An in vitro assessment of titanium functionalized with polysaccharides conjugated with vascular endothelial growth factor for enhanced osseointegration and inhibition of bacterial adhesion

Biomaterials

Volumn 31, Issue 34, 2010, Pages 8854-8863

  Hu, Xuefeng ^a   Neoh, Koon Gee ^a   Shi, Zhilong ^a   Kang, En Tang ^a   Poh, Chyekhoon ^a   Wang, Wilson ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Bacterial adhesion; Osteoblasts; Polysaccharide; Surface grafting; VEGF

Indexed keywords

ALKALINE PHOSPHATASE ACTIVITY; ANGIOGENESIS; ANTIBACTERIAL PROPERTIES; BACTERIAL ADHESION; BACTERIAL INFECTIONS; BONE-FORMING CELLS; CALCIUM DEPOSITION; CARBOXYMETHYL CHITOSAN; FUNCTIONALIZED; FUNCTIONALIZED SUBSTRATES; HYALURONIC ACIDS; IMPLANT FAILURES; IN-VITRO; ORTHOPEDIC IMPLANT; OSSEOINTEGRATION; OSTEOBLAST FUNCTION; S. AUREUS; STAPHYLOCOCCUS AUREUS; SURFACE GRAFTING; TI SUBSTRATES; VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF;

ADHESION; CALCIUM; GRAFTING (CHEMICAL); ORGANIC ACIDS; OSTEOBLASTS; PEPTIDES; PHENOLS; PHOSPHATASES; POLYSACCHARIDES; SELF ASSEMBLY; SUBSTRATES; TITANIUM;

BACTERIOLOGY;

ALKALINE PHOSPHATASE; CALCIUM; CHITOSAN; DOPAMINE; HYALURONIC ACID; POLYSACCHARIDE; TITANIUM; VASCULOTROPIN;

ANGIOGENESIS; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM ADHERENCE; BONE REGENERATION; CELL ADHESION; CELL FUNCTION; CONJUGATION; IN VITRO STUDY; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

ALKALINE PHOSPHATASE; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; CALCIUM; CELL ADHESION; CELL COUNT; CELL PROLIFERATION; ELEMENTS; IMMOBILIZED PROTEINS; MATERIALS TESTING; MICE; MICROSCOPY, FLUORESCENCE; OSSEOINTEGRATION; OSTEOBLASTS; PHOTOELECTRON SPECTROSCOPY; POLYSACCHARIDES; PROTEIN STABILITY; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTIES; TITANIUM; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 77957316676     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.08.006     Document Type: Article

References (63)

1. Senger D.R., Galli S.J., Dvorak A.M., Perruzzi C.A., Harvey V.S., Dvorak H.F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983, 219:983-985.
2. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
3. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
4. Leslie-Barbick J.E., Moon J.J., West J.L. Covalently-immobilized vascular endothelial growth factor promotes endothelial cell tubulogenesis in poly(ethylene glycol) diacrylate hydrogels. J Biomater Sci Polym Ed 2009, 20:1763-1779.
5. Zhou M., Liu Z., Wei Z., Liu C., Qiao T., Ran F., et al. Development and validation of small-diameter vascular tissue from a decellularized scaffold coated with heparin and vascular endothelial growth factor. Artif Organs 2009, 33:230-239.
6. Müller S., Koenig G., Charpiot A., Debry C., Voegel J.C., Lavalle P., et al. VEGF-functionalized polyelectrolyte multilayers as proangiogenic prosthetic coatings. Adv Funct Mater 2008, 18:1767-1775.
7. Poh C.K., Shi Z.L., Lim T.Y., Neoh K.G., Wang W. The effect of VEGF functionalization of titanium on endothelial cells in vitro. Biomaterials 2010, 31:1578-1585.
8. Gerber H.P., Vu T.H., Ryan A.M., Kowalski J., Werb Z., Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 1999, 5:623-628.
9. Jacobsen K.A., Al-Aql Z.S., Wan C., Fitch J.L., Stapleton S.N., Mason Z.D., et al. Bone formation during distraction osteogenesis is dependent on both VEGFR1 and VEGFR2 signaling. J Bone Miner Res 2008, 23:596-609.
10. Dai J., Rabie A.B. VEGF: an essential mediator of both angiogenesis and endochondral ossification. J Dent Res 2007, 86:937-950.
11. Wang D.S., Miura M., Demura H., Sato K. Anabolic effects of 1,25-dihydroxyvitamin D3 on osteoblasts are enhanced by vascular endothelial growth factor produced by osteoblasts and by growth factors produced by endothelial cells. Endocrinology 1997, 138:2953-2962.
12. Midy V., Plouet J. Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem Biophys Res Commun 1994, 199:380-386.
13. Deckers M.M., Karperien M., van der Bent C., Yamashita T., Papapoulos S.E., Lowik C.W. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 2000, 141:1667-1674.
14. Street J., Bao M., deGuzman L., Bunting S., Peale F.V., Ferrara N., et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 2002, 99:9656-9661.
15. Clarkin C.E., Emery R.J., Pitsillides A.A., Wheeler-Jones C.P. Evaluation of VEGF-mediated signaling in primary human cells reveals a paracrine action for VEGF in osteoblast-mediated crosstalk to endothelial cells. J Cell Physiol 2008, 214:537-544.
16. Okazaki Y., Gotoh E., Nishimori M., Katsuda S., Manabe T., Kobayashi K. Osteocompatibility of stainless steel, Co-Cr-Mo, Ti-6Al-4V and Ti-15Zr-4Nb-4Ta alloy implants in rat bone tissue. Mater Trans 2005, 46:1610-1617.
17. Weinlaender M., Kenney E.B., Lekovic V., Beumer J., Moy P.K., Lewis S. Histomorphometry of bone apposition around three types of endosseous dental implants. Int J Oral Max Impl 1992, 7:491-496.
18. Campoccia D., Montanaro L., Arciola C.R. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 2006, 27:2331-2339.
19. Widmer A.F. New developments in diagnosis and treatment of infection in orthopedic implants. Clin Infect Dis 2001, 33(Suppl. 2):S94-S106.
20. Vasilev K., Sah Vasu, Anselme K., Ndi C., Mateescu M., Dollmann B., et al. Tunable antibacterial coatings that support mammalian cell growth. Nano Lett 2009, 10:202-207.
21. Subbiahdoss G, Grijpma DW, van der Mei HC, Busscher HJ, Kuijer R. Microbial biofilm growth versus tissue integration on biomaterials with different wettabilities and a polymer-brush coating. J Biomed Mater Res A, in press.
22. Harris L.G., Tosatti S., Wieland M., Textor M., Richards R.G. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 2004, 25:4135-4148.
23. Rinaudo M. Main properties and current applications of some polysaccharides as biomaterials. Polym Int 2008, 57:397-430.
24. Chua P.H., Neoh K.G., Kang E.T., Wang W. Surface functionalization of titanium with hyaluronic acid/chitosan polyelectrolyte multilayers and RGD for promoting osteoblast functions and inhibiting bacterial adhesion. Biomaterials 2008, 29:1412-1421.
25. Liu X.F., Guan Y.L., Yang D.Z., Li Z., Yao K.D. Antibacterial action of chitosan and carboxymethylated chitosan. J Appl Polym Sci 2001, 79:1324-1335.
26. Lee H., Lee Y., Statz A.R., Rho J., Park T.G., Messersmith P.B. Substrate-independent layer-by-layer assembly by using mussel-adhesive-inspired polymers. Adv Mater 2008, 20:1619-1623.
27. He T., Shi Z.L., Fang N., Neoh K.G., Kang E.T., Chan V. The effect of adhesive ligands on bacterial and fibroblast adhesions to surfaces. Biomaterials 2009, 30:317-326.
28. Boulos L., Prevost M., Barbeau B., Coallier J., Desjardins R. LIVE/DEAD BacLight: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J Microbiol Methods 1999, 37:77-86.
29. Shi Z.L., Neoh K.G., Kang E.T., Wang W. Antibacterial and mechanical properties of bone cement impregnated with chitosan nanoparticles. Biomaterials 2006, 27:2440-2449.
30. Faghihi S., Azari F., Li H., Bateni M.R., Szpunar J.A., Vali H., et al. The significance of crystallographic texture of titanium alloy substrates on pre-osteoblast responses. Biomaterials 2006, 27:3532-3539.
31. Paul H., Reginato A.J., Schumacher H.R. Alizarin red S staining as a screening test to detect calcium compounds in synovial fluid. Arthritis Rheum 1983, 26:191-200.
32. Nanci A., Wuest J.D., Peru L., Brunet P., Sharma V., Zalzal S., et al. Chemical modification of titanium surfaces for covalent attachment of biological molecules. J Biomed Mater Res 1998, 40:324-335.
33. Wolf-Brandstetter C., Lode A., Hanke T., Scharnweber D., Worch H. Influence of modified extracellular matrices on TI6AL4V implants on binding and release of VEGF. J Biomed Mater Res A 2006, 79:882-894.
34. Gottenbos B., van der Mei H.C., Busscher H.J. Initial adhesion and surface growth of Staphylococcus epidermidis and Pseudomonas aeruginosa on biomedical polymers. J Biomed Mater Res 2000, 50:208-214.
35. Poelstra K.A., Barekzi N.A., Rediske A.M., Felts A.G., Slunt J.B., Grainger D.W. Prophylactic treatment of gram-positive and gram-negative abdominal implant infections using locally delivered polyclonal antibodies. J Biomed Mater Res 2002, 60:206-215.
36. Cassinelli C., Morra M., Pavesio A., Renier D. Evaluation of interfacial properties of hyaluronan coated poly(methylmethacrylate) intraocular lenses. J Biomater Sci Polym Ed 2000, 11:961-977.
37. An Y.H., Friedman R.J. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res 1998, 43:338-348.
38. Genzer J., Efimenko K. Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review. Biofouling 2006, 22:339-360.
39. Zheng L.Y., Zhu J.F. Study on antimicrobial activity of chitosan with different molecular weights. Carbohydr Polym 2003, 54:527-530.
40. Bordenave N., Grelier S., Coma V. Hydrophobization and antimicrobial activity of chitosan and paper-based packaging material. Biomacromolecules 2010, 11:88-96.
41. Rabea E.I., Badawy M.E., Stevens C.V., Smagghe G., Steurbaut W. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 2003, 4:1457-1465.
42. Chua P.H., Neoh K.G., Shi Z.L., Kang E.T. Structural stability and bioapplicability assessment of hyaluronic acid-chitosan polyelectrolyte multilayers on titanium substrates. J Biomed Mater Res A 2008, 87:1061-1074.
43. Tang H., Cao T., Wang A., Liang X., Salley S.O., McAllister J.P., et al. Effect of surface modification of silicone on Staphylococcus epidermidis adhesion and colonization. J Biomed Mater Res A 2007, 80:885-894.
44. Magnani A., Barbucci R., Montanaro L., Arciola C.R., Lamponi S. In vitro study of blood-contacting properties and effect on bacterial adhesion of a polymeric surface with immobilized heparin and sulphated hyaluronic acid. J Biomater Sci Polym Ed 2000, 11:801-815.
45. McDevitt D., Francois P., Vaudaux P., Foster T.J. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 1994, 11:237-248.
46. Dickinson R.B., Nagel J.A., Proctor R.A., Cooper S.L. Quantitative comparison of shear-dependent Staphylococcus aureus adhesion to three polyurethane ionomer analogs with distinct surface properties. J Biomed Mater Res 1997, 36:152-162.
47. Kang I.K., Kwon B.K., Lee J.H., Lee H.B. Immobilization of proteins on poly(methyl methacrylate) films. Biomaterials 1993, 14:787-792.
48. Fletcher M., Marshall K.C. Bubble contact angle method for evaluating substratum interfacial characteristics and its relevance to bacterial attachment. Appl Environ Microbiol 1982, 44:184-192.
49. Vaudaux P.E., Francois P., Proctor R.A., McDevitt D., Foster T.J., Albrecht R.M., et al. Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts. Infect Immun 1995, 63:585-590.
50. Shi Z.L., Neoh K.G., Kang E.T., Poh C.K., Wang W. Surface functionalization of titanium with carboxymethyl chitosan and immobilized bone morphogenetic protein-2 for enhanced osseointegration. Biomacromolecules 2009, 10:1603-1611.
51. Fan X., Lin L., Dalsin J.L., Messersmith P.B. Biomimetic anchor for surface-initiated polymerization from metal substrates. J Am Chem Soc 2005, 127:15843-15847.
52. Scotchford C.A., Ball M., Winkelmann M., Voros J., Csucs C., Brunette D.M., et al. Chemically patterned, metal-oxide-based surfaces produced by photolithographic techniques for studying protein- and cell-interactions. II: protein adsorption and early cell interactions. Biomaterials 2003, 24:1147-1158.
53. Tsukamoto T., Matsui T., Fukase M., Fujita T. Platelet-derived growth factor B chain homodimer enhances chemotaxis and DNA synthesis in normal osteoblast-like cells (MC3T3-E1). Biochem Biophys Res Commun 1991, 175:745-751.
54. Lind M., Eriksen E.F., Bunger C. Bone morphogenetic protein-2 but not bone morphogenetic protein-4 and -6 stimulates chemotactic migration of human osteoblasts, human marrow osteoblasts, and U2-OS cells. Bone 1996, 18:53-57.
55. Mayr-Wohlfart U., Waltenberger J., Hausser H., Kessler S., Günther K.P., Dehio C., et al. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 2002, 30:472-477.
56. Boontheekul T., Mooney D.J. Protein-based signaling systems in tissue engineering. Curr Opin Biotechnol 2003, 14:559-565.
57. Backer M.V., Patel V., Jehning B.T., Claffey K.P., Backer J.M. Surface immobilization of active vascular endothelial growth factor via a cysteine-containing tag. Biomaterials 2006, 27:5452-5458.
58. Bluteau G., Julien M., Magne D., Mallein-Gerin F., Weiss P., Daculsi G., et al. VEGF and VEGF receptors are differentially expressed in chondrocytes. Bone 2007, 40:568-576.
59. Park Y.J., Kim K.H., Lee J.Y., Ku Y., Lee S.J., Min B.M., et al. Immobilization of bone morphogenetic protein-2 on a nanofibrous chitosan membrane for enhanced guided bone regeneration. Biotechnol Appl Biochem 2006, 43:17-24.
60. Shen H., Hu X., Yang F., Bei J., Wang S. The bioactivity of rhBMP-2 immobilized poly(lactide-co-glycolide) scaffolds. Biomaterials 2009, 30:3150-3157.
61. Popat K.C., Eltgroth M., Latempa T.J., Grimes C.A., Desai T.A. Decreased Staphylococcus epidermis adhesion and increased osteoblast functionality on antibiotic-loaded titania nanotubes. Biomaterials 2007, 28:4880-4888.
62. 5 controls osteoblastic proliferation and differentiation responses to titanium substrates presenting different roughness characteristics in a roughness independent manner. J Biomed Mater Res A 2007, 80:700-710.
63. van den Beucken J.J., Walboomers X.F., Boerman O.C., Vos M.R.J., Sommerdijk N.A.J.M., Hayakawa T., et al. Functionalization of multilayered DNA-coatings with bone morphogenetic protein 2. J Control Release 2006, 113:63-72.