VLA‐2 mediates the interaction of collagen with endothelium during <i>in vitro</i> vascular tube formation.

Jackson, Chris; Knop, Alison; Giles, Irina; Jenkins, Kate; Schrieber, Les

doi:10.1006/cbir.1994.1122

Cited by 23 publications

(14 citation statements)

References 17 publications

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“…Endothelial tubes formed in this way were found to have typical endothelial cell junctional complexes and to contain type I collagen (21,32,33). Type I collagen and sulfated GAGs were required for the effect, but laminin or type IV collagen and heparin were inactive (21,34), and anti-VLA-2 antibodies, which block ␣ 2 ␤ 1 integrin function, inhibited collagen-induced tube formation (35). We first tested the effects of various forms of collagen or the peptides (Table 1) as the inducer.…”

Section: Resultsmentioning

confidence: 98%

“…Endothelial cells grown between collagen gels form branching networks of tubes (32,33), and in HUVEC monolayers, angiogenesis rapidly proceeds in the presence of type I collagen and sulfated glycosaminoglycans (GAGs) (21,34). The signals mediated by type I collagen may be transduced by integrins (35), and it seems probable that HSPGs may also contribute to cell-collagen interactions of angiogenesis, because the endothelium produces HSPGs (36), which may bind collagens (24), and evidence suggests a role for GAGs in angiogenesis (34,37,38). Therefore, we have examined the structural basis of type I collagen-heparin interactions and their function in endothelial tube formation.…”

Section: Resultsmentioning

confidence: 99%

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Defining the domains of type I collagen involved in heparin- binding and endothelial tube formation

Sweeney

Guy

Fields

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

105

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Cell surface heparan sulfate proteoglycan (HSPG) interactions with type I collagen may be a ubiquitous cell adhesion mechanism. However, the HSPG binding sites on type I collagen are unknown. Previously we mapped heparin binding to the vicinity of the type I collagen N terminus by electron microscopy. The present study has identified type I collagen sequences used for heparin binding and endothelial cell-collagen interactions. Using affinity coelectrophoresis, we found heparin to bind as follows: to type I collagen with high affinity ( Cell surface proteoglycan interactions with type I collagen are likely a ubiquitous mechanism of cell adhesion, yet the interactive sites on these molecules are undefined. Consideration of the complexity of type I collagen structure is relevant to understanding its interactions with heparan sulfate proteoglycans (HSPGs) (see refs. 1 and 2 for review). Type I collagen is secreted as procollagen, which, after proteolytic cleavages, yields the triple-helical monomer composed of two ␣1 and one ␣2 chains. These monomers assemble in a regular staggered fashion into fibrils, which display the repeating D-period pattern, consisting of fine crossfibril bands (called the a, b, c, d, and e bands) in positively stained electron microscopy preparations.Triple-helical type I collagen conformation is necessary for its high-affinity binding to HSPGs, or to heparin, a chemical analog of its heparan sulfate chains (3-5). Furthermore, the C-terminal triple-helical fragment of type I collagen, generated by vertebrate collagenase treatment, showed a higher affinity for heparin than the did the N-terminal fragment (4).To localize more precisely the heparin-binding regions on type I collagen, we studied complexes between collagen monomers and heparin-albumin-gold particles by electron microscopy (6), and we observed heparin binding primarily to a region on the triple helix near the procollagen N terminus. In collagen fibrils, heparin-gold bound to the a bands region within each D-period, which is consistent with an N-terminal heparinbinding site on its monomers. The resolution of the mapping technique was insufficient to assign heparin-binding function to any particular protein sequence. Thus, amino acid sequences were inspected in relation to the heparin-binding locations observed by electron microscopy, searching for basic domains that might be suitable as heparin-binding sites. A highly basic sequence was found near the procollagen N terminus, and within the a bands fibril region, corresponding to amino acid residues 87-92 of the rat ␣1 chain. To test the heparin-binding function of this or other sites of type I collagen, here we have studied how mimetic triple-helical peptides (THPs) including various collagen sequences interact with heparin. We have also explored the function of these sequences in endothelial cell interactions with type I collagen during endothelial tube formation.

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Section: Resultsmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

Defining the domains of type I collagen involved in heparin- binding and endothelial tube formation

Sweeney

Guy

Fields

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

105

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“…In addition, ECM can exert important signaling functions directly to regulate EC shape and morphogenesis. For example, threedimensional interstitial collagen I stimulates ECs in vitro to assume a spindle-shaped morphology and to align into cords similarly to those observed during angiogenesis in vivo (Delvos et al 1982;Montesano et al 1983;Jackson et al 1994;Richard et al 1998;Sweeney et al 1998;Whelan and Senger 2003). Within collagen I gels, these cords mature to form tubes with hollow lumens through formation and coalescence of intracellular vacuoles (Davis and Camarillo 1996) and expansion of the lumenal compartment through ECM proteolysis (Chun et al 2004;Saunders et al 2006;Stratman et al 2009b).…”

Section: Ecm Function In Formation Of Vascular Cords the Precursors mentioning

confidence: 86%

Angiogenesis

Senger¹,

Davis²

2011

Cold Spring Harbor Perspectives in Biology

313

302

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Extracellular matrix (ECM) is essential for all stages of angiogenesis. In the adult, angiogenesis begins with endothelial cell (EC) activation, degradation of vascular basement membrane, and vascular sprouting within interstitial matrix. During this sprouting phase, ECM binding to integrins provides critical signaling support for EC proliferation, survival, and migration. ECM also signals the EC cytoskeleton to initiate blood vessel morphogenesis. Dynamic remodeling of ECM, particularly by membrane-type matrix metalloproteases (MT-MMPs), coordinates formation of vascular tubes with lumens and provides guidance tunnels for pericytes that assist ECs in the assembly of vascular basement membrane. ECM also provides a binding scaffold for a variety of cytokines that exert essential signaling functions during angiogenesis. In the embryo, ECM is equally critical for angiogenesis and vessel stabilization, although there are likely important distinctions from the adult because of differences in composition and abundance of specific ECM components.T he extracellular matrix (ECM) provides a critical framework for angiogenesis through structural support and also by conferring molecular signals essential for all stages of blood vessel formation, including vascular sprouting, lumen formation, vessel maturation, and ultimately vessel stabilization. In addition, ECM provides an immobilizing scaffold for cytokines that are important for angiogenesis. Thus, by providing basic structural support, direct signaling functions, and scaffolding for cytokines, ECM exerts fundamental control over angiogenesis. Moreover, the established functional complexity of ECM together with known mechanisms available for dynamic ECM remodeling suggest that ECM is capable of exerting precise control over all aspects of angiogenesis and blood vessel maturation.This article is divided into four parts: (1) Overview of angiogenesis and ECM in the adult; (2) key functions of ECM during angiogenesis; (3) distinctions between the composition of embryonic and adult ECMs, including implications for the involvement of specific integrins in angiogenesis; and (4) ECM remodeling during vascular tube formation and stabilization. The scientific literature on ECM and angiogenesis is vast, and it is therefore impossible to cover this topic completely in a single article. Thus, rather than striving for an exhaustive review of

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“…Previously, the ␣ 2 ␤ 1 integrin alone had been implicated in mediating collagen-induced cord formation by umbilical vein ECs (8) The apparent discrepancy between those findings and our observations, which also implicate integrin ␣ 1 ␤ 1 , is attributable to the fact that umbilical vein ECs do not express integrin ␣ 1 ␤ 1 and that both ␣ 1 ␤ 1 and ␣ 2 ␤ 1 are prominent collagen receptors on MVECs (14,31). This distinction is important, because MVECs are derived from the small capillaries of the microvasculature, whereas umbilical vein ECs are derived from large veins.…”

Section: Discussionmentioning

confidence: 99%

Collagen I Initiates Endothelial Cell Morphogenesis by Inducing Actin Polymerization through Suppression of Cyclic AMP and Protein Kinase A

Whelan

Senger

2003

Journal of Biological Chemistry

157

128

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Collagen I provokes endothelial cells to assume a spindle-shaped morphology and to align into solid cord-like assemblies. These cords closely imitate the solid precapillary cords of embryonic angiogenesis, raising interesting questions about underlying mechanisms. Studies described here identify a critical mechanism beginning with collagen I ligation of integrins ␣ 1 ␤ 1 and ␣ 2 ␤ 1 , followed by suppression of cyclic AMP and cyclic AMP (cAMP)-dependent protein kinase A, and marked induction of actin polymerization to form prominent stress fibers. In contrast to collagen I, laminin-1 neither suppressed cAMP nor protein kinase A activity nor induced actin polymerization or changes in cell shape. Moreover, fibroblasts did not respond to collagen I with changes in cAMP, actin polymerization, or cell shape, thus indicating that collagen signaling, as observed in endothelial cells, does not extend to all cell types. Pharmacological elevation of cAMP blocked collagen-induced actin polymerization and formation of cords by endothelial cells; conversely, pharmacological suppression of either cAMP or protein kinase A induced actin polymerization. Collectively, these studies identify a previously unrecognized and critical mechanism, involving suppression of cAMP-dependent protein kinase A and induction of actin polymerization, through which collagen I drives endothelial cell organization into multicellular precapillary cords.During angiogenesis, proliferating endothelial cells (ECs) 1 organize to form new three-dimensional capillary networks. This process has been studied extensively in the embryo, establishing that an early stage of angiogenesis involves transition of endothelial precursor cells to a spindle-shape morphology (1) in combination with alignment into solid, multicellular, pre-capillary, cord-like structures (2, 3). Moreover, these cordlike structures are interconnected to form a polygonal network (1, 4). Solid pre-capillary cords have also been observed during angiogenesis in the adult (5). These solid cords subsequently mature into tubes with hollow lumens for the transport of blood (1, 5).Three-dimensional type I collagen provokes ECs in culture to undergo marked shape changes that closely imitate pre-capillary formation during embryonic angiogenesis. Within hours after addition of collagen I to confluent cultures, ECs partially retract and exhibit a spindle-shaped morphology, together with re-alignment to form solid cords organized in a polygonal pattern (6 -10). Subsequently, over the course of several days, these structures mature to form tubes with hollow lumens through a process involving development and coalescence of intracellular vacuoles (11).Consistent with the importance of collagens in regulating EC shape and multicellular organization into pre-capillary cords, there exists considerable evidence that interactions between collagens and ECs are highly relevant in vivo. For example, in the developing embryo, blood vessels arise from the organization of EC precursors within an extracellular matrix r...

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VLA‐2 mediates the interaction of collagen with endothelium during in vitro vascular tube formation.

Cited by 23 publications

References 17 publications

Defining the domains of type I collagen involved in heparin- binding and endothelial tube formation

Defining the domains of type I collagen involved in heparin- binding and endothelial tube formation

Angiogenesis

Collagen I Initiates Endothelial Cell Morphogenesis by Inducing Actin Polymerization through Suppression of Cyclic AMP and Protein Kinase A

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