Elastic Fibers: Building Bridges Between Cells and Their Matrix

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Elastic Fibers: Building Bridges Between Cells and Their Matrix Current Biology, Vol. 12, R279–R281, April 16, 2002, ©2002 Elsevier Science Ltd. All rights reserved. PII S0960-9822(02)00800-X Elastic Fibers: Building Bridges Dispatch Between Cells and Their Matrix Kim S. Midwood and Jean E. Schwarzbauer Other proteins, including the emerging family of fibulin proteins, contact elastic fibers in vivo and are thought to promote the formation and stabilization of Extracellular elastic fibers confer resilience and the fiber. Fibulin is derived from the Latin for clasp or flexibility to tissues. Recent studies have identified a buckle and there are currently five members of this protein, fibulin-5, that connects these fibers to cells family. The fibulins have overlapping but distinct pat- and regulates their assembly and organization. terns of expression and are particularly prominent in tissues rich in elastic fibers such as lung and blood vessels. Recent studies [5,6] have identified fibulin-5 In animals, cells within tissues specifically contact as a protein that links elastic fibers to cells and other cells. They also contact a complex network of regulates fiber assembly and organization. These secreted proteins and carbohydrates, the extracellu- complementary studies focus on the function of lar matrix. Animals contain many different types of fibulin-5 — also known as DANCE and EVEC — a extracellular matrix, each specialized for a different 66 kDa protein that co-localizes with, and binds to, function. For example, tendons exhibit great strength elastin on the surface of elastic fibers. Fibulin-5 also and the extracellular matrix in the kidney is designed binds to cells by interacting with integrin cell surface for filtration. Many vertebrate tissues, including skin, receptors. blood vessels and lungs, need to be both strong and Both groups responsible for the recent advances extensible in order to function. This is accomplished successfully generated fibulin-5-deficient mice [5,6], by a network of elastic fibers in the extracellular which show similar gross morphological and ultra- matrix, which allows the tissue to stretch and recoil structural defects. The mice exhibit disrupted elastic without damage (Figure 1). These fibers are five times fiber networks in organs rich in elastin. These mice more extensible than a rubber band of the same survive into adulthood but develop severe elastin- cross-sectional area [1]. opathies, including loose skin, vascular abnormalities Extracellular elastic fibers comprise two distinct and emphysema. On the basis of this phenotype, the parts, an abundant amorphous component sur- authors [5,6] propose a role for fibulin-5 in the organi- rounded by a sheet of microfibrils. The amorphous zation of elastic fibers, and suggest that fibulin-5 may component is made up of the protein elastin, which act as a bridging molecule that connects elastin to the has an unusual chemical composition that con- cell surface. Fibulin-5-deficient mice are undoubtedly tributes to the elasticity of the fiber. Precursor tropoe- valuable as tools that will facilitate the further analysis lastin molecules are secreted from cells into the of elastogenesis in vivo, and as the first animal models extracellular space, where they assemble into loose of diseases such as cutis laxa. These mice may also chains that are covalently cross-linked to form an provide clues to the functions of the other, less well insoluble elastic meshwork. The microfibrils consist characterized, members of the fibulin family. of several proteins, including fibrillin and micro- Fibulin-5 has a modular structure of different fibril-associated glycoprotein. These proteins appear functional domains, which enables it to interact with prior to tropoelastin secretion and form a scaf- different combinations of cells and macromolecules, fold upon which elastin is deposited before it is and which facilitates its function as a bridging mol- displaced to the periphery of the growing fiber [2] ecule. It has epidermal growth factor-like motifs which (Figure 2A). are proposed to bind to elastin in a calcium-depen- Defects in elastic fiber structure result in a myriad of dent manner [6], as well as an arginine-glycine-aspartate pathological conditions. Cutis laxa, for example, is a (RGD) cell attachment sequence which it uses to inter- connective tissue disorder resulting from markedly act with αvβ3 and αvβ5 integrins [5]. This pattern is reduced dermal elastin content in which skin becomes seen throughout the fibulin family, all of which are inelastic and hangs loosely in folds [3]. Damage or modular proteins. Although little is known about the degradation of elastic fibers leads to emphysema, a function of fibulin-3 or fibulin-4, fibulin-1 has been degenerative disease of the lungs in which the air- shown to interact with several matrix proteins and inte- sacs lose their elasticity and become larger and less grins, and to localize to the amorphous elastin-rich core numerous, causing inefficient gaseous exchange [4]. of the elastic fiber [7]. Fibulin-2 also interacts with inte- Mutations in the fibrillin gene have been shown to grins and extracellular proteins, as well as with fibulin- cause Marfan syndrome, a common genetic disorder 1, and localizes to fibrillin containing microfibrils [8]. with clinical manifestations including aortic dilatation The idea that fibulin-5 acts as a bridge between and dissection, which in severe cases may cause the elastin and the cell surface adds an extra level of com- aorta to rupture [3]. plexity to the existing model of elastic fiber assembly. Close collaboration between cells and elastin is Department of Molecular Biology, Princeton University, needed for fiber formation to occur, and molecules Princeton, New Jersey, 08544-1014 , USA. that facilitate this have been identified. Elastin recep- E-mail: [email protected] tors have been shown to associate with tropoelastin Dispatch R280 Figure 1. A network of elastic fibers. AB Scanning electron micrographs show (A) a low-power view of a segment of a dog’s aorta, and (B) a high-power view of the dense network of longitudinally ori- ented elastic fibers within the same blood vessel. The aorta and other blood vessels consist of an impermeable inner layer of endothelial cells supported by elastic fibers and smooth muscle cells. 1mm 100 µm Current Biology and serve as chaperones to aid in its intracellular Comparisons can be made between elastic fiber transport and extracellular assembly [2]. Fibulin-5 may assembly and the assembly of other types of extra- coordinate the actions of these molecules by directing cellular matrix. RGD sequences are commonly found elastic fiber assembly at the cell surface (Figure 2B). It in matrix-resident proteins, such as fibronectin and may regulate the rate of elastin deposition onto vitronectin. RGD-mediated binding to cell surface inte- microfibrils, promote the initiation or termination of grin receptors has been extensively characterized and fiber formation, or control the orientation and localiza- found to play both structural and functional roles. tion of fibers over a specific cell surface area. As These connections initiate and propagate matrix fibulin-5 is essential for formation of new elastic fibers, formation [9] and convey information between matri- but apparently not for the maintenance of already ces and cells [10]. Cellular events coordinated by such existing fibrils [5,6], it plays an important role during interactions include adhesion, migration, proliferation development. In more mature fibers, however, poten- and apoptosis. RGD–integrin interactions also tial constraints imposed by fibulin-5 connections function in the transmission of human immunodefi- between elastin and the cell surface may be released ciency virus between cells, and mediate adhesion in order to allow full extensibility of the elastic fibers. between tumor cells and target tissues during metas- tasis [11]. Other fibulins have been shown to regulate A Tropoelastin fibronectin-mediated cell adhesion and migration [12], and they are thought to play vital roles in hemostasis [13] and tumor invasion [14]. Whether fibulin-5 is able to signal to the cell and regulate cell behavior in a Integrin similar manner remains to be seen. Calcium-binding epidermal growth factor-like repeats mediate protein–protein interactions and are found in numerous extracellular and membrane pro- teins. These modules consist of approximately 45 Cytoplasm Microfibril Elastic fiber amino acids, and are involved in such diverse processes Plasma as blood coagulation, determination of cell fate, and membrane Figure 2. Elastic fiber assembly and the role of fibulin-5. Tropoelastin B (A) Microfibrils (green) are assembled at the cell surface, where Fibulin-5 the fibrillin and microfibril-associated glycoprotein components interact with integrin receptors via RGD sequences. Tropo- elastin (red) is secreted from the cell and deposited onto Integrin microfibril scaffolds. This allows alignment of elastin cross- linking domains and enables efficient polymerization. Elastin molecules are joined together by covalent bonds (short black lines) to generate a flexible network. (B) Fibulin-5 may act as a chaperone in elastic fiber assembly. Fibulin-5 contains six tandem calcium-binding epidermal growth factor-like repeats Cytoplasm (blue) which bind to tropoelastin (red). Fibulin-5 may tether elastin to the cell by interacting with integrins (orange) on the Plasma cell surface using the RGD motif in the first epidermal growth membrane factor-like repeat.
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