A quantitative analysis of the incorporation of fibulin-1 into extracellular matrix indicates that fibronectin assembly is required

Godyna, S

doi:10.1016/0945-053x(95)90004-7

Cited by 65 publications

(48 citation statements)

References 51 publications

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“…Plotted are the elution volumes versus their absorbance at 280 nm (mA units). Aliquots (20 l) from the elution volumes indicated were analyzed by silver staining after SDS gel electrophoresis under reducing (ϩ) and nonreducing ( 1993; Godyna et al, 1995), fibrinogen (Pereira et al, 2002), and LTBP-1 (Dallas et al, 2005). With fibronectin having a key role in the assembly of another important extracellular fibril system, the fibrillin-containing microfibrils, it becomes increasingly evident that fibronectin is a master orchestrator for the organization of various matrix components.…”

Section: Discussionmentioning

confidence: 99%

“…This portion of the molecule is directly followed by the binding site for collagen/gelatin, which is located between FNI 6 and FNI 9 (Engvall et al, 1978;Balian et al, 1979;Shimizu et al, 1997). Although a plethora of reports have been published on the initial assembly mechanisms for fibronectin, virtually nothing is known about how individual fibronectin molecules are spatially oriented and organized in early and fully assembled fibronectin networks.The assembly of a few extracellular matrix proteins have been demonstrated to be dependent on the presence of fibronectin, including collagen types I and III and thrombospondin-1 (McDonald et al, 1982;Sottile and Hocking, 2002;Velling et al, 2002; Li et al, 2003), fibulin-1 (Roman andMcDonald, 1993;Godyna et al, 1995), fibrinogen (Pereira et al, 2002), and LTBP-1 (Dallas et al, 2005). Further studies established for collagen type I, thrombospondin-1, and LTBP-1 that a continuous assembly and supply of fibronectin is a prerequisite for matrix stability of these proteins Dallas et al, 2005).…”

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confidence: 99%

“…The assembly of a few extracellular matrix proteins have been demonstrated to be dependent on the presence of fibronectin, including collagen types I and III and thrombospondin-1 (McDonald et al, 1982;Sottile and Hocking, 2002;Velling et al, 2002; Li et al, 2003), fibulin-1 (Roman andMcDonald, 1993;Godyna et al, 1995), fibrinogen (Pereira et al, 2002), and LTBP-1 (Dallas et al, 2005). Further studies established for collagen type I, thrombospondin-1, and LTBP-1 that a continuous assembly and supply of fibronectin is a prerequisite for matrix stability of these proteins Dallas et al, 2005).…”

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confidence: 99%

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Fibrillin Assembly Requires Fibronectin

Sabatier

Chen²,

Fagotto‐Kaufmann³

et al. 2009

MBoC

225

240

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Fibrillins constitute the major backbone of multifunctional microfibrils in elastic and nonelastic extracellular matrices. Proper assembly mechanisms are central to the formation and function of these microfibrils, and their properties are often compromised in pathological circumstances such as in Marfan syndrome and in other fibrillinopathies. Here, we have used human dermal fibroblasts to analyze the assembly of fibrillin-1 in dependence of other matrix-forming proteins. siRNA knockdown experiments demonstrated that the assembly of fibrillin-1 is strictly dependent on the presence of extracellular fibronectin fibrils. Immunolabeling performed at the light and electron microscopic level showed colocalization of fibrillin-1 with fibronectin fibrils at the early stages of the assembly process. Protein-binding assays demonstrated interactions of fibronectin with a C-terminal region of fibrillin-1, -2, and -3 and with an N-terminal region of fibrillin-1. The C-terminal half of fibrillin-2 and -3 had propensities to multimerize, as has been previously shown for fibrillin-1. The C-terminal of all three fibrillins interacted strongly with fibronectin as multimers, but not as monomers. Mapping studies revealed that the major binding interaction between fibrillins and fibronectin involves the collagen/ gelatin-binding region between domains FNI 6 and FNI 9 . INTRODUCTIONFibrillins are extracellular matrix components with important functions in elastic and nonelastic tissues including blood vessels, bone, and the eye. Fibrillins, together with the latent transforming growth factor-␤ (TGF-␤)-binding proteins (LTBPs), constitute the fibrillin-LTBP family of proteins (Hubmacher et al., 2006). Fibrillins are ϳ350 kDa in size, are disulfide-rich and glycosylated, and have a characteristic modular structure. The three human fibrillinsfibrillin-1, -2, and -3 -are encoded by different genes and are conserved at the amino acid level both in relation to one another and among species. Fibrillins are mainly composed of tandem arrays of calcium-binding epidermal growth factor-like domains interspersed with TGF-␤-binding protein domains (TB/8-Cys) and hybrid domains Hubmacher et al., 2006). Mutations in fibrillins give rise to the so-called fibrillinopathies, which include Marfan syndrome and autosomal dominant Weill-Marchesani syndrome, both caused by mutations in fibrillin-1, and Beal's syndrome, caused by mutations in fibrillin-2 (Robinson et al., 2006).High-molecular-weight, multiprotein assemblies called microfibrils are the functional units of fibrillins, which serve as a scaffold for the biogenesis of elastic fibers, confer structural integrity to individual organ systems, regulate growth factor signaling of TGF-␤-bone morphogenic protein (BMP) superfamily members and provide limited elasticity to tissues (Kielty et al., 2002;Charbonneau et al., 2004;Ramirez and Dietz, 2007). Extracted microfibrils from cell culture or tissues display a typical bead-on-a-string ultrastructure, having a 50 -55-nm periodicity when analyzed by ele...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Fibrillin Assembly Requires Fibronectin

Sabatier

Chen²,

Fagotto‐Kaufmann³

et al. 2009

MBoC

225

240

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“…Others have shown that cells that lack fibronectin fibrils also lack tenascin C fibrils (Chung and Erickson, 1997). In addition, fibronectin deposition regulates the deposition of fibulin (Roman and McDonald, 1993;Godyna et al, 1995b;Sasaki et al, 1996) and fibrinogen (Pereira et al, 2002) in the extracellular matrix. Our data indicate that collagen I and thrombosponin-1 are deposited into fibrillar structures in the extracellular matrix only when fibronectin fibrils are present.…”

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confidence: 99%

Fibronectin Polymerization Regulates the Composition and Stability of Extracellular Matrix Fibrils and Cell-Matrix Adhesions

Sottile

Hocking

2002

MBoC

552

510

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Remodeling of extracellular matrices occurs during development, wound healing, and in a variety of pathological processes including atherosclerosis, ischemic injury, and angiogenesis. Thus, identifying factors that control the balance between matrix deposition and degradation during tissue remodeling is essential for understanding mechanisms that regulate a variety of normal and pathological processes. Using fibronectin-null cells, we found that fibronectin polymerization into the extracellular matrix is required for the deposition of collagen-I and thrombospondin-1 and that the maintenance of extracellular matrix fibronectin fibrils requires the continual polymerization of a fibronectin matrix. Further, integrin ligation alone is not sufficient to maintain extracellular matrix fibronectin in the absence of fibronectin deposition. Our data also demonstrate that the retention of thrombospondin-1 and collagen I into fibrillar structures within the extracellular matrix depends on an intact fibronectin matrix. An intact fibronectin matrix is also critical for maintaining the composition of cell-matrix adhesion sites; in the absence of fibronectin and fibronectin polymerization, neither ␣5␤1 integrin nor tensin localize to fibrillar cell-matrix adhesion sites. These data indicate that fibronectin polymerization is a critical regulator of extracellular matrix organization and stability. The ability of fibronectin polymerization to act as a switch that controls the organization and composition of the extracellular matrix and cell-matrix adhesion sites provides cells with a means of precisely controlling cell-extracellular matrix signaling events that regulate many aspects of cell behavior including cell proliferation, migration, and differentiation. INTRODUCTIONExtracellular matrix remodeling plays an important role during development, wound healing, atherosclerosis, ischemic injury, and angiogenesis. Perturbing matrix remodeling by preventing the turnover of collagen I or by altering the levels of matrix-degrading proteases or protease inhibitors has been shown to result in fibrosis, arthritis, reduced angiogenesis, and developmental abnormalities (Liu et al., 1995;Vu et al., 1998;Holmbeck et al., 1999;Ducharme et al., 2000). In normal adult tissue, some extracellular matrix components such as elastin and fibrillar collagen have half lives of months to years (Krane, 1985;Debelle and Tamburro, 1999). Other extracellular matrix components, such as proteoglycans, thrombospondin-1 and -2, and vitronectin, can be endocytosed and degraded in the lysosomes (McKeownLongo et al., 1984;Yanagishita and Hascall, 1984; MurphyUllrich and Mosher, 1987;Hausser et al., 1992;Godyna et al., 1995a;Pijuan-Thompson and Gladson, 1997;Memmo and McKeown-Longo, 1998). Extracellular matrix molecules can also be degraded extracellularly by proteases such as matrix metalloproteinases (MMPs), plasminogen activators, and plasmin (Hynes, 1990;Marchina and Barlati, 1996;Shapiro, 1998).Recent data indicate that polymerized forms of extracellular matri...

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“…Both proteins are very similar in their rod-like region but differ by a large N-terminal globular domain unique to fibulin-2 which was considered to be responsible for oligomerization (Pan et al, 1993b). These fibulins show a similar but not completely identical binding repertoire for other extracellular ligands including fibronectin, nidogen, collagen IV, laminins and perlecan (Balbona et al, 1992 ;Pan et al, 1993a;Sasaki et al, 1995a,b) indicating that they participate in supramolecular matrix structures and, in particular, in microfibrillar assembly (Godyna et al, 1994;Roark et al, 1995). Most of these interactions are dependent on calcium which suggested the involvement of EGF-like repeats of the rod domain.…”

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confidence: 99%

Different Susceptibilities of Fibulin‐1 and Fibulin‐2 to Cleavage by Matrix Metalloproteinases and Other Tissue Proteases

Sasaki

Mann

Murphy

et al. 1996

European Journal of Biochemistry

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Fibulin-1 and fibulin-2 are two novel rod-like proteins which occur either in basement membranes or in interstitial fibrils in close association with fibronectin. They were examined for their sensitivity to proteolysis by matrix metalloproteinases (stromelysin, matrilysin), circulating proteases (thrombin, plasmin, kallikrein), leucocyte elastase and mast cell chymase. Fibulin-1 (95 kDa) was readily cleaved by leucocyte elastase, weakly by matrilysin and not by the other proteases. Cleavage occurred in a domainconnecting link region close to the N-terminus, giving rise to fragments of 70 kDa and 26 kDa. A much more extensive cleavage by all seven proteases was observed for fibulin-2 (195 m a ) , giving rise to many fragments in the range 15-150 kDa. Vulnerable sites included two central link regions, the cysteine-free part of the large N-terminal globular domain but also several regions of epidermal-growth-factor(EGF)-like repeats which are a major part of the rod-like domain. The latter domain became much more sensitive to proteolysis in the presence of EDTA, demonstrating that calcium is required for stabilization. Edman degradation demonstrated cleavage of peptide bonds corresponding to the known specificities of these proteases. A similar proteolysis was also observed for fibulin-2 deposited by cultured fibroblasts into a dense fibrillar network. Since fibulin-2 is an abundant component of small and large blood vessels it could be a major target for proteolysis during vascular injuries.

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A quantitative analysis of the incorporation of fibulin-1 into extracellular matrix indicates that fibronectin assembly is required

Cited by 65 publications

References 51 publications

Fibrillin Assembly Requires Fibronectin

Fibrillin Assembly Requires Fibronectin

Fibronectin Polymerization Regulates the Composition and Stability of Extracellular Matrix Fibrils and Cell-Matrix Adhesions

Different Susceptibilities of Fibulin‐1 and Fibulin‐2 to Cleavage by Matrix Metalloproteinases and Other Tissue Proteases

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