journal article·2011-01

Heparin-functionalized collagen matrices with controlled release of basic fibroblast growth factor

J. M. Wu, Y. Y. Xu, Z. H. Li, X. Y. Yuan, P. F. Wang, X. Z. Zhang, Y. Q. Liu, J. Guan, Y. Guo, R. X. Li, H. Zhang

Publisher page

Abstract

Tissue engineering scaffolds with controlled long-term release of growth factors are constructed in an attempt to mimic the intelligent ability of the extracellular matrix (ECM) to release endogenous growth factors. In this study, collagen sponges (Collagen group) were modified by N-(3-dimethylaminopropyl)-N-ethylcarbodiimide hydrochloride (EDC) and N-hydroxysuccinimide (NHS) crosslinking (EDC/NHS group) and heparin immobilization (EDC/NHS-H group), and subsequently seeded with human umbilical vein endothelial cells (HUVECs). Native and modified sponges were pre-adsorbed with basic fibroblast growth factor (bFGF) to evaluate the sustained release and bioactive maintenance of bFGF from the sponges. We found that modified collagen matrices permitted HUVECs to proliferate and migrate well and to distribute uniformly. The EDC/NHS-H group exhibited an excellent sustained-release profile and bioactive maintenance of the pre-adsorbed bFGF as compared with the Collagen and EDC/NHS groups. These results suggest that heparin-functionalized collagen matrices can support a controlled release of bFGF and thus, have potential as a tissue engineering scaffold.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Proteoglycans and glycosaminoglycans research · Periodontal Regeneration and Treatments · Connective tissue disorders research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (45)

Show source-provided references
1. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol. 2003;200:423–8.10.1002/path.1437 ↗
2. Taipale J, Keski-Oja J. Growth factors in the extracellular matrix. FASEB J. 1997;11:51–9.10.1096/fasebj.11.1.9034166 ↗
3. Gumbiner BW. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996;84:345–57.10.1016/S0092-8674(00)81279-9 ↗
4. Mizuno K, Inoue H, Hagiya M, Shimizu S, Nose T, Shimohigashi Y, Nakamura T. Hairpin loop and second kringle domain are essential sites for heparin binding and biological activity of hepatocyte growth factor. J Biol Chem. 1994;269:1131–6.10.1016/S0021-9258(17)42231-9 ↗
5. Tessler S, Rockwell P, Hicklin D, Cohen T, Levi BZ, Witte L, Lemischka IR, Neufeld G. Heparin modulates the interaction of VEGF165 with soluble and cell associated flk-1 receptors. J Biol Chem. 1994;269:12456–61.10.1016/S0021-9258(18)99896-0 ↗
6. Schonherr E, Hausser HJ. Extracellular matrix and cytokines: a functional unit. Dev Immunol. 2000;7:89–101.10.1155/2000/31748 ↗
7. Bergers G, Brekken R, McMahon G, Vu T, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2000;2:737–44.10.1038/35036374 ↗
8. Ye S, Luo Y, Lu W, Jones RB, Linhardt RJ, Capila I, Toida T, Kan M, Pelletier H, McKeehan WL. Structural basis for interaction of FGF-1, FGF-2, and FGF-7 with different heparan sulfate motifs. Biochemistry. 2001;40:14429–39.10.1021/bi011000u ↗
9. Salmivirta M, Heino J, Jalkanen M. Fibroblast growth factor-syndecan complex at cell surface or immobilized to matrix promotes cell growth. J Biol Chem. 1992;267:17606–10.10.1016/S0021-9258(19)37085-1 ↗
10. Capila I, Linhardt RJ. Heparin-protein interactions. Angew Chem Int Ed. 2002;41:390–412.10.1002/1521-3773(20020201)41:3<390::AID-ANIE390>3.0.CO;2-B ↗
11. Kamei K, Wu XF, Xu XY, Minami K, Huy NT, Takano R, Kato H, Hara S. The analysis of heparin–protein interactions using evanescent wave biosensor with regioselectively desulfated heparins as the ligands. Anal Biochem. 2001;295:203–13.10.1006/abio.2001.5193 ↗
12. Nugent M, Iozzo R. Fibroblast growth factor-2. Int J Biochem Cell Biol. 2000;32:115–20.10.1016/S1357-2725(99)00123-5 ↗
13. Zhang L, Furst EM, Kiick KL. Manipulation of hydrogel assembly and growth factor delivery via the use of peptide-polysaccharide interactions. J Control Release. 2006;114:130–42.10.1016/j.jconrel.2006.06.005 ↗
14. Jeon O, Ryu SH, Chung JH, Kim BS. Control of basic fibroblast growth factor release from fibrin gel with heparin and concentrations of fibrinogen and thrombin. J Control Release. 2005;105:249–59.10.1016/j.jconrel.2005.03.023 ↗
15. Tae GY, Scatena M, Stayton P, Hoffman A. PEG-crosslinked heparin is an affinity hydrogel for sustained release of vascular endothelial growth factor. J Biomater Sci Polym Ed. 2006;17:187–97.10.1163/156856206774879090 ↗
16. Nakamura M, Ishihara K, Masuoka K, Ishizuka T, Kanatani Y, Takase B, Matsui T, Hattori H, Sato T, Kariya Y, Maehara T. Controlled release of fibroblast growth factor-2 from an injectable 6-O-desulfated heparin hydrogel and subsequent effect on in vivo vascularization. J Biomed Mater Res A. 2006;78:337–64.
17. Niklason LE, Langer R. Prospects for organ and tissue replacement. JAMA. 2001;285:573–6.10.1001/jama.285.5.573 ↗
18. Goldberg M, Langer R, Jia X. Nanostructured materials for applications in drug delivery and tissue engineering. J Biomater Sci Polym Ed. 2007;18:241–68.10.1163/156856207779996931 ↗
19. Ueda H, Liu H, Yamamoto M, Shigeno K, Inoue M, Toba T, Nakamura T, Tabata Y, Simizu Y. Use of collagen sponge incorporating transforming growth factor-β1 to promote bone repair in skull defects in rabbits. Biomaterials. 2002;23:1003–10.10.1016/S0142-9612(01)00211-3 ↗
20. Lu Q, Zhang SJ, Hu K, Feng QL, Cao CB, Cui FZ. Cytocompatibility and blood compatibility of multifunctional fibroin/collagen/heparin scaffolds. Biomaterials. 2007;28:2306–13.10.1016/j.biomaterials.2007.01.031 ↗
21. Wissink MJB, Beernink R, Poot AA, Engbers GHM, Beugeling T, van Aken WG, Feijen J. Improved endothelialization of vascular grafts by local release of growth factor from heparinized collagen matrices. J Control Release. 2000;64:103–14.10.1016/S0168-3659(99)00145-5 ↗
22. Madaghiele M, Piccinno A, Saponaro M, Maffezzoli A, Sannino A. Collagen- and gelatine-based films sealing vascular prostheses: evaluation of the degree of crosslinking for optimal blood impermeability. J Mater Sci Mater Med. 2009;20:1979–89.10.1007/s10856-009-3778-1 ↗
23. Wu JM, Imamura Y, Mizuno K, Hayashi T. Preparation of type III and V collagens and study of their structures (in Chinese). Chin J Biochem Pharm. 2003;24:239–41.
24. Wu JM, Ye P, Shun WJ, Guan J. Collagen sponge and study on its hemostatic properties (in Chinese). J Biomed Eng. 1998;15:63–5.
25. Wissink MJB, Beernink R, Pieper JS, Poot AA, Engbers GHM, Beugeling T, van Aken WG, Feijen J. Binding and release of basic fibroblast growth factor from heparinized collagen matrices. Biomaterials. 2001;22:2291–9.10.1016/S0142-9612(00)00418-X ↗
26. Yao C, Roderfeld M, Rath T, Roeb E, Bernhagena J, Steffens G. The impact of proteinase-induced matrix degradation on the release of VEGF from heparinized collagen matrices. Biomaterials. 2006;27:1608–16.10.1016/j.biomaterials.2005.08.037 ↗
27. Nam K, Kimura T, Kishida A. Physical and biological properties of collagen-phospholipid polymer hybrid gels. Biomaterials. 2007;28:3153–62.10.1016/j.biomaterials.2007.03.001 ↗
28. Angelea P, Abke J, Kujata R, Faltermeiera H, Schumanna D, Nerlicha M, Kinnera B, Englerta C, Ruszczakc Z, Mehrlc R, Mueller R. Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials. 2004;25:2831–41.10.1016/j.biomaterials.2003.09.066 ↗
29. Ma ZW, Gao CY, Gong YH, Shen JC. Cartilage tissue engineering PLLA scaffold with surface immobilized collagen and basic fibroblast growth factor. Biomaterials. 2005;26:1253–9.10.1016/j.biomaterials.2004.04.031 ↗
30. Wissink MJB, Beernink R, Scharenborg NM, Poot AA, Engbers GHM, Beugeling T, van Aken WG, Feijen J. Endothelial cell seeding of collagen matrices: effects of bFGF pre-loading on proliferation and pro-coagulant factors. J Control Release. 2000;67:141–55.10.1016/S0168-3659(00)00202-9 ↗
31. Kanematsu A, Marui A, Yamamoto S, Ozeki M, Hirano Y, Yamamoto M, Ogawa O, Komeda M, Tabata Y. Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release. 2004;99:281–92.10.1016/j.jconrel.2004.07.008 ↗
32. Ohshima M, Yamaguchi Y, Kappert K, Micke P, Otsuka K. bFGF rescues imatinib/STI571-induced apoptosis of sis-NIH3T3 fibroblasts. Biochem Biophys Res Commun. 2009;381:165–70.10.1016/j.bbrc.2009.02.012 ↗
33. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63.10.1016/0022-1759(83)90303-4 ↗
34. Sohn YD, Lim HJ, Hwang KC, Kwon JH, Park HY, Chung KH, Cho SY, Jang Y. A novel recombinant basic fibroblast growth factor and its secretion. Biochem Biophys Res Commun. 2001;284:931–6.10.1006/bbrc.2001.5076 ↗
35. Cote MF, Laroche G, Gagnon E, Chevallier P, Doillon CJ. Denatured collagen as support for a FGF-2 delivery system: physicochemical characterizations and in vitro release kinetics and bioactivity. Biomaterials. 2004;25:3761–72.10.1016/j.biomaterials.2003.10.026 ↗
36. Wissink MJB, Beernink R, Pieper JS, Poot AA, Engbers GHM, Beugeling T, van Aken WG, Feijen J. Immobilization of heparin to EDC/NHS-crosslinked collagen. Characterization and in vitro evaluation. Biomaterials. 2001;22:151–63.10.1016/S0142-9612(00)00164-2 ↗
37. Venkataramani ES, Senatore FF, Lokapur AK, Shankar H. Studies on heparin immobilization to collagen. Res Commun Chem Pathol Pharmacol. 1986;54:421–4.
38. Velichko TI, Shtopenko AN, Fedoseeva NV, Katrukha GS. Covalent immobilization of heparin on a collagen membrane. Khim Prir Soedin (English Transl). 1987;5:700–4.
39. Perets A, Baruch Y, Weisbuch F, Shoshany G, Neufeld G, Cohen S. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J Biomed Mater Res. 2003;65A:489–97.10.1002/jbm.a.10542 ↗
40. Bouafsoun A, Ponsonnet L, Kerkeni A, Jaffrézic N, Othmane A. Comparative wettability study of polystyrene functionalized with different proteins. Mater Sci Eng C. 2007;27:709–15.10.1016/j.msec.2006.06.038 ↗
41. Guan J, Wagner WR. Synthesis, characterization and cytocompatibility of polyurethaneurea elastomers with designed elastase sensitivity. Biomacromolecules. 2005;6:2833–42.10.1021/bm0503322 ↗
42. Tabata Y, Nagano A, Muniruzzaman M, Ikada Y. In vitro sorption and desorption of basic fibroblast growth factor from biodegradable hydrogels. Biomaterials. 1998;19(19):1781–9.10.1016/S0142-9612(98)00089-1 ↗
43. Jaklenec A, Wan E, Murray ME, Mathiowitz E. Novel scaffolds fabricated from protein-loaded microspheres for tissue engineering. Biomaterials. 2008;29:185–92.10.1016/j.biomaterials.2007.09.017 ↗
44. Jeon O, Kang SW, Lim HW, Chung JH, Kim BS. Long-term and zero-order release of basic fibroblast growth factor from heparin-conjugated poly (l-lactide-co glycolide) nanospheres and fibrin gel. Biomaterials. 2006;27:1598–607.10.1016/j.biomaterials.2005.08.030 ↗
45. Wu JM, Wang PF, Li ZH, Yuan XY. Preparation of bFGF-PLGA controlled-release microspheres and their sustained release performance in vitro (in Chinese). Chin J Biochem Pharm. 2010;31(1):32–4.