Fibulin's Organization into the Extracellular Matrix of Fetal Lung Fibroblasts Is Dependent on Fibronectin Matrix Assembly

Roman, Jesse; McDonald, John A.

doi:10.1165/ajrcmb/8.5.538

Cited by 35 publications

(18 citation statements)

References 29 publications

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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.…”

Section: Discussionmentioning

confidence: 99%

“…Fibronectin contains binding sites for a number of extracellular matrix molecules, including collagens, proteoglycans, fibulin, and thrombospondin (Yamada, 1989;Hynes, 1990;Chung et al, 1995;Sasaki et al, 1996) and has been shown to be required for the matrix deposition of fibulin and fibrinogen (Roman and McDonald, 1993;Sasaki et al, 1996;Pereira et al, 2002). In addition, inhibition of fibronectin matrix deposition has been correlated with a reduction in collagen type I deposition (McDonald et al, 1982).…”

Section: Deposition and Retention Of Thrombospondin-1 And Collagen I mentioning

confidence: 99%

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

Sottile

Hocking

2002

MBoC

548

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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Section: Discussionmentioning

confidence: 99%

Section: Deposition and Retention Of Thrombospondin-1 And Collagen I mentioning

confidence: 99%

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

Sottile

Hocking

2002

MBoC

548

510

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“…5). Fibronectin is known to be important for the deposition of several noncollagenous ECM molecules into fibrillar structures (15,63,67,76), some of which are known to bind to collagens (17,22,70). Hence, it is possible that deposition of collagen III into matrix fibrils is fibronectin dependent but occurs due to interaction with an ECM component other than fibronectin.…”

Section: Discussionmentioning

confidence: 99%

Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin

Sottile

Shi²,

Rublyevska³

et al. 2007

American Journal of Physiology-Cell Physiology

151

178

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munication between cells and the extracellular matrix (ECM) is critical for regulation of cell growth, survival, migration, and differentiation. Remodeling of the ECM can occur under normal physiological conditions, as a result of tissue injury, and in certain pathological conditions. ECM remodeling leads to alterations in ECM composition and organization that can alter many aspects of cell behavior, including cell migration. The cell migratory response varies depending on the type, amount, and organization of ECM molecules present, as well as the integrin and proteoglycan repertoire of the cells. We and others have shown that the deposition of several ECM molecules, including collagen types I and III, depends on the presence and stability of ECM fibronectin. Hence, the effect of fibronectin and fibronectin matrix on cell function may partially depend on its ability to direct the deposition of collagen in the ECM. In this study, we used collagen-binding fibronectin mutants and recombinant peptides that interfere with fibronectin-collagen binding to show that fibronectindependent collagen I deposition regulates the cell migratory response to fibronectin. These data show that the ability of fibronectin to organize other proteins in the ECM is an important aspect of fibronectin function and highlight the importance of understanding how interactions between ECM proteins influence cell behavior. extracellular matrix; contractility CELL FATE DECISIONS involving cell growth, differentiation, and survival rely on the ability of cells to coordinate diverse input from cytokines, growth factors, and extracellular matrix (ECM) molecules (3,89,94). The effects of ECM molecules on cell behavior are particularly complicated, since they depend on the mixture of ECM molecules that are present, the way the ECM proteins are organized and presented to cells, and the presence of proteases, protease inhibitors, and endocytic mechanisms that can alter the levels of ECM proteins and ECM degradation products. Understanding how ECM proteins act in concert to elicit biological effects is key to understanding how cell-ECM interactions maintain normal tissue function and influence the cell response to tissue injury.There is much data showing that mixtures of different ECM molecules can have effects distinct from that of a single ECM molecule. For example, coating dishes with a combination of tenascin C and fibronectin results in altered expression of matrix metalloproteinases (MMPs) (86), whereas addition of tenascin C to dishes coated with fibrin and fibronectin results in altered cytoskeletal organization (90) compared with cells seeded in the absence of tenascin C. The ability of fibronectin null cells to produce a fibronectin matrix is also dependent on the combination of matrix proteins present on the substrate (4). Furthermore, mixed collagen and fibronectin substrates have been shown to alter the response of endothelial cells to shear stress compared with their response to fibronectin alone (59). Similarly, addition of soluble matric...

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“…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 and McDonald, 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).…”

Section: Introductionmentioning

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).…”

mentioning

confidence: 99%

Fibrillin Assembly Requires Fibronectin

Sabatier

Chen²,

Fagotto‐Kaufmann³

et al. 2009

MBoC

223

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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Fibulin's Organization into the Extracellular Matrix of Fetal Lung Fibroblasts Is Dependent on Fibronectin Matrix Assembly

Cited by 35 publications

References 29 publications

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

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

Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin

Fibrillin Assembly Requires Fibronectin

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