All vascular implants, including stents, heart valves and graft materials exhibit suboptimal biocompatibility that significantly reduces their clinical efficacy. A range of biomolecules in the subendothelial space have been shown to play critical roles in local regulation of thrombosis, endothelial growth and smooth muscle cell proliferation, making these attractive candidates for modulation of vascular device biointegration. However, classically used biomaterial coatings, such as fibronectin and laminin, modulate only one of these components; enhancing endothelial cell attachment, but also activating platelets and triggering thrombosis. This review examines a subset of extracellular matrix molecules that have demonstrated multi-faceted vascular compatibility and accordingly are promising candidates to improve the biointegration of vascular biomaterials.
References
[1]
Kannan, R.Y.; Salacinski, H.J.; Butler, P.E.; Hamilton, G.; Seifalian, A.M. Current status of prosthetic bypass grafts: A review. J. Biomed. Mater. Res. B 2005, 74, 570–581.
[2]
Devine, C.; Hons, B.; McCollum, C. Heparin-bonded dacron or polytetrafluoroethylene for femoropopliteal bypass grafting: A multicenter trial. J. Vasc. Surg. 2001, 33, 533–539, doi:10.1067/mva.2001.113578.
[3]
Devine, C.; McCollum, C. Heparin-bonded dacron or polytetrafluorethylene for femoropopliteal bypass: Five-year results of a prospective randomized multicenter clinical trial. J. Vasc. Surg. 2004, 40, 924–931, doi:10.1016/j.jvs.2004.08.033.
[4]
Maegdefessel, L.; Linde, T.; Krapiec, F.; Hamilton, K.; Steinseifer, U.; van Ryn, J.; Raaz, U.; Buerke, M.; Werdan, K.; Schlitt, A. In vitro comparison of dabigatran, unfractionated heparin, and low-molecular-weight heparin in preventing thrombus formation on mechanical heart valves. Thromb. Res. 2010, 126, e196–e200, doi:10.1016/j.thromres.2010.06.011.
[5]
Cutlip, D.E.; Baim, D.S.; Ho, K.K.; Popma, J.J.; Lansky, A.J.; Cohen, D.J.; Carrozza, J.P., Jr.; Chauhan, M.S.; Rodriguez, O.; Kuntz, R.E. Stent thrombosis in the modern era: A pooled analysis of multicenter coronary stent clinical trials. Circulation 2001, 103, 1967–1971.
[6]
Joner, M.; Finn, A.V.; Farb, A.; Mont, E.K.; Kolodgie, F.D.; Ladich, E.; Kutys, R.; Skorija, K.; Gold, H.K.; Virmani, R. Pathology of drug-eluting stents in humans: Delayed healing and late thrombotic risk. J. Am. Coll. Cardiol. 2006, 48, 193–202, doi:10.1016/j.jacc.2006.03.042.
[7]
Lemesle, G.; Delhaye, C.; Bonello, L.; de Labriolle, A.; Waksman, R.; Pichard, A. Stent thrombosis in 2008: Definition, predictors, prognosis and treatment. Arch. Cardiovasc. Dis. 2008, 101, 769–777, doi:10.1016/j.acvd.2008.10.006.
[8]
Cutlip, D.E.; Windecker, S.; Mehran, R.; Boam, A.; Cohen, D.J.; van Es, G.A.; Steg, P.G.; Morel, M.A.; Mauri, L.; Vranckx, P.; et al. Clinical end points in coronary stent trials: A case for standardized definitions. Circulation 2007, 115, 2344–2351, doi:10.1161/CIRCULATIONAHA.106.685313.
[9]
Daemen, J.; Wenaweser, P.; Tsuchida, K.; Abrecht, L.; Vaina, S.; Morger, C.; Kukreja, N.; Juni, P.; Sianos, G.; Hellige, G.; et al. Early and late coronary stent thrombosis of sirolimus-eluting and paclitaxel-eluting stents in routine clinical practice: Data from a large two-institutional cohort study. Lancet 2007, 369, 667–678.
[10]
Kedhi, E.; Joesoef, K.S.; McFadden, E.; Wassing, J.; van Mieghem, C.; Goedhart, D.; Smits, P.C. Second-generation everolimus-eluting and paclitaxel-eluting stents in real-life practice (compare): A randomised trial. Lancet 2010, 375, 201–209.
[11]
Pendyala, L.; Jabara, R.; Robinson, K.; Chronos, N. Passive and active polymer coatings for intracoronary stents: Novel devices to promote arterial healing. J. Int. Cardiol. 2009, 22, 37–48, doi:10.1111/j.1540-8183.2009.00423.x.
[12]
Williams, D.F. On the mechanisms of biocompatibility. Biomaterials 2008, 29, 2941–2953, doi:10.1016/j.biomaterials.2008.04.023.
[13]
Ott, H.C.; Matthiesen, T.S.; Goh, S.K.; Black, L.D.; Kren, S.M.; Netoff, T.I.; Taylor, D.A. Perfusion-decellularized matrix: Using nature’s platform to engineer a bioartificial heart. Nat. Med. 2008, 14, 213–221.
[14]
Campbell, J.H.; Efendy, J.L.; Campbell, G.R. Novel vascular graft grown within recipient’s own peritoneal cavity. Circ. Res. 1999, 85, 1173–1178.
[15]
Yin, Y.; Wise, S.G.; Nosworthy, N.J.; Waterhouse, A.; Bax, D.V.; Youssef, H.; Byrom, M.J.; Bilek, M.M.; McKenzie, D.R.; Weiss, A.S.; et al. Covalent immobilisation of tropoelastin on a plasma deposited interface for enhancement of endothelialisation on metal surfaces. Biomaterials 2009, 30, 1675–1681, doi:10.1016/j.biomaterials.2008.11.009.
[16]
Bennett, J.S.; Berger, B.W.; Billings, P.C. The structure and function of platelet integrins. J. Thromb. Haem. 2009, 7, 200–205, doi:10.1111/j.1538-7836.2009.03378.x.
[17]
Vyas, S.P.; Vaidya, B. Targeted delivery of thrombolytic agents: Role of integrin receptors. Expert Opin. Drug Deliv. 2009, 6, 499–508, doi:10.1517/17425240902878002.
[18]
Maurer, L.M.; Tomasini-Johansson, B.R.; Mosher, D.F. Emerging roles of fibronectin in thrombosis. Thromb. Res. 2010, 125, 287–291, doi:10.1016/j.thromres.2009.12.017.
[19]
Dufourcq, P.; Couffinhal, T.; Alzieu, P.; Daret, D.; Moreau, C.; Duplaa, C.; Bonnet, J. Vitronectin is upregulated after vascular injury and vitronectin blockade prevents neointima formation. Card. Res. 2002, 53, 952–962, doi:10.1016/S0008-6363(01)00547-8.
[20]
Nelson, P.R.; Yamamura, S.; Kent, K.C. Extracellular matrix proteins are potent agonists of human smooth muscle cell migration. J. Vasc. Surg. 1996, 24, 25–33, doi:10.1016/S0741-5214(96)70141-6.
De Mel, A.; Jell, G.; Stevens, M.M.; Seifalian, A.M. Biofunctionalization of biomaterials for accelerated in situ endothelialization: A review. Biomacromolecules 2008, 9, 2969–2979, doi:10.1021/bm800681k.
[23]
Lewis, A.L. Phosphorylcholine-based polymers and their use in the prevention of biofouling. Coll. Surf. B Bioint. 2000, 18, 261–275, doi:10.1016/S0927-7765(99)00152-6.
[24]
Whelan, D.M.; van der Giessen, W.J.; Krabbendam, S.C.; van Vliet, E.A.; Verdouw, P.D.; Serruys, P.W.; van Beusekom, H.M. Biocompatibility of phosphorylcholine coated stents in normal porcine coronary arteries. Heart 2000, 83, 338–345, doi:10.1136/heart.83.3.338.
[25]
Adams, J.C.; Watt, F.M. Regulation of development and differentiation by the extracellular matrix. Development 1993, 117, 1183–1198.
[26]
Mecham, R. Overview of extracellular matrix. Curr. Prot. Cell Biol. 1998, 10, 1–14, doi:10.1016/S0955-0674(98)80079-3.
[27]
Juliano, R.L.; Haskill, S. Signal transduction from the extracellular matrix. J. Cell Biol. 1993, 120, 577–585, doi:10.1083/jcb.120.3.577.
[28]
Stephan, S.; Ball, S.G.; Williamson, M.; Bax, D.V.; Lomas, A.; Shuttleworth, C.A.; Kielty, C.M. Cell-matrix biology in vascular tissue engineering. J. Aant. 2006, 209, 495–502.
[29]
Williamson, M.R.; Shuttleworth, A.; Canfield, A.E.; Black, R.A.; Kielty, C.M. The role of endothelial cell attachment to elastic fibre molecules in the enhancement of monolayer formation and retention, and the inhibition of smooth muscle cell recruitment. Biomaterials 2007, 28, 5307–5318, doi:10.1016/j.biomaterials.2007.08.019.
[30]
Kalluri, R. Basement membranes: Structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3, 422–433, doi:10.1038/nrc1094.
[31]
Knox, S.M.; Whitelock, J.M. Perlecan: How does one molecule do so many things? Cell. Mol. Life Sci. 2006, 63, 2435–2445, doi:10.1007/s00018-006-6162-z.
[32]
Nugent, M.A.; Nugent, H.M.; Iozzo, R.V.; Sanchack, K.; Edelman, E.R. Perlecan is required to inhibit thrombosis after deep vascular injury and contributes to endothelial cell-mediated inhibition of intimal hyperplasia. Proc. Natl. Acad. Sci. USA 2000, 97, 6722–6727.
[33]
Robb, B.W.; Wachi, H.; Schaub, T.; Mecham, R.P.; Davis, E.C. Characterization of an in vitro model of elastic fiber assembly. Mol. Biol. Cell 1999, 10, 3595–3605.
Dietz, H.C.; Cutting, G.R.; Pyeritz, R.E.; Maslen, C.L.; Sakai, L.Y.; Corson, G.M.; Puffenberger, E.G.; Hamosh, A.; Nanthakumar, E.J.; Curristin, S.M.; et al. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 1991, 352, 337–339.
[43]
Charbonneau, N.L.; Carlson, E.J.; Tufa, S.; Sengle, G.; Manalo, E.C.; Carlberg, V.M.; Ramirez, F.; Keene, D.R.; Sakai, L.Y. In vivo studies of mutant fibrillin-1 microfibrils. J. Biol. Chem. 2010, 285, 24943–24955.
[44]
Massam-Wu, T.; Chiu, M.; Choudhury, R.; Chaudhry, S.S.; Baldwin, A.K.; McGovern, A.; Baldock, C.; Shuttleworth, C.A.; Kielty, C.M. Assembly of fibrillin microfibrils governs extracellular deposition of latent tgf beta. J. Cell. Sci. 2010, 123, 3006–3018, doi:10.1242/jcs.073437.
[45]
Rock, M.J.; Cain, S.A.; Freeman, L.J.; Morgan, A.; Mellody, K.; Marson, A.; Shuttleworth, C.A.; Weiss, A.S.; Kielty, C.M. Molecular basis of elastic fiber formation: Critical interactions and a tropoelastin-fibrillin-1 cross-link. J. Biol. Chem. 2004, 279, 23748–23758.
[46]
Bax, D.V.; Mahalingam, Y.; Cain, S.; Mellody, K.; Freeman, L.; Younger, K.; Shuttleworth, C.A.; Humphries, M.J.; Couchman, J.R.; Kielty, C.M. Cell adhesion to fibrillin-1: Identification of an arg-gly-asp-dependent synergy region and a heparin-binding site that regulates focal adhesion formation. J. Cell. Sci. 2007, 120, 1383–1392, doi:10.1242/jcs.003954.
[47]
Bax, D.V.; Bernard, S.E.; Lomas, A.; Morgan, A.; Humphries, J.; Shuttleworth, C.A.; Humphries, M.J.; Kielty, C.M. Cell adhesion to fibrillin-1 molecules and microfibrils is mediated by alpha 5 beta 1 and alpha v beta 3 integrins. J. Biol. Chem. 2003, 278, 34605–34616.
[48]
Mariko, B.; Ghandour, Z.; Raveaud, S.; Quentin, M.; Usson, Y.; Verdetti, J.; Huber, P.; Kielty, C.; Faury, G. Microfibrils and fibrillin-1 induce integrin-mediated signaling, proliferation and migration in human endothelial cells. Am. J. Phys. Cell Phys. 2010, 299, C977–C987, doi:10.1152/ajpcell.00377.2009.
[49]
Carta, L.; Pereira, L.; Arteaga-Solis, E.; Lee-Arteaga, S.Y.; Lenart, B.; Starcher, B.; Merkel, C.A.; Sukoyan, M.; Kerkis, A.; Hazeki, N.; et al. Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J. Biol. Chem. 2006, 281, 8016–8023.
[50]
Bunton, T.E.; Biery, N.J.; Myers, L.; Gayraud, B.; Ramirez, F.; Dietz, H.C. Phenotypic alteration of vascular smooth muscle cells precedes elastolysis in a mouse model of marfan syndrome. Circ. Res. 2001, 88, 37–43.
[51]
Nataatmadja, M.; West, M.; West, J.; Summers, K.; Walker, P.; Nagata, M.; Watanabe, T. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation 2003, 108 Suppl. 1, II329–II334.
[52]
Baumgartner, H.R.; Muggli, R.; Tschopp, T.B.; Turitto, V.T. Platelet adhesion, release and aggregation in flowing blood: Effects of surface properties and platelet function. Thromb. Haem. 1976, 35, 124–138.
[53]
Legrand, Y.; Karniguian, A.; Fauvel, F.; Gutman, N. The molecular interaction between platelet and vascular wall. Blood Cells 1983, 9, 263–274.
[54]
Zheng, W.; Wang, Z.; Song, L.; Zhao, Q.; Zhang, J.; Li, D.; Wang, S.; Han, J.; Zheng, X.L.; Yang, Z.; et al. Endothelialization and patency of rgd-functionalized vascular grafts in a rabbit carotid artery model. Biomaterials 2012, 33, 2880–2891.
[55]
Jozwiak, A.B.; Kielty, C.M.; Black, R.A. Surface functionalization of polyurethane for the immobilization of bioactive moieties on tissue scaffolds. J. Mater. Chem. 2008, 18, 2240–2248.
[56]
Yanagisawa, H.; Davis, E.C. Unraveling the mechanism of elastic fiber assembly: The roles of short fibulins. Int. J. Biochem. Cell Biol. 2010, 42, 1084–1093, doi:10.1016/j.biocel.2010.03.009.
[57]
Yanagisawa, H.; Davis, E.C.; Starcher, B.C.; Ouchi, T.; Yanagisawa, M.; Richardson, J.A.; Olson, E.N. Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 2002, 415, 168–171.
[58]
Lomas, A.C.; Mellody, K.T.; Freeman, L.J.; Bax, D.V.; Shuttleworth, C.A.; Kielty, C.M. Fibulin-5 binds human smooth-muscle cells through alpha5beta1 and alpha4beta1 integrins, but does not support receptor activation. Biochem. J. 2007, 405, 417–428, doi:10.1042/BJ20070400.
[59]
Freeman, L.J.; Lomas, A.; Hodson, N.; Sherratt, M.J.; Mellody, K.T.; Weiss, A.S.; Shuttleworth, A.; Kielty, C.M. Fibulin-5 interacts with fibrillin-1 molecules and microfibrils. Biochem. J. 2005, 388, 1–5.
[60]
Spencer, J.A.; Hacker, S.L.; Davis, E.C.; Mecham, R.P.; Knutsen, R.H.; Li, D.Y.; Gerard, R.D.; Richardson, J.A.; Olson, E.N.; Yanagisawa, H. Altered vascular remodeling in fibulin-5-deficient mice reveals a role of fibulin-5 in smooth muscle cell proliferation and migration. Proc. Natl. Acad. Sci. USA 2005, 102, 2946–2951.
[61]
Chapman, S.L.; Sicot, F.X.; Davis, E.C.; Huang, J.; Sasaki, T.; Chu, M.L.; Yanagisawa, H. Fibulin-2 and fibulin-5 cooperatively function to form the internal elastic lamina and protect from vascular injury. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 68–74.
[62]
Yanagisawa, H.; Schluterman, M.K.; Brekken, R.A. Fibulin-5, an integrin-binding matricellular protein: Its function in development and disease. J. Cell Commun. Sig. 2009, 3, 337–347, doi:10.1007/s12079-009-0065-3.
[63]
Nakamura, T.; Ruiz-Lozano, P.; Lindner, V.; Yabe, D.; Taniwaki, M.; Furukawa, Y.; Kobuke, K.; Tashiro, K.; Lu, Z.; Andon, N.L.; et al. Dance, a novel secreted rgd protein expressed in developing, atherosclerotic, and balloon-injured arteries. J. Biol. Chem. 1999, 274, 22476–22483.
[64]
Preis, M.; Cohen, T.; Sarnatzki, Y.; Ben Yosef, Y.; Schneiderman, J.; Gluzman, Z.; Koren, B.; Lewis, B.S.; Shaul, Y.; Flugelman, M.Y. Effects of fibulin-5 on attachment, adhesion, and proliferation of primary human endothelial cells. Biochem. Biophys. Res. Commun. 2006, 348, 1024–1033.
[65]
Guadall, A.; Orriols, M.; Rodriguez-Calvo, R.; Calvayrac, O.; Crespo, J.; Aledo, R.; Martinez-Gonzalez, J.; Rodriguez, C. Fibulin-5 is up-regulated by hypoxia in endothelial cells through a hypoxia-inducible factor-1 (hif-1alpha)-dependent mechanism. J. Biol. Chem. 2011, 286, 7093–7103.
[66]
Whitelock, J.; Melrose, J. Heparan sulfate proteoglycans in healthy and diseased systems. Wiley Inter. Rev. Sys. Biol. Med. 2011, 3, 739–751, doi:10.1002/wsbm.149.
[67]
Hayes, A.J.; Lord, M.S.; Smith, S.M.; Smith, M.M.; Whitelock, J.M.; Weiss, A.S.; Melrose, J. Colocalization in vivo and association in vitro of perlecan and elastin. Histo. Cell Biol. 2011, 136, 437–454.
[68]
Whitelock, J.M.; Melrose, J.; Iozzo, R.V. Diverse cell signaling events modulated by perlecan. Biochemistry 2008, 47, 11174–11183.
[69]
Alexopoulou, A.N.; Multhaupt, H.A.; Couchman, J.R. Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 2007, 39, 505–528, doi:10.1016/j.biocel.2006.10.014.
[70]
Kirkpatrick, C.A.; Selleck, S.B. Heparan sulfate proteoglycans at a glance. J. Cell. Sci. 2007, 120, 1829–1832, doi:10.1242/jcs.03432.
[71]
Olsen, B.R. Life without perlecan has its problems. J. Cell Biol. 1999, 147, 909–912, doi:10.1083/jcb.147.5.909.
[72]
Arikawa-Hirasawa, E.; Watanabe, H.; Takami, H.; Hassell, J.R.; Yamada, Y. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 1999, 23, 354–358, doi:10.1038/15537.
Costell, M.; Carmona, R.; Gustafsson, E.; Gonzalez-Iriarte, M.; Fassler, R.; Munoz-Chapuli, R. Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice. Circ. Res. 2002, 91, 158–164, doi:10.1161/01.RES.0000026056.81424.DA.
[75]
Hayashi, K.; Madri, J.A.; Yurchenco, P.D. Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins: An adhesion modulated by glycosaminoglycan. J. Cell Biol. 1992, 119, 945–959, doi:10.1083/jcb.119.4.945.
[76]
Whitelock, J.M.; Graham, L.D.; Melrose, J.; Murdoch, A.D.; Iozzo, R.V.; Underwood, P.A. Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol. 1999, 18, 163–178, doi:10.1016/S0945-053X(99)00014-1.
[77]
Segev, A.; Nili, N.; Strauss, B.H. The role of perlecan in arterial injury and angiogenesis. Cardiovasc. Res. 2004, 63, 603–610, doi:10.1016/j.cardiores.2004.03.028.
Garl, P.J.; Wenzlau, J.M.; Walker, H.A.; Whitelock, J.M.; Costell, M.; Weiser-Evans, M.C. Perlecan-induced suppression of smooth muscle cell proliferation is mediated through increased activity of the tumor suppressor pten. Circ. Res. 2004, 94, 175–183, doi:10.1161/01.RES.0000109791.69181.B6.
[80]
Kinsella, M.G.; Tran, P.K.; Weiser-Evans, M.C.; Reidy, M.; Majack, R.A.; Wight, T.N. Changes in perlecan expression during vascular injury: Role in the inhibition of smooth muscle cell proliferation in the late lesion. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 608–614, doi:10.1161/01.ATV.0000063109.94810.EE.
[81]
Tran, P.K.; Tran-Lundmark, K.; Soininen, R.; Tryggvason, K.; Thyberg, J.; Hedin, U. Increased intimal hyperplasia and smooth muscle cell proliferation in transgenic mice with heparan sulfate-deficient perlecan. Circ. Res. 2004, 94, 550–558, doi:10.1161/01.RES.0000117772.86853.34.
[82]
Guyton, J.R.; Rosenberg, R.D.; Clowes, A.W.; Karnovsky, M.J. Inhibition of rat arterial smooth muscle cell proliferation by heparin. In vivo studies with anticoagulant and nonanticoagulant heparin. Circ. Res. 1980, 46, 625–634, doi:10.1161/01.RES.46.5.625.
[83]
Mysliwiec, M.; Borawski, J.; Naumnik, B.; Rydzewska-Rosolowska, A. Endothelial dysfunction, atherosclerosis and thrombosis in uremia—possibilities of intervention. Rocz. Akad. Med. Bialymst. 2004, 49, 151–156.
[84]
Lord, M.S.; Yu, W.; Cheng, B.; Simmons, A.; Poole-Warren, L.; Whitelock, J.M. The modulation of platelet and endothelial cell adhesion to vascular graft materials by perlecan. Biomaterials 2009, 30, 4898–4906.
[85]
Segev, A.; Nili, N.; Osherov, A.B.; Qiang, B.; Wong, A.J.; Pillarisetti, S.; Strauss, B.H. A perlecan-inducing compound significantly inhibits smooth muscle cell function and in-stent intimal hyperplasia: Novel insights into the diverse biological effects of perlecan. EuroIntervention 2010, 6, 134–140, doi:10.4244/EIJV6I1A20.
Kagan, H.M.; Li, W. Lysyl oxidase: Properties, specificity, and biological roles inside and outside of the cell. J. Cell. Biochem. 2003, 88, 660–672, doi:10.1002/jcb.10413.
[88]
Baldock, C.; Oberhauser, A.F.; Ma, L.; Lammie, D.; Siegler, V.; Mithieux, S.M.; Tu, Y.; Chow, J.Y.; Suleman, F.; Malfois, M.; et al. Shape of tropoelastin, the highly extensible protein that controls human tissue elasticity. Proc. Natl. Acad. Sci. USA 2011, 108, 4322–4327.
Wagenseil, J.E.; Nerurkar, N.L.; Knutsen, R.H.; Okamoto, R.J.; Li, D.Y.; Mecham, R.P. Effects of elastin haploinsufficiency on the mechanical behavior of mouse arteries. Am. J. Phys. Heart Circ. Phys. 2005, 289, H1209–H1217, doi:10.1152/ajpheart.00046.2005.
[91]
Wagenseil, J.E.; Ciliberto, C.H.; Knutsen, R.H.; Levy, M.A.; Kovacs, A.; Mecham, R.P. Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circ. Res. 2009, 104, 1217–1224, doi:10.1161/CIRCRESAHA.108.192054.
[92]
Li, D.Y.; Brooke, B.; Davis, E.C.; Mecham, R.P.; Sorensen, L.K.; Boak, B.B.; Eichwald, E.; Keating, M.T. Elastin is an essential determinant of arterial morphogenesis. Nature 1998, 393, 276–280, doi:10.1038/30522.
[93]
Sims, F.H.; Gavin, J.B.; Edgar, S.; Koelmeyer, T.D. Comparison of the endothelial surface and subjacent elastic lamina of anterior descending coronary arteries at the location of atheromatous lesions with internal thoracic arteries of the same subjects: A scanning electron microscopic study. Pathology 2002, 34, 433–441, doi:10.1080/0031302021000009351.
[94]
Ito, S.; Ishimaru, S.; Wilson, S.E. Effect of coacervated alpha-elastin on proliferation of vascular smooth muscle and endothelial cells. Angiology 1998, 49, 289–297, doi:10.1177/000331979804900407.
[95]
Long, M.M.; King, V.J.; Prasad, K.U.; Freeman, B.A.; Urry, D.W. Elastin repeat peptides as chemoattractants for bovine aortic endothelial cells. J. Cell. Phys. 1989, 140, 512–518, doi:10.1002/jcp.1041400316.
[96]
Robinet, A.; Fahem, A.; Cauchard, J.-H.; Huet, E.; Vincent, L.; Lorimier, S.; Antonicelli, F.; Soria, C.; Crepin, M.; Hornebeck, W.; et al. Elastin-derived peptides enhance angiogenesis by promoting endothelial cell migration and tubulogenesis through upregulation of mt1-mmp. J. Cell Sci. 2005, 118, 343–356, doi:10.1242/jcs.01613.
[97]
Lee, S.J.; Yoo, J.J.; Lim, G.J.; Atala, A.; Stitzel, J. In vitro evaluation of electrospun nanofiber scaffolds for vascular graft application. J. Biomed. Mater. Res. A 2007, 83, 999–1008.
[98]
Wise, S.G.; Byrom, M.J.; Waterhouse, A.; Bannon, P.G.; Ng, M.K.; Weiss, A.S. A multilayered synthetic human elastin/polycaprolactone hybrid vascular graft with tailored mechanical properties. Acta Biomater. 2011, 7, 295–303.
[99]
Wilson, B.D.; Gibson, C.C.; Sorensen, L.K.; Guilhermier, M.Y.; Clinger, M.; Kelley, L.L.; Shiu, Y.T.; Li, D.Y. Novel approach for endothelializing vascular devices: Understanding and exploiting elastin-endothelial interactions. Ann. Biomed. Eng. 2010, 39, 337–346.
[100]
Karnik, S.K.; Wythe, J.D.; Sorensen, L.; Brooke, B.S.; Urness, L.D.; Li, D.Y. Elastin induces myofibrillogenesis via a specific domain, vgvapg. Matrix Biol. 2003, 22, 409–425, doi:10.1016/S0945-053X(03)00076-3.
Ito, S.; Ishimaru, S.; Wilson, S.E. Inhibitory effect of type 1 collagen gel containing alpha-elastin on proliferation and migration of vascular smooth muscle and endothelial cells. Cardiovasc. Surg. 1997, 5, 176–183, doi:10.1016/S0967-2109(97)00004-5.
[103]
Miyamoto, K.; Atarashi, M.; Kadozono, H.; Shibata, M.; Koyama, Y.; Okai, M.; Inakuma, A.; Kitazono, E.; Kaneko, H.; Takebayashi, T.; et al. Creation of cross-linked electrospun isotypic-elastin fibers controlled cell-differentiation with new cross-linker. Int. J. Biol. Macromol. 2009, 45, 33–41, doi:10.1016/j.ijbiomac.2009.03.014.
[104]
Karnik, S.K.; Brooke, B.S.; Bayes-Genis, A.; Sorensen, L.; Wythe, J.D.; Schwartz, R.S.; Keating, M.T.; Li, D.Y. A critical role for elastin signaling in vascular morphogenesis and disease. Development 2003, 130, 411–423, doi:10.1242/dev.00223.
[105]
Waterhouse, A.; Wise, S.G.; Ng, M.K.; Weiss, A.S. Elastin as a nonthrombogenic biomaterial. Tissue Eng. Part B 2011, 17, 93–99.
[106]
Waterhouse, A.; Yin, Y.B.; Wise, S.G.; Bax, D.V.; McKenzie, D.R.; Bilek, M.M.M.; Weiss, A.S.; Ng, M.K.C. The immobilization of recombinant human tropoelastin on metals using a plasma-activated coating to improve the biocompatibility of coronary stents. Biomaterials 2010, 31, 8332–8340.
[107]
Hinds, M.T.; Rowe, R.C.; Ren, Z.; Teach, J.; Wu, P.-C.; Kirkpatrick, S.J.; Breneman, K.D.; Gregory, K.W; Courtman, D.W. Development of a reinforced porcine elastin composite vascular scaffold. J. Biomed. Mater. Res. A 2006, 77A, 458–469, doi:10.1002/jbm.a.30571.
[108]
Woodhouse, K.A.; Klement, P.; Chen, V.; Gorbet, M.B.; Keeley, F.W.; Stahl, R.; Fromstein, J.D.; Bellingham, C.M. Investigation of recombinant human elastin polypeptides as non-thrombogenic coatings. Biomaterials 2004, 25, 4543–4553.
[109]
Jordan, S.W.; Haller, C.A.; Sallach, R.E.; Apkarian, R.P.; Hanson, S.R.; Chaikof, E.L. The effect of a recombinant elastin-mimetic coating of an eptfe prosthesis on acute thrombogenicity in a baboon arteriovenous shunt. Biomaterials 2007, 28, 1191–1197, doi:10.1016/j.biomaterials.2006.09.048.
[110]
Karnik, S.K.; Brooke, B.S.; Bayes-Genis, A.; Sorensen, L.; Wythe, J.D.; Schwartz, R.S.; Keating, M.T.; Li, D.Y. A critical role for elastin signaling in vascular morphogenesis and disease. Development 2003, 130, 411–423, doi:10.1242/dev.00223.
[111]
Bilek, M.M.; Bax, D.V.; Kondyurin, A.; Yin, Y.; Nosworthy, N.J.; Fisher, K.; Waterhouse, A.; Weiss, A.S.; dos Remedios, C.G.; McKenzie, D.R. Free radical functionalization of surfaces to prevent adverse responses to biomedical devices. Proc. Natl. Acad. Sci. USA 2011, 108, 14405–14410.