Multifunctional silk-heparin biomaterials for vascular tissue engineering applications

Biomaterials

Volumn 35, Issue 1, 2014, Pages 83-91

  Seib, F Philipp ^a,d   Herklotz, Manuela ^b   Burke, Kelly A ^a   Maitz, Manfred F ^b   Werner, Carsten ^b,c   Kaplan, David L ^a  

^a Tufts University   (United States)

^b LEIBNIZ INSTITUTE OF POLYMER RESEARCH DRESDEN   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Blood compatibility; Endothelial cells; Heparin; Silk; Vascular engineering; VEGF

Indexed keywords

BIOCOMPATIBILITY TESTING; BLOOD COMPATIBILITY; HEPARIN; LOW-MOLECULAR WEIGHT HEPARINS; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENGINEERING; VASCULAR TISSUE ENGINEERING; VEGF;

BIOCOMPATIBILITY; BIOLOGICAL MATERIALS; ENDOTHELIAL CELLS; MEDICAL APPLICATIONS; POLYSACCHARIDES; TISSUE ENGINEERING;

SILK;

LOW MOLECULAR WEIGHT HEPARIN; POLITEF; SILK; SUTURE MATERIAL; VASCULOTROPIN;

ARTICLE; BLOOD COMPATIBILITY; CONTROLLED STUDY; DRUG RELEASE; ENDOTHELIUM; ENDOTHELIUM CELL; HEPARINIZATION; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; PRIORITY JOURNAL; SILK SUTURE; THROMBOGENICITY; TISSUE ENGINEERING; VASCULAR TISSUE;

BLOOD COMPATIBILITY; ENDOTHELIAL CELLS; HEPARIN; SILK; VASCULAR ENGINEERING; VEGF;

BIOCOMPATIBLE MATERIALS; BLOOD VESSELS; HEPARIN; HUMANS; SILK; TISSUE ENGINEERING;

EID: 84887016992     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.09.053     Document Type: Article

References (53)

1. Bordenave L., Menu P., Baquey C. Developments towards tissue-engineered, small-diameter arterial substitutes. Expert Rev Med Devices 2008, 5:337-347.
2. Achneck H.E., Sileshi B., Parikh A., Milano C.A., Welsby I.J., Lawson J.H. Pathophysiology of bleeding and clotting in the cardiac surgery patient: from vascular endothelium to circulatory assist device surface. Circulation 2010, 122:2068-2077.
3. Liu S., Liu T., Chen J., Maitz M., Chen C., Huang N. Influence of a layer-by-layer-assembled multilayer of anti-CD34 antibody, vascular endothelial growth factor, and heparin on the endothelialization and anticoagulation of titanium surface. JBiomed Mater Res A 2013, 101:1144-1157.
4. McGuigan A.P., Sefton M.V. The influence of biomaterials on endothelial cell thrombogenicity. Biomaterials 2007, 28:2547-2571.
5. Kasoju N., Bora U. Silk fibroin in tissue engineering. Adv Healthcare Mater 2012, 1:393-412.
6. Wenk E., Merkle H.P., Meinel L. Silk fibroin as a vehicle for drug delivery applications. JControl Release 2011, 150:128-141.
7. Pan C.J., Shao Z.Y., Tang J.J., Wang J., Huang N. Invitro studies of platelet adhesion, activation, and protein adsorption on curcumin-eluting biodegradable stent materials. JBiomed Mater Res A 2007, 82:740-746.
8. Domachuk P., Tsioris K., Omenetto F.G., Kaplan D.L. Bio-microfluidics: biomaterials and biomimetic designs. Adv Mater 2010, 22:249-260.
9. Enomoto S., Sumi M., Kajimoto K., Nakazawa Y., Takahashi R., Takabayashi C., et al. Long-term patency of small-diameter vascular graft made from fibroin, a silk-based biodegradable material. JVasc Surg 2010, 51:155-164.
10. Christenson J.T., Eklof B., Al-Huneidi W., Owunwanne A. Elastic and thrombogenic properties for different vascular grafts and its influence on graft patency. Int Angiol 1987, 6:81-87.
11. Huang F., Sun L., Zheng J. Invitro and invivo characterization of a silk fibroin-coated polyester vascular prosthesis. Artif Organs 2008, 32:932-941.
12. Lovett M., Lee K., Edwards A., Kaplan D.L. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev 2009, 15:353-370.
13. Peters M.C., Isenberg B.C., Rowley J.A., Mooney D.J. Release from alginate enhances the biological activity of vascular endothelial growth factor. JBiomater Sci Polym Ed 1998, 9:1267-1278.
14. Richardson T.P., Peters M.C., Ennett A.B., Mooney D.J. Polymeric system for dual growth factor delivery. Nat Biotechnol 2001, 19:1029-1034.
15. Kaigler D., Wang Z., Horger K., Mooney D.J., Krebsbach P.H. VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. JBone Miner Res 2006, 21:735-744.
16. Zieris A., Chwalek K., Prokoph S., Levental K.R., Welzel P.B., Freudenberg U., et al. Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels. JControl Release 2011, 156:28-36.
17. Ashikari-Hada S., Habuchi H., Kariya Y., Kimata K. Heparin regulates vascular endothelial growth factor165-dependent mitogenic activity, tube formation, and its receptor phosphorylation of human endothelial cells. Comparison of the effects of heparin and modified heparins. JBiol Chem 2005, 280:31508-31515.
18. Nishiguchi K.M., Kataoka K., Kachi S., Komeima K., Terasaki H. Regulation of pathologic retinal angiogenesis in mice and inhibition of VEGF-VEGFR2 binding by soluble heparan sulfate. PLoS One 2010, 5:e13493.
19. Motta A., Maniglio D., Migliaresi C., Kim H.J., Wan X., Hu X., et al. Silk fibroin processing and thrombogenic responses. JBiomater Sci Polym Ed 2009, 20:1875-1897.
20. Motta A., Migliaresi C., Lloyd A.W., Denyer S.P., Santin M. Serum protein absorption on silk fibroin fibers and films: surface opsonization and binding strength. JBioact Compat Polym 2002, 17:23-35.
21. Santin M., Denyer S.P., Lloyd A.W., Motta A. Domain-driven binding of fibrin(ogen) onto silk fibroin biomaterials. JBioact Compat Polym 2002, 17:195-208.
22. Lu Q., Zhang S., Hu K., Feng Q., Cao C., Cui F. Cytocompatibility and blood compatibility of multifunctional fibroin/collagen/heparin scaffolds. Biomaterials 2007, 28:2306-2313.
23. Tang Y., Cao C., Ma X., Chen C., Zhu H. Study on the preparation of collagen-modified silk fibroin films and their properties. Biomed Mater 2006, 1:242-246.
24. Lee K.Y., Kong S.J., Park W.H., Ha W.S., Kwon I.C. Effect of surface properties on the antithrombogenicity of silk fibroin/S-carboxymethyl kerateine blend films. JBiomater Sci Polym Ed 1998, 9:905-914.
25. Wang J., Hu W., Liu Q., Zhang S. Dual-functional composite with anticoagulant and antibacterial properties based on heparinized silk fibroin and chitosan. Colloids Surf B Biointerfaces 2011, 85:241-247.
26. Wang S., Gao Z., Chen X., Lian X., Zhu H., Zheng J., et al. The anticoagulant ability of ferulic acid and its applications for improving the blood compatibility of silk fibroin. Biomed Mater 2008, 3:044106.
27. Tamada Y. Sulfation of silk fibroin by chlorosulfonic acid and the anticoagulant activity. Biomaterials 2004, 25:377-383.
28. Ma X., Cao C., Zhu H. The biocompatibility of silk fibroin films containing sulfonated silk fibroin. JBiomed Mater Res Part B Appl Biomater 2006, 78:89-96.
29. Seib F.P., Maitz M.F., Hu X., Werner C., Kaplan D.L. Impact of processing parameters on the haemocompatibility of Bombyx mori silk films. Biomaterials 2012, 33:1017-1023.
30. Cines D.B., Pollak E.S., Buck C.A., Loscalzo J., Zimmerman G.A., McEver R.P., et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998, 91:3527-3561.
31. 13C NMR Spectroscopy. Macromolecules 1979, 12:1001-1007.
32. Weis J.R., Sun B., Rodgers G.M. Improved method of human umbilical arterial endothelial cell culture. Thromb Res 1991, 61:171-173.
33. Herklotz M., Werner C., Pompe T. The impact of primary and secondary ligand coupling on extracellular matrix characteristics and formation of endothelial capillaries. Biomaterials 2009, 30:35-44.
34. Streller U., Sperling C., Hubner J., Hanke R., Werner C. Design and evaluation of novel blood incubation systems for invitro hemocompatibility assessment of planar solid surfaces. JBiomed Mater Res B Appl Biomater 2003, 66B:379-390.
35. Omenetto F.G., Kaplan D.L. New opportunities for an ancient material. Science 2010, 329:528-531.
36. Cattaneo I., Figliuzzi M., Azzollini N., Catto V., Fare S., Tanzi M.C., et al. Invivo regeneration of elastic lamina on fibroin biodegradable vascular scaffold. Int J Artif Organs 2013, 36:166-174.
37. Unger R.E., Peters K., Wolf M., Motta A., Migliaresi C., Kirkpatrick C.J. Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of human endothelial cells. Biomaterials 2004, 25:5137-5146.
38. Ono K., Hattori H., Takeshita S., Kurita A., Ishihara M. Structural features in heparin that interact with VEGF165 and modulate its biological activity. Glycobiology 1999, 9:705-711.
39. Engstad C.S., Gutteberg T.J., Osterud B. Modulation of blood cell activation by four commonly used anticoagulants. Thromb Haemost 1997, 77:690-696.
40. Kelton J.G., Warkentin T.E. Heparin-induced thrombocytopenia: a historical perspective. Blood 2008, 112:2607-2616.
41. Martel N., Lee J., Wells P.S. Risk for heparin-induced thrombocytopenia with unfractionated and low-molecular-weight heparin thromboprophylaxis: a meta-analysis. Blood 2005, 106:2710-2715.
42. Wang S., Zhang Y., Wang H., Dong Z. Preparation, characterization and biocompatibility of electrospinning heparin-modified silk fibroin nanofibers. Int J Biol Macromol 2011, 48:345-353.
43. Zhao W., McCallum S.A., Xiao Z., Zhang F., Linhardt R.J. Binding affinities of vascular endothelial growth factor (VEGF) for heparin-derived oligosaccharides. Biosci Rep 2012, 32:71-81.
44. Norrby K. Low-molecular-weight heparins and angiogenesis. APMIS 2006, 114:79-102.
45. Norrby K., Nordenhem A. Dalteparin, a low-molecular-weight heparin, promotes angiogenesis mediated by heparin-binding VEGF-A invivo. APMIS 2010, 118:949-957.
46. Norrby K., Ostergaard P. A5.0-kD heparin fraction systemically suppresses VEGF165-mediated angiogenesis. Int J Microcirc Clin Exp 1997, 17:314-321.
47. Mousa S.A., Mohamed S. Inhibition of endothelial cell tube formation by the low molecular weight heparin, tinzaparin, is mediated by tissue factor pathway inhibitor. Thromb Haemost 2004, 92:627-633.
48. Saitow C., Kaplan D.L., Castellot J.J. Heparin stimulates elastogenesis: application to silk-based vascular grafts. Matrix Biol 2011, 30:346-355.
49. Perkins S.J., Nan R., Li K., Khan S., Miller A. Complement factor H-ligand interactions: self-association, multivalency and dissociation constants. Immunobiology 2012, 217:281-297.
50. Gorbet M.B., Sefton M.V. Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 2004, 25:5681-5703.
51. Rauterberg E.W., Ritz E. Bioincompatibility of dialysis membranes: factor H binding correlates inversely with complement activation indicating a local imbalance of involved proteases/anti-proteases. Adv Exp Med Biol 1988, 240:365-375.
52. Andersson J., Larsson R., Richter R., Ekdahl K.N., Nilsson B. Binding of a model regulator of complement activation (RCA) to a biomaterial surface: surface-bound factor H inhibits complement activation. Biomaterials 2001, 22:2435-2443.
53. Khan S., Nan R., Gor J., Mulloy B., Perkins S.J. Bivalent and co-operative binding of complement factor H to heparan sulfate and heparin. Biochem J 2012, 444:417-428.