Primary structure of the long and short splice variants of mouse collagen XII and their tissue‐specific expression during embryonic development

Böhme, Kathrin; Li, Yefu; Oh, Paul; Olsen, Bjørn R.

doi:10.1002/aja.1002040409

Cited by 52 publications

(46 citation statements)

References 22 publications

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“…Collagen XII is also a FACIT collagen with four VWA domains (15). Using the short splice variant of collagen XII molecule lacking the first two VWA domains we demonstrated cysteine-rich domain-mediated binding to collagen XII with subsequent proteolytic cleavages localized in the VWA4 domain, again indicating PIII SVMP cysteine-rich domain interaction with VWA domains.…”

Section: Discussionmentioning

confidence: 84%

“…Among the VWA-containing proteins are the fibril-associated collagens with interrupted triple helices (FACITs) that form a subclass of collagens characterized by the presence of more than one triple helical domain separated by non-triple helical segments. FACIT collagens XII (12) and XIV (13,14) have one domain that anchors the molecule to the surface of the fibril and three "finger-like" domains containing VWA-like regions (15).…”

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confidence: 99%

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The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

Serrano

Kim

Wang

et al. 2006

Journal of Biological Chemistry

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Snake venom metalloproteinases (SVMPs) are members of the Reprolysin family of metalloproteinases to which the ADAM (a disintegrin and metalloproteinase) proteins also belong. The disintegrin-like/cysteine-rich domains of the ADAMs have been implicated in their function. In the case of the SVMPs, we hypothesized that these domains could function to target the metalloproteinases to key extracellular matrix proteins or cell surface proteins. Initially we detected interaction of collagen XIV, a fibril-associated collagen with interrupted triple helices containing von Willebrand factor A (VWA) domains, with the PIII SVMP catrocollastatin. Next we investigated whether other VWA domain-containing matrix proteins could support the binding of PIII SVMPs. Using surface plasmon resonance, the PIII SVMP jararhagin and a recombinant cysteine-rich domain from a PIII SVMP were demonstrated to bind to collagen XIV, collagen XII, and matrilins 1, 3, and 4. Jararhagin was shown to cleave these proteins predominantly at sites localized at or near the VWA domains suggesting that it is the VWA domains to which the PIII SVMPs are binding via their cysteine-rich domain. In light of the fact that these extracellular matrix proteins function to stabilize matrix, targeting the SVMPs to these proteins followed by their specific cleavage could promote the destabilization of extracellular matrix and cell-matrix interactions and in the case of capillaries could contribute to their disruption and hemorrhage. Although there is only limited structural homology shared by the cysteine-rich domains of the PIII SVMPs and the ADAMs our results suggest an analogous function for the cysteine-rich domains in certain members of the expanded ADAM family of proteins to target them to VWA domain-containing proteins.One of the hallmarks of viperid envenoming is local hemorrhage caused by the snake venom metalloproteinases (SVMPs) 2 (1, 2). SVMPs are members of the Reprolysin subfamily of the M12 family of metalloproteinases (3). Of the SVMPs, the PIII class is distinguished by being comprised of proproteinase, proteinase, disintegrin-like, and cysteine-rich domains (4). The proteinase domain of all the SVMP hemorrhagic toxins is believed to function to degrade capillary basement membranes, endothelial cell surfaces, and stromal matrix ultimately causing extravasation of capillary contents into the surround stroma (5, 6). Interestingly the PIII class of SVMPs is typically much more potent in causing hemorrhage compared with the PI and PII classes that lack the cysteine-rich domain found in the PIII class (4) suggesting a role for this domain in the pathophysiology of the PIII hemorrhagic toxins. Indeed the disintegrin-like/cysteine-rich domains of certain hemorrhagic toxins have been shown to be potent inhibitors of collagen-induced platelet aggregation as a result of interaction of the cysteine-rich domain with the ␣2␤1 integrin on platelets (7,8). Proteolytic degradation of capillary basement membrane structures and inhibition of platelet aggregation have...

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Section: Discussionmentioning

confidence: 84%

mentioning

confidence: 99%

The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

Serrano

Kim

Wang

et al. 2006

Journal of Biological Chemistry

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“…Type XII collagen mRNA expression has been demonstrated in the periosteum, a site of active bone formation (Böhme et al, 1995). This suggests involvement of type XII collagen in the regulation of osteoblasts, including differentiation and maturation, alignment, polarization, and cell interactions.…”

Section: Altered Bone Formation In Type XII Collagen-null Micementioning

confidence: 96%

Type XII collagen regulates osteoblast polarity and communication during bone formation

Izu¹,

Sun²,

Zwolanek³

et al. 2011

J Exp Med

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Abbreviations used in this paper: CT, computed tomography; FACIT, fibrilassociated collagen with interrupted triple helices; HA, hydroxyapatite; H&E, hematoxylin and eosin; HU, Hounsfield unit; shRNA, short hairpin RNA; TMDn, tissue mineral density; TRAP, tartrate resistance acid phosphatase. IntroductionOsteoblast differentiation and maturation are crucial events in the formation of new bone and determination of bone quality (Nakashima et al., 2002;Yoshida et al., 2002;Komori, 2010). Bone formation begins with the differentiation of osteoblasts from pluripotent mesenchymal cells. The progenitors migrate to the sites of bone matrix deposition and differentiate into fully functional, bone matrix-producing osteoblasts (Imai et al., 1998). These events are regulated by the expression of runtrelated gene 2 (Runx2, also known as Cbfa1) and sp7 transcription factor (Sp7, also known as osterix) and by canonical Wnt signaling followed by the secretion of specific bone matrix proteins such as type I collagen (Col1a1), secreted phosphoprotein1 (Spp1, also known as osteopontin), integrin-binding sialoprotein (Ibsp), and bone -carboxyglutamate protein (Bglap, also known as osteocalcin; Harada and Rodan, 2003;Koga et al., 2005). In addition to these changes in gene expression and matrix protein secretion, the mature osteoblasts become aligned along regions of bone deposition with an epithelioid arrangement. The mature, terminally differentiated osteoblasts are highly polarized relative to the site of bone matrix deposition (Ilvesaro et al., 1999;Nakashima et al., 2002;Stains et al., 2002). These features are common to periosteal and endosteal bone and both long and flat bones. Therefore, the alignment, polarization, and interaction of osteoblasts are important events necessary for production of a functional bone matrix.Cell motility, communication, and shape are controlled via the local microenvironment where the extracellular matrix provides a substrate for cell anchorage, stores and presents growth factors or cytokines, and serves as a tissue scaffold (Rozario and DeSimone, 2010). The extracellular matrix interacts with the intracellular actin cytoskeleton via transmembrane proteins that affect cytoskeletal organization, cell motility and polarity, proliferation, and survival (Berthiaume et al., 1996;Geiger et al., 2001;Théry et al., 2005;Parsons et al., 2010;Kim et al., 2011). Thus, extracellular matrix-transmembrane protein-cytoskeleton D ifferentiated osteoblasts are polarized in regions of bone deposition, demonstrate extensive cell interaction and communication, and are responsible for bone formation and quality. Type XII collagen is a fibril-associated collagen with interrupted triple helices and has been implicated in the osteoblast response to mechanical forces. Type XII collagen is expressed by osteoblasts and localizes to areas of bone formation. A transgenic mouse null for type XII collagen exhibits skeletal abnormalities including shorter, more slender long bones with decreased mechanical strength as well as a...

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“…2A) (6). The isoforms differ in their histological and developmental distribution: the large forms XIIA-1 and XIIA-2 are preferably expressed during embryonic stages, whereas the expression of the small forms persists in adult tissues (7). Furthermore, the small isoform XIIB-1 predominantly occurs in ligaments and tendons, whereas the XIIB-2 shows a more widespread expression (6).…”

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confidence: 99%

Collagen XII Interacts with Avian Tenascin-X through Its NC3 Domain

Veit

Hansen

Keene

et al. 2006

Journal of Biological Chemistry

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Large oligomeric proteins often contain several binding sites for different molecules and can therefore induce formation of larger protein complexes. Collagen XII, a multidomain protein with a small collagenous region, interacts with fibrillar collagens through its C-terminal region. However, no interactions to other extracellular proteins have been identified involving the non-collagenous N-terminal NC3 domain. To further elucidate the components of protein complexes present close to collagen fibrils, different extracellular matrix proteins were tested for interaction in a solid phase assay. Binding to the NC3 domain of collagen XII was found for the avian homologue of tenascin-X that in humans is linked to Ehlers-Danlos disease. The binding was further characterized by surface plasmon resonance spectroscopy and supported by immunohistochemical co-localization in chick and mouse tissue. On the ultrastructural level, detection of collagen XII and tenascin-X by immunogold labeling confirmed this finding.The integrity of extracellular matrix is maintained by supramolecular networks assembled by a large variety of matrix macromolecules. Among those is the group of 28 different collagen types so far described in the literature. Collagens are further subdivided into several families reflecting their assemblyforming properties (1). As a common feature, fibril-associated collagens with interrupted triple helices (FACITs) 2 comprise at least two collagenous domains interrupted by non-collagenous domains. Collagen XII is a member of the FACIT subfamily, and its three chains are encoded by a single gene. The two collagenous domains (Col1 and Col2) are interrupted and flanked by three non-collagenous domains (NC1-NC3), of which the large trimeric NC3 domain contains up to 90% of the molecular mass of collagen XII. The N-terminal NC3 part of each polypeptide chain consists of two to four von Willebrand factor type A domains, several fibronectin type III repeats, and a thrombospondin N-terminal domain (2, 3). The size of the protein is variable due to two alternative splice sites located at the 5Ј-and 3Ј-ends of the collagen XII mRNA. Especially remarkable is the splicing mechanism that produces mRNA encoding for NC3 domains that differ ϳ100 kDa in mass, denoted as XIIA for the large form and as XIIB for the small form (4, 5). The other alternative splicing generates two NC1 domains of similar size, termed -1 or -2, which results in the nomenclature of the four different collagen XII isoforms: XIIA-1, XIIA-2, XIIB-1 and XIIB-2 (for overview of the domain structure please refer to Fig. 2A) (6). The isoforms differ in their histological and developmental distribution: the large forms XIIA-1 and XIIA-2 are preferably expressed during embryonic stages, whereas the expression of the small forms persists in adult tissues (7). Furthermore, the small isoform XIIB-1 predominantly occurs in ligaments and tendons, whereas the XIIB-2 shows a more widespread expression (6). The isoforms also differ in their biochemical properties. The ...

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Primary structure of the long and short splice variants of mouse collagen XII and their tissue‐specific expression during embryonic development

Cited by 52 publications

References 22 publications

The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

The Cysteine-rich Domain of Snake Venom Metalloproteinases Is a Ligand for von Willebrand Factor A Domains

Type XII collagen regulates osteoblast polarity and communication during bone formation

Collagen XII Interacts with Avian Tenascin-X through Its NC3 Domain

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