Sulfated Polysaccharides Are Required for Collagen-Induced Vascular Tube Formation

Jackson, Chris; Giles, Irina; Knop, Alison; Nethery, Andrew; Schrieber, Leslie

doi:10.1006/excr.1994.1345

Cited by 20 publications

(13 citation statements)

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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: 99%

“…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%

“…Endothelial Cell-Type I Collagen Interactions. To examine the structural features of collagen necessary for endothelial tube induction, we used a system in which endothelial tubes rapidly form in HUVEC monolayers in the presence of type I collagen and heparin (21,34). Because tubes form within 4 hr, cell proliferation and migration are not involved and the assay is most representative of the endothelial tube formation phase of angiogenesis.…”

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: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

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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“…This demonstrates the importance of laminin in inducing tube formation. By using human neonatal foreskin microvascular endothelial cells, Jackson et al [18] were able to demonstrate that soluble type I collagen can induce vascular tube formation when it contacts the apical side of a confluent endothelial monolayer. In the same study, they also determined that sulfated polysaccharides such as heparin are required for collagen-induced vascular tube formation.…”

Section: Discussionmentioning

confidence: 99%

In Vitro Endothelial Differentiation of Long‐Term Cultured Murine Embryonic Yolk Sac Cells Induced by Matrigel

Wei

Wagner

1999

STEM CELLS

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“…Thus, bovine aortic endothelial cells synthesize type I collagen (4,5), and its expression precedes angiogenesis and is limited to the vicinity of cells forming capillary tubes in endothelial cell monolayers (6,7). Furthermore, endothelial cells grown between or dispersed within collagen gels form branching networks of tubes (8 -10), and in HUVEC 1 monolayers, angiogenesis rapidly proceeds in the presence of type I collagen and sulfated glycosaminoglycans (11)(12)(13). In vivo, angiogenesis is disrupted in the chick embryo by inhibiting collagen triple helix formation or fibrillogenesis using ␣,␣-dipyridyl or ␤-aminopropionitrile, respectively (14).…”

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confidence: 99%

Angiogenesis in Collagen I Requires α2β1 Ligation of a GFP*GER Sequence and Possibly p38 MAPK Activation and Focal Adhesion Disassembly

Sweeney

DiLullo

Slater

et al. 2003

Journal of Biological Chemistry

129

138

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Angiogenesis depends on proper collagen biosynthesis and cross-linking, and type I collagen is an ideal angiogenic scaffold, although its mechanism is unknown. We examined angiogenesis using an assay wherein confluent monolayers of human umbilical vein endothelial cells were overlain with collagen in a serumfree defined medium. Small spaces formed in the cell layer by 2 h, and cells formed net-like arrays by 6 -8 h and capillary-like lumens by 24 h. Blocking of ␣ 2 ␤ 1 , but not ␣ 1 or ␣ v ␤ 3 integrin function halted morphogenesis. We found that a triple-helical, homotrimeric peptide mimetic of a putative ␣ 2 ␤ 1 binding site: ␣ 1 (I)496 -507 GARGERGFP*GER (where single-letter amino acid nomenclature is used, P* ‫؍‬ hydroxyproline) inhibited tube formation, whereas a peptide carrying another putative site: ␣ 1 (I)127-138 GLP*GERGRP*GAP* or control peptides did not. A chemical inhibitor of p38 mitogen-activated protein kinase (p38 MAPK), SB202190, blocked tube formation, and p38 MAPK activity was increased in collagen-treated cultures, whereas targeting MAPK kinase (MEK), focal adhesion kinase (FAK), or phosphatidylinositol 3-kinase (PI3K) had little effect. Collagentreated cells had fewer focal adhesions and 3-to 5-fold less activated FAK. Thus capillary morphogenesis requires endothelial ␣ 2 ␤ 1 integrin engagement of a single type I collagen integrin-binding site, possibly signaling via p38 MAPK and focal adhesion disassembly/FAK inactivation.

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Sulfated Polysaccharides Are Required for Collagen-Induced Vascular Tube Formation

Cited by 20 publications

References 0 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

In Vitro Endothelial Differentiation of Long‐Term Cultured Murine Embryonic Yolk Sac Cells Induced by Matrigel

Angiogenesis in Collagen I Requires α2β1 Ligation of a GFP*GER Sequence and Possibly p38 MAPK Activation and Focal Adhesion Disassembly

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