibroblasts (14).…”

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confidence: 99%

The Type XIII Collagen Ectodomain Is a 150-nm Rod and Capable of Binding to Fibronectin, Nidogen-2, Perlecan, and Heparin

Tu¹,

Sasaki²,

Snellman³

et al. 2002

Journal of Biological Chemistry

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Type XIII collagen consists of a short N-terminal intracellular domain, a transmembrane domain, and a collagenous ectodomain, and it is found at many sites of cell adhesion. We report on the characterization of recombinant type XIII collagen. The shed ectodomain was purified from insect cell culture medium and shown to form 240-kDa trimers with a T m of 42°C. Correct chain association into a triple-helical conformation was confirmed by limited pepsin digestion and CD spectroscopy. Rotary shadowing electron microscopy of the ectodomain revealed it to be a 150-nm rod with two flexible hinges separating 31-, 52-, and 68-nm portions. The rods represent the collagenous domains 1-3, and the hinges coincide with the non-collagenous domains 2 and 3. By using surface plasmon resonance analysis, the ectodomain showed interaction with immobilized fibronectin, nidogen-2, and perlecan with K D values in the nanomolar range. The binding sites of type XIII collagen for fibronectin were localized to the collagenous domains, whereas the binding activities for nidogen-2 and perlecan resided in the pepsin-sensitive portions of the ectodomain. Furthermore, the ectodomain bound significantly to heparin, which also inhibited shedding of the ectodomain in insect cell cultures. The results reveal that type XIII collagen is notably distinct in its structure compared with other cell-surface proteins, and the in vitro binding with fibronectin, heparin, and two basement membrane components is indicative of multiple cell-matrix interactions in which this ubiquitously expressed protein participates.Two of the 19 collagens described in vertebrates belong to the subgroup of transmembrane collagens, namely type XIII and the hemidesmosomal component, type XVII collagen (1-3). These two nonfibrillar collagens are not structurally homologous except that both have a transmembrane domain. The collagen superfamily also includes other transmembrane proteins that have short collagenous domains, namely the types I and II macrophage scavenger receptors; C1q, the first component of complement C1; a macrophage receptor with a collagenous structure; and the ectodysplasin-A family of proteins (1, 3, 4).Type XIII collagen molecules reside in the plasma membrane of cells in a type II orientation with a short N-terminal cytosolic domain, a single transmembrane domain, and a large, mainly collagenous ectodomain (5, 6). The N-terminal non-collagenous domain, NC1, 1 of the human protein encompasses a 38-residue cytosolic domain, a 23-residue transmembrane domain, and the first 60 residues of the non-collagenous extracellular sequences adjacent to the plasma membrane (5). The rest of the ectodomain contains three collagenous sequences, COL1-3, with sizes of 104, 172, and 235 residues, respectively, and non-collagenous domains, NC2-4, with sizes of 34, 22, and 18 residues (5). The precursor RNAs encoding human and mouse type XIII collagen are known to be subject to complex alternative splicing, and hence the sizes of the COL1, NC2, COL3, and NC4 domains in humans ca...

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The Type XIII Collagen Ectodomain Is a 150-nm Rod and Capable of Binding to Fibronectin, Nidogen-2, Perlecan, and Heparin

Tu¹,

Sasaki²,

Snellman³

et al. 2002

Journal of Biological Chemistry

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“…: 358-8-5375800; Fax: 358-8-5375810; E-mail: taina.pihlajaniemi@oulu.fi. 1 The abbreviations used are: COL, collagenous domain; NC, noncollagenous domain; m.o.i., multiplicity of infection; PBS, phosphatebuffered saline; 4PH, prolyl 4-hydroxylase; MSRs, macrophage scavenger receptors; MES, 4-morpholineethanesulfonic acid; SRCL, scavenger receptor with C-type lectin. …”

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“…Type XIII collagen is a type II transmembrane protein that is expressed in many tissues throughout development and adult life (1). It is located in focal adhesions of cultured fibroblasts and other cells and in adhesive structures of tissues such as the myotendinous junctions in muscle, intercalated discs in heart, and the cell basement membrane interphases (1,2).…”

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“…It is located in focal adhesions of cultured fibroblasts and other cells and in adhesive structures of tissues such as the myotendinous junctions in muscle, intercalated discs in heart, and the cell basement membrane interphases (1,2). The type XIII collagen ectodomain can bind to fibronectin, heparin, the basement membrane components nidogen-2 and perlecan, and the ␣ 1 -subunit of integrin (3)(4)(5).…”

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Type XIII Collagen and Some Other Transmembrane Collagens Contain Two Separate Coiled-coil Motifs, Which May Function as Independent Oligomerization Domains

Latvanlehto¹,

Snellman²,

et al. 2003

Journal of Biological Chemistry

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Type XIII collagen is a homotrimeric transmembrane collagen composed of a short intracellular domain, a single membrane-spanning region, and an extracellular ectodomain with three collagenous domains (COL1-3) separated by short non-collagenous domains (NC1-4). Several collagenous transmembrane proteins have been found to harbor a conserved sequence next to their membrane-spanning regions, and in the case of type XIII collagen this sequence has been demonstrated to be important for chain association. We show here that this 21-residue sequence is necessary but not sufficient for NC1 association. Furthermore, the NC1 association region was predicted to form an ␣-helical coiled-coil structure, which may already begin at the membrane-spanning region, as is also predicted for the related collagen types XXIII and XXV. Interestingly, a second coiled-coil structure is predicted to be located in the NC3 domain of type XIII collagen and in the corresponding domains of types XXIII and XXV. It is found experimentally that the absence of the NC1 coiled-coil domain leads to a lack of disulfide-bonded trimers and misfolding of the membrane-proximal collagenous domain COL1, whereas the COL2 and COL3 domains are correctly folded. We suggest that the NC1 coiled-coil domain is important for association of the N-terminal part of the type XIII collagen ␣ chains, whereas the NC3 coiled-coil domain is implicated in the association of the C-terminal part of the molecule. All in all, we propose that two widely separated coiled-coil domains of type XIII and related collagens function as independent oligomerization domains participating in the folding of distinct areas of the molecule.Type XIII collagen is a type II transmembrane protein that is expressed in many tissues throughout development and adult life (1). It is located in focal adhesions of cultured fibroblasts and other cells and in adhesive structures of tissues such as the myotendinous junctions in muscle, intercalated discs in heart, and the cell basement membrane interphases (1, 2). The type XIII collagen ectodomain can bind to fibronectin, heparin, the basement membrane components nidogen-2 and perlecan, and the ␣ 1 -subunit of integrin (3-5). Due to its location at the tissue and cell level and its binding properties, it has been postulated that type XIII collagen is involved in cellular adhesion and migration.Type XIII collagen ␣ chains produced in a recombinant insect cell culture system have been shown to form homotrimers (6). The primary structure is composed of three collagenous domains (COL1 1 to COL3), which are flanked and interrupted by non-collagenous domains (NC1 to NC4). The short cytosolic domain and the transmembrane domain encompass about half of the NC1 domain, whereas the rest of the molecule forms the ectodomain, which is a rod of about 150 nm with two flexible hinges coinciding with the NC2 and NC3 domains (5). The primary structures of COL1, NC2, COL3, and NC4 can vary, on account of complex alternative splicing (7-10). It has been shown recently that ext...

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“…As development proceeds, it is found in developing bone, cartilage, intestine, skeletal muscle, lung, and skin, with clear developmental shifts in expression pattern. 16 To understand the biological function of type XIII collagen, we have generated a mouse strain that expresses it in an N-terminally altered form through site-specific Cre-loxP-mediated deletion of exon 1 sequences in embryonic stem (ES) cells. The data suggest a role for the cytosolic and transmembrane domains in skeletal muscle integrity.…”

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Lack of Cytosolic and Transmembrane Domains of Type XIII Collagen Results in Progressive Myopathy

Kvist¹,

Latvanlehto²,

Sund³

et al. 2001

The American Journal of Pathology

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Type XIII collagen is a type II transmembrane protein found at many sites of cell adhesion in tissues. Homologous recombination was used to generate a transgenic mouse line (Col13a1 N/N ) that expresses N-terminally altered type XIII collagen molecules lacking the short cytosolic and transmembrane domains but retaining the large collagenous ectodomain. The mutant molecules were correctly transported to focal adhesions in cultured fibroblasts derived from the Col13a1 N/N mice, but the cells showed decreased adhesion when plated on type IV collagen. These mice were viable and fertile, and in immunofluorescence stainings the mutant protein was located in adhesive tissue structures in the same manner as normal ␣1(XIII) chains. In immunoelectron microscopy of wild-type mice type XIII collagen was detected at the plasma membrane of skeletal muscle cells whereas in the mutant mice the protein was located in the adjacent extracellular matrix. Affected skeletal muscles showed abnormal myofibers with a fuzzy plasma membrane-basement membrane interphase along the muscle fiber and at the myotendinous junctions, disorganized myofilaments, and streaming of z-disks. The findings were progressive and the phenotype was aggravated by exercise. Thus type XIII collagen seems to participate in the linkage between muscle fiber and basement membrane, a function impaired by lack of the cytosolic and transmembrane domains. The collagen superfamily of proteins consists of more than 19 types of collagen and several other proteins with collagen-like domains.1 Type XIII collagen and the hemidesmosomal component type XVII collagen form a subfamily of transmembrane collagens. 2 The genes of human and mouse type XIII collagen are 135 to 138 kb in size, consisting of 42 exons, and they are localized to chromosome 10 in both species.3-5 The encoded type XIII collagen consists of three collagenous domains (COL1 to COL3) separated and flanked by four noncollagenous domains (NC1 to NC4). 6,7 The precursor RNAs that encode type XIII collagen undergo complex alternative splicing, which is predicted to affect the structures of the COL1, NC2, and COL3 domains of the human and mouse chains. 5,6,8 -10 Type XIII collagen produced in insect cells forms ␣1(XIII) homotrimers, and the three collagenous domains fold into a stable triple-helical conformation. 11 The type XIII collagen molecules have been shown to reside on the plasma membranes of cells in a type II orientation with a short N-terminal cytosolic portion, a transmembrane domain, and an extensive collagenous ectodomain.12 Sequences that are important for association of the three ␣1(XIII) chains reside in the Nterminal region, and hence triple helix formation is thought to proceed from the N terminus to the C terminus, in the opposite orientation to that known to occur in the fibrillar collagens.12 The extracellular ligands of type XIII collagen have not been identified, but recent studies with recombinant protein demonstrate that its ectodomain interacts strongly with the I domain of ␣1 integrin. ...

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Distinct expression of type XIII collagen in neuronal structures and other tissues during mouse development

Cited by 67 publications

References 36 publications

The Type XIII Collagen Ectodomain Is a 150-nm Rod and Capable of Binding to Fibronectin, Nidogen-2, Perlecan, and Heparin

The Type XIII Collagen Ectodomain Is a 150-nm Rod and Capable of Binding to Fibronectin, Nidogen-2, Perlecan, and Heparin

Type XIII Collagen and Some Other Transmembrane Collagens Contain Two Separate Coiled-coil Motifs, Which May Function as Independent Oligomerization Domains

Lack of Cytosolic and Transmembrane Domains of Type XIII Collagen Results in Progressive Myopathy

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