Crucial Role for Endothelial Cell α2β1 Integrin Receptor Clustering in Collagen-Induced Angiogenesis.
angiogenesis
biomimetic
collagen
integrins
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
31
05
2018
revised:
11
04
2019
accepted:
26
04
2019
pubmed:
4
10
2019
medline:
17
2
2021
entrez:
4
10
2019
Statut:
ppublish
Résumé
Angiogenesis is a crucial mechanism of vascular growth and regeneration that requires biosynthesis and cross-linking of collagens in vivo and is induced by collagen in vitro. Here, we use an in vitro model in which apical Type I collagen gels rapidly induce angiogenesis in endothelial monolayers. We extend previous studies demonstrating the importance of the endothelial α2β1 integrin, a key collagen receptor, in angiogenesis by investigating the roles of receptor clustering and conformational activation. Immunocytochemical localization of α2β1 integrins in endothelial monolayers showed a concentration of integrins along cell-cell borders. After inducing angiogenesis with collagen, the receptors redistributed to apical cell surfaces, aligning with collagen fibers, which were also redistributed during angiogenesis. Levels of conformationally activated α2β1 integrins were unchanged during angiogenesis and undetected on endothelial cells binding collagen in suspension. We mimicked the polyvalency of collagen fibrils using antibody-coated polystyrene beads to cluster endothelial cell surface α2β1 integrins, which induced rapid angiogenesis in the absence of collagen gels. Clustering of αvβ3 integrins and PECAM-1 but not of α1 integrins also induced angiogenesis. Soluble antibodies alone had no effect. Thus, the angiogenic property of collagen may reside in its ability to ligate and cluster cell surface receptors such as α2β1 integrins. Furthermore, synthetic substrates that promote the clustering of select endothelial cell surface receptors mimic the angiogenic properties of Type I collagen and may have applications in promoting vascularization of engineered tissues. Anat Rec, 2019. © 2019 American Association for Anatomy.
Substances chimiques
Integrin alpha2beta1
0
Collagen
9007-34-5
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1604-1618Informations de copyright
© 2019 American Association for Anatomy.
Références
Brooks PC, Clark RA, Cheresh DA. 1994. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264:569-571.
Brooks PC, Stromblad S, Klemke R, Visscher D, Sarkar FH, Cheresh DA. 1995. Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J Clin Invest 96:1815-1822.
Buckley CD, Doyonnas R, Newton JP, Blystone SD, Brown EJ, Watt SM, Simmons DL. 1996. Identification of alpha v beta 3 as a heterotypic ligand for CD31/PECAM-1. J Cell Sci 109:437-445.
Cantarero LA, Butler JE, Osborne JW. 1980. The adsorptive characteristics of proteins for polystyrene and their significance in solid-phase imunoassays. Anal Biochem 105:375-382.
Cavalcanti-Adam EA, Volberg T, Micoulet A, Kessler H, Geiger B, Spatz JP. 2007. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys J 92:2964-2974.
Chalupowicz DG, Chowdhury ZA, Bach TL, Barsigian C, Martinez J. 1995. Fibrin II induces endothelial cell capillary tube formation. J Cell Biol 130:207-215.
Davis GE, Camarillo CW. 1996. An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224:39-51.
Davis GE, Black SM, Bayless KJ. 2000. Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev Biol Anim 36:513-519.
DeLisser HM, Christofidou-Solomidou M, Strieter RM, Burdick MD, Robinson CS, Wexler RS, Kerr JS, Garlanda C, Merwin JR, Madri JA, et al. 1997. Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol 151:671-677.
Drake CJ, LaRue A, Ferrara N, Little CD. 2000. VEGF regulates cell behavior during vasculogenesis. Dev Biol 224:178-188.
Ellerbroek SM, Wu YI, Overall CM, Stack MS. 2001. Functional interplay between type I collagen and cell surface matrix metalloproteinase activity. J Biol Chem 276:24833-24842.
Folkman J, Haudenschild C. 1980. Angiogenesis in vitro. Nature 288:551.
Gimbrone MA Jr. 1976. Culture of vascular endothelium. Prog Hemost Thromb 3:1-28.
Grinnell F, Geiger B. 1986. Interaction of fibronectin-coated beads with attached and spread fibroblasts. Binding, phagocytosis, and cytoskeletal reorganization. Exp Cell Res 162:449-461.
Gruber HE, Fisher EC Jr, Desai B, Stasky AA, Hoelscher G, Hanley EN Jr. 1997. Human intervertebral disc cells from the annulus: three-dimensional culture in agarose or alginate and responsiveness to TGF-beta1. Exp Cell Res 235:13-21.
Hynes RO. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
Hynes RO. 2007. Cell-matrix adhesion in vascular development. J Thromb Haemostasis 5:32-40.
Ilan N, Mahooti S, Madri JA. 1998. Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J Cell Sci 111:3621-3631.
Jokinen J, Dadu E, Nykvist P, Kapyla J, White DJ, Ivaska J, Vehvilainen P, Reunanen H, Larjava H, Hakkinen L, et al. 2004. Integrin-mediated cell adhesion to type I collagen fibrils. J Biol Chem 279:31956-31963.
Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. 2000. The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35-40.
Koo LY, Irvine DJ, Mayes AM, Lauffenburger DA, Griffith LG. 2002. Co-regulation of cell adhesion by nanoscale RGD organization and mechanical stimulus. J Cell Sci 115:1423-1433.
Lampugnani MG, Resnati M, Dejana E, Marchisio PC. 1991. The role of integrins in the maintenance of endothelial monolayer integrity. J Cell Biol 112:479-490.
Leitinger B, Hohenester E. 2007. Mammalian collagen receptors. Matrix Biol 26:146-155.
Lima AM, Wegner SV, Martins Cavaco AC, Estevao-Costa MI, Sanz-Soler R, Niland S, Nosov G, Klingauf J, Spatz JP, Eble JA. 2018. The spatial molecular pattern of integrin recognition sites and their immobilization to colloidal nanobeads determine alpha2beta1 integrin-dependent platelet activation. Biomaterials 167:107-120.
Maciag T, Cerundolo J, Ilsley S, Kelley PR, Forand R. 1979. An endothelial cell growth factor from bovine hypothalamus: identification and partial characterization. Proc Natl Acad Sci U S A 76:5674-5678.
Maheshwari G, Brown G, Lauffenburger DA, Wells A, Griffith LG. 2000. Cell adhesion and motility depend on nanoscale RGD clustering. J Cell Sci 113:1677-1686.
Matsumura T, Wolff K, Petzelbauer P. 1997. Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol 158:3408-3416.
Meredith JE, Fazeli B, Schwartz MA. 1993. The extracellular matrix as a cell survival factor. Mol Biol Cell 4:953-961.
Miyamoto S, Akiyama SK, Yamada KM. 1995a. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267:883-885.
Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, Akiyama SK, Yamada KM. 1995b. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131:791-805.
Montesano R, Orci L, Vassalli P. 1983. In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol 97:1648-1652.
Nicosia RF, Ottinetti A. 1990. Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab Invest 63:115-122.
Orgel JP, Antipova O, Sagi I, Bitler A, Qiu D, Wang R, Xu Y, San Antonio JD. 2011. Collagen fibril surface displays a constellation of sites capable of promoting fibril assembly, stability, and hemostasis. Connect Tissue Res 52:18-24.
Orr AW, Ginsberg MH, Shattil SJ, Deckmyn H, Schwartz MA. 2006. Matrix-specific suppression of integrin activation in shear stress signaling. Mol Biol Cell 17:4686-4697.
Sachar A, Strom TA, San Miguel S, Serrano MJ, Svoboda KKH, Liu X. 2014. Cell-matrix and cell-cell interactions of human gingival fibroblasts on three-dimensional nanofibrous gelatin scaffolds. J Tissue Eng Regen Med 8:862-873.
San Antonio JD, Lander AD, Wright TC, Karnovsky MJ. 1992. Heparin inhibits the attachment and growth of Balb/c-3T3 fibroblasts on collagen substrata. J Cell Physiol 150:8-16.
San Antonio JD, Zoeller JJ, Habursky K, Turner K, Pimtong W, Burrows M, Choi S, Basra S, Bennett JS, DeGrado WF, et al. 2009. A key role for the integrin alpha2beta1 in experimental and developmental angiogenesis. Am J Pathol 175:1338-1347.
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671.
Schoolmeester A, Vanhoorelbeke K, Katsutani S, Depraetere H, Feys HB, Heemskerk JM, Hoylaerts MF, Deckmyn H. 2004. Monoclonal antibody IAC-1 is specific for activated alpha2beta1 and binds to amino acids 199 to 201 of the integrin alpha2 I-domain. Blood 104:390-396.
Senger DR, Ledbetter SR, Claffey KP, Papadopoulos-Sergiou A, Peruzzi CA, Detmar M. 1996. Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alphavbeta3 integrin, osteopontin, and thrombin. Am J Pathol 149:293-305.
Senger DR, Claffey KP, Benes JE, Perruzzi CA, Sergiou AP, Detmar M. 1997. Angiogenesis promoted by vascular endothelial growth factor: regulation through alpha1beta1 and alpha2beta1 integrins. Proc Natl Acad Sci U S A 94:13612-13617.
Siljander PR, Hamaia S, Peachey AR, Slatter DA, Smethurst PA, Ouwehand WH, Knight CG, Farndale RW. 2004. Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J Biol Chem 279:47763-47772.
Stupack DG, Cheresh DA. 2004. Integrins and angiogenesis. Curr Top Dev Biol 64:207-238.
Sweeney SM, Guy CA, Fields GB, San Antonio JD. 1998. Defining the domains of type I collagen involved in heparin-binding and endothelial tube formation. Proc Natl Acad Sci U S A 95:7275-7280.
Sweeney SM, DiLullo G, Slater SJ, Martinez J, Iozzo RV, Lauer-Fields JL, Fields GB, San Antonio JD. 2003. Angiogenesis in collagen I requires alpha2beta1 ligation of a GFP*GER sequence and possibly p38 MAPK activation and focal adhesion disassembly. J Biol Chem 278:30516-30524.
Sweeney SM, Orgel JP, Fertala A, McAuliffe JD, Turner KR, Di Lullo GA, Chen S, Antipova O, Perumal S, Ala-Kokko L, et al. 2008. Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J Biol Chem 283:21187-21197.
Tulla M, Lahti M, Puranen JS, Brandt AM, Kapyla J, Domogatskaya A, Salminen TA, Tryggvason K, Johnson MS, Heino J. 2008. Effects of conformational activation of integrin alpha 1I and alpha 2I domains on selective recognition of laminin and collagen subtypes. Exp Cell Res 314:1734-1743.
Twardowski T, Fertala A, Orgel JP, San Antonio JD. 2007. Type I collagen and collagen mimetics as angiogenesis promoting superpolymers. Curr Pharm Des 13:3608-3621.
Van de Walle GR, Vanhoorelbeke K, Majer Z, Illyes E, Baert J, Pareyn I, Deckmyn H. 2005. Two functional active conformations of the integrin {alpha}2{beta}1, depending on activation condition and cell type. J Biol Chem 280:36873-36882.
Woltersdorf C, Bonk M, Leitinger B, Huhtala M, Kapyla J, Heino J, Gil Girol C, Niland S, Eble JA, Bruckner P, et al. 2017. The binding capacity of alpha1beta1-, alpha2beta1- and alpha10beta1-integrins depends on non-collagenous surface macromolecules rather than the collagens in cartilage fibrils. Matrix Biol 63:91-105.
Wong CW, Wiedle G, Ballestrem C, Wehrle-Haller B, Etteldorf S, Bruckner M, Engelhardt B, Gisler RH, Imhof BA. 2000. PECAM-1/CD31 trans-homophilic binding at the intercellular junctions is independent of its cytoplasmic domain; evidence for heterophilic interaction with integrin alphavbeta3 in Cis. Mol Biol Cell 11:3109-3121.
Xu Y, Gurusiddappa S, Rich RL, Owens RT, Keene DR, Mayne R, Hook A, Hook M. 2000. Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J Biol Chem 275:38981-38989.