Release and bioactivity of bone morphogenetic protein-2 are affected by scaffold binding techniques in vitro and in vivo

Journal of Controlled Release

Volumn 197, Issue , 2015, Pages 148-157

  Suliman, Salwa ^a   Xing, Zhe ^a   Wu, Xujun ^b   Xue, Ying ^a   Pedersen, Torbjorn O ^a   Sun, Yang ^c   Døskeland, Anne P ^d   Nickel, Joachim ^e,f   Waag, Thilo ^h   Lygre, Henning ^d   Finne Wistrand, Anna ^c   Steinmüller Nethl, Doris ^g   Krueger, Anke ^h   Mustafa, Kamal ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^d UNIVERSITY OF BERGEN   (Norway)

^e UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^f FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

^g DiaCoating GmbH   (Austria)

^h UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Copolymer scaffold; Drug delivery; Functionalization; Growth factor; Nanodiamond; Tissue engineering

Indexed keywords

BIOACTIVITY; BONE; CELL CULTURE; COMPUTERIZED TOMOGRAPHY; DEFECTS; DRUG DELIVERY; GENE EXPRESSION; MASS SPECTROMETRY; MINERALOGY; NANODIAMONDS; PROTEINS; STEM CELLS; TISSUE ENGINEERING;

BONE MORPHOGENETIC PROTEIN-2; COPOLYMER SCAFFOLDS; EXTRACELLULAR PROTEINS; FUNCTIONALIZATIONS; GROWTH FACTOR; HUMAN MESENCHYMAL STEM CELLS; NANO-DIAMOND PARTICLES; OSTEOGENIC POTENTIAL;

SCAFFOLDS (BIOLOGY);

ALIZARIN RED S; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; MOLECULAR SCAFFOLD; NANODIAMOND; OSTEOCALCIN; POLYCAPROLACTONE; POLYLACTIDE; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; TRANSCRIPTION FACTOR RUNX2; LACTIDE-CAPROLACTONE COPOLYMER; MICROSPHERE; POLYESTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DRUG BINDING; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; JAW MALFORMATION; LOW DRUG DOSE; MALE; MASS SPECTROMETRY; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; MINERALIZATION; NANOENCAPSULATION; NONHUMAN; PROTEIN EXPRESSION; RAT; SUSTAINED DRUG RELEASE; TISSUE SCAFFOLD; UPREGULATION; ANIMAL; BONE REGENERATION; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICROSPHERES; POLYESTERS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TISSUE SCAFFOLDS;

EID: 84912055096     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.11.003     Document Type: Article

References (59)

1. K. Lee, E.A. Silva, D.J. Mooney, Growth factor delivery-based tissue engineering: general approaches and a review of recent developments, J. R. Soc. Interface./R. Soc. 8 (2011) 153-170.
2. J.E. Schroeder, R. Mosheiff, Tissue engineering approaches for bone repair: concepts and evidence, Injury 42 (2011) 609-613.
3. Q. Zhang, Q.F. He, T.H. Zhang, X.L. Yu, Q. Liu, F.L. Deng, Improvement in the delivery system of bone morphogenetic protein-2: a new approach to promote bone formation, Biomed. Mater. 7 (2012) 045002.
4. S. Govender, C. Csimma, H.K. Genant, A. Valentin-Opran, Y. Amit, R. Arbel, H. Aro, D. Atar, M. Bishay, M.G. Borner, P. Chiron, P. Choong, J. Cinats, B. Courtenay, R. Feibel, B. Geulette, C. Gravel, N. Haas, M. Raschke, E. Hammacher, D. van der Velde, P. Hardy, M. Holt, C. Josten, R.L. Ketterl, B. Lindeque, G. Lob, H. Mathevon, G. McCoy, D. Marsh, R. Miller, E. Munting, S. Oevre, L. Nordsletten, A. Patel, A. Pohl, W. Rennie, P. Reynders, P.M. Rommens, J. Rondia, W.C. Rossouw, P.J. Daneel, S. Ruff, A. Ruter, S. Santavirta, T.A. Schildhauer, C. Gekle, R. Schnettler, D. Segal, H. Seiler, R.B. Snowdowne, J. Stapert, G. Taglang, R. Verdonk, L. Vogels, A. Weckbach, A. Wentzensen, T. Wisniewski, B.M.P.E.i.S.f.T.T.S. Group, Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients, J. Bone Joint Surg. 84-A (2002) 2123-2134.
5. L.B. Shields, G.H. Raque, S.D. Glassman, M. Campbell, T. Vitaz, J. Harpring, C.B. Shields, Adverse effects associated with high-dose recombinant human bone morphogenetic protein-2 use in anterior cervical spine fusion, Spine 31 (2006) 542-547.
6. A.C. Carreira, F.H. Lojudice, E. Halcsik, R.D. Navarro, M.C. Sogayar, J.M. Granjeiro, Bone morphogenetic proteins: facts, challenges, and future perspectives, J. Dent. Res. 93 (2014) 335-345.
7. J.P. Issa, M.V. Bentley, M.M. Iyomasa, W. Sebald, R.F. De Albuquerque, Sustained release carriers used to delivery bone morphogenetic proteins in the bone healing process, Anat. Histol. Embryol. 37 (2008) 181-187.
8. T.H. Kim, Y.P. Yun, Y.E. Park, S.H. Lee, W. Yong, J. Kundu, J.W. Jung, J.H. Shim, D.W. Cho, S.E. Kim, H.R. Song, In vitro and in vivo evaluation of bone formation using solid freeform fabrication-based bone morphogenic protein-2 releasing PCL/PLGA scaffolds, Biomed. Mater. 9 (2014) 025008.
9. E.L. Hsu, J.H. Ghodasra, A. Ashtekar, M.S. Nickoli, S.S. Lee, S.I. Stupp, W.K. Hsu, A comparative evaluation of factors influencing osteoinductivity among scaffolds designed for bone regeneration, Tissue Eng. A 19 (2013) 1764-1772.
10. G.Wu, Y. Liu, T. Iizuka, E.B. Hunziker, The effect of a slowmode of BMP-2 delivery on the in flammatory response provoked by bone-defect-filling polymeric scaffolds, Biomaterials 31 (2010) 7485-7493.
11. D.H. Kempen, L. Lu, T.E. Hefferan, L.B. Creemers, A. Maran, K.L. Classic, W.J. Dhert, M.J. Yaszemski, Retention of in vitro and in vivo BMP-2 bioactivities in sustained delivery vehicles for bone tissue engineering, Biomaterials 29 (2008) 3245-3252.
12. S. Asamura, Y. Mochizuki, M. Yamamoto, Y. Tabata, N. Isogai, Bone regeneration using a bone morphogenetic protein-2 saturated slow-release gelatin hydrogel sheet: evaluation in a canine orbital fl oor fracture model, Ann. Plast. Surg. 64 (2010) 496-502.
13. S. Srouji, D. Ben-David, R. Lotan, E. Livne, R. Avrahami, E. Zussman, Slow-release human recombinant bone morphogenetic protein-2 embedded within electrospun scaffolds for regeneration of bone defect: in vitro and in vivo evaluation, Tissue Eng. A 17 (2011) 269-277.
14. A. Shekaran, A.J. Garcia, Extracellular matrix-mimetic adhesive biomaterials for bone repair, J. Biomed. Mater. Res. A 96 (2011) 261-272.
15. F. Yang, J. Wang, J. Hou, H. Guo, C. Liu, Bone regeneration using cell-mediated responsive degradable PEG-based scaffolds incorporating with rhBMP-2, Biomaterials 34 (2013) 1514-1528.
16. H. Zhang, F. Migneco, C.Y. Lin, S.J. Hollister, Chemically-conjugated bone morphogenetic protein-2 on three-dimensional polycaprolactone scaffolds stimulates osteogenic activity in bone marrow stromal cells, Tissue Eng. A 16 (2010) 3441-3448.
17. T.S. Tsapikouni, Y.F. Missirlis, Protein-material interactions: from micro-to-nano scale, Sci. Eng. B Adv. Funct. Solid-State Mater. 152 (2008) 2-7.
18. S. Freiberg, X.X. Zhu, Polymermicrospheres for controlled drug release, Int. J. Pharm. 282 (2004) 1-18.
19. C. Nugraha, M. Bora, S.S. Venkatraman, Release retardation of model protein on polyelectrolyte-coated PLGA nano- and microparticles, PLoS One 9 (2014) e92393.
20. F.R. Kloss, M. Najam-Ul-Haq, M. Rainer, R. Gassner, G. Lepperdinger, C.W. Huck, G. Bonn, F. Klauser, X. Liu, N. Memmel, E. Bertel, J.A. Garrido, D. Steinmuller-Nethl, Nanocrystalline diamond-an excellent platform for life science applications, J. Nanosci. Nanotechnol. 7 (2007) 4581-4587.
21. A. Krueger, D. Lang, Functionality is key: recent progress in the surface modification of nanodiamond, Adv. Funct. Mater. 22 (2012) 890-906.
22. M. Mansoorianfar, M.A. Shokrgozar, M. Mehrjoo, E. Tamjid, A. Simchi, Nanodiamonds for surface engineering of orthopedic implants: enhanced biocompatibility in human osteosarcoma cell culture, Diam. Relat. Mater. 40 (2013) 107-114.
23. V.N. Mochalin, A. Pentecost, X.M. Li, I. Neitzel, M. Nelson, C.Y. Wei, T. He, F. Guo, Y. Gogotsi, Adsorption of drugs on nanodiamond: toward development of a drug delivery platform, Mol. Pharm. 10 (2013) 3728-3735.
24. L. Moore, M. Gatica, H. Kim, E. Osawa, D. Ho, Multi-protein delivery by nanodiamonds promotes bone formation, J. Dent. Res. 92 (2013) 976-981.
25. D. Steinmuller-Nethl, F.R. Kloss, M. Najam-Ul-Haq, M. Rainer, K. Larsson, C. Linsmeier, G. Kohler, C. Fehrer, G. Lepperdinger, X. Liu, N. Memmel, E. Bertel, C.W. Huck, R. Gassner, G. Bonn, Strong binding of bioactive BMP-2 to nanocrystalline diamond by physisorption, Biomaterials 27 (2006) 4547-4556.
26. F.R. Kloss, R. Gassner, J. Preiner, A. Ebner, K. Larsson, O. Hachl, T. Tuli, M. Rasse, D. Moser, K. Laimer, E.A. Nickel, G. Laschober, R. Brunauer, G. Klima, P. Hinterdorfer, D. Steinmuller-Nethl, G. Lepperdinger, The role of oxygen termination of nanocrystalline diamond on immobilisation of BMP-2 and subsequent bone formation, Biomaterials 29 (2008) 2433-2442.
27. A. Krueger, New carbon materials: biological applications of functionalized nanodiamond materials, Chemistry 14 (2008) 1382-1390.
28. Z. Xing, T.O. Pedersen, X. Wu, Y. Xue, Y. Sun, A. Finne-Wistrand, F.R. Kloss, T. Waag, A. Krueger, D. Steinmuller-Nethl, K. Mustafa, Biological effects of functionalizing copolymer scaffolds with nanodiamond particles, Tissue Eng. A 19 (2013) 1783-1791.
29. E.B. Hunziker, L. Enggist, A. Kuffer, D. Buser, Y. Liu, Osseointegration: the slow delivery of BMP-2 enhances osteoinductivity, Bone 51 (2012) 98-106.
30. G. Bhakta, B. Rai, Z.X. Lim, J.H. Hui, G.S. Stein, A.J. van Wijnen, V. Nurcombe, G.D. Prestwich, S.M. Cool, Hyaluronic acid-based hydrogels functionalized with heparin that support controlled release of bioactive BMP-2, Biomaterials 33 (2012) 6113-6122.
31. S. Danmark, A. Finne-Wistrand, M. Wendel, K. Arvidson, A.C. Albertsson, K. Mustafa, Osteogenic differentiation by rat bone marrow stromal cells on customized biodegradable polymer scaffolds, J. Bioact. Compat. Polym. 25 (2010) 207-223.
32. S.B. Idris, S. Danmark, A. Finne-Wistrand, K. Arvidson, A.C. Albertsson, A.I. Bolstad, K. Mustafa, Biocompatibility of polyester scaffolds with fibroblasts and osteoblast-like cells for bone tissue engineering, J. Bioact. Compat. Polym. 25 (2010) 567-583.
33. U. Edlund, S. Danmark, A.C. Albertsson, A strategy for the covalent functionalization of resorbable polymers with heparin and osteoinductive growth factor, Biomacromolecules 9 (2008) 901-905.
34. T. Kirsch, J. Nickel, W. Sebald, BMP-2 antagonists emerge from alterations in the low-affinity binding epitope for receptor BMPR-II, EMBO J. 19 (2000) 3314-3324.
35. A. Krüger, F. Kataoka, M. Ozawa, T. Fujino, Y. Suzuki, A.E. Aleksenskii, A.Y. Vul', E. O¯sawa, Unusually tight aggregation in detonation nanodiamond: identification and disintegration, Carbon 43 (2005) 1722-1730.
36. Y. Yang, G. Tang, H. Zhang, Y. Zhao, X. Yuan, Y. Fan, M. Wang, Controlled release of BSA by microsphere-incorporated PLGA scaffolds under cyclic loading, Mater. Sci. Eng. C 31 (2011) 350-356.
37. G. Wei, Q. Jin, W.V. Giannobile, P.X. Ma, Nano-fibrous scaffold for controlled delivery of recombinant human PDGF-BB, J. Control. Release 112 (2006) 103-110.
38. Z.Q. Fei, Y.Y. Hu, D.C.Wu, H.Wu, R. Lu, J.P. Bai, H.X. Song, Preparation and property of a novel bone graft composite consisting of rhBMP-2 loaded PLGA microspheres and calcium phosphate cement, J. Mater. Sci. Mater. Med. 19 (2008) 1109-1116.
39. A.C. Kroksveen, E. Aasebo, H. Vethe, V. Van Pesch, D. Franciotta, C.E. Teunissen, R.J. Ulvik, C. Vedeler, K.M. Myhr, H. Barsnes, F.S. Berven, Discovery and initial verification of differentially abundant proteins between multiple sclerosis patients and controls using iTRAQ and SID-SRM, J. Proteome 78 (2013) 312-325.
40. Z. Xing, Y. Xue, S. Danmark, A. Finne-Wistrand, K. Arvidson, S. Hellem, Z.Q. Yang, K. Mustafa, Comparison of short-run cell seeding methods for poly(L-lactide-co-1,5-dioxepan-2-one) scaffold intended for bone tissue engineering, Int. J. Artif. Organs 34 (2011) 432-441.
41. K. Mustafa, A. Wennerberg, J. Wroblewski, K. Hultenby, B.S. Lopez, K. Arvidson, Determining optimal surface roughness of TiO2 blasted titanium implant material for attachment, proliferation and differentiation of cells derived from human mandibular alveolar bone, Clin. Oral Implant. Res. 12 (2001) 515-525.
42. J. Schnabl, R. Glueckert, G. Feuchtner, W. Recheis, T. Potrusil, V. Kuhn, A. Wolf-Magele, H. Riechelmann, G.M. Sprinzl, Sheep as a large animal model for middle and inner ear implantable hearing devices: a feasibility study in cadavers, Otol. Neurotol. 33 (2012) 481-489.
43. Z. Xing, Y. Xue, S. Danmark, K. Schander, S. Ostvold, K. Arvidson, S. Hellem, A. Finne-Wistrand, A.C. Albertsson, K. Mustafa, Effect of endothelial cells on bone regeneration using poly(L-lactide-co-1,5-dioxepan-2-one) scaffolds, J. Biomed. Mater. Res. A 96 (2011) 349-357.
44. S.A. Gerber, J. Rush, O. Stemman, M.W. Kirschner, S.P. Gygi, Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6940-6945.
45. S. Danmark, A. Finne-Wistrand, K. Schander, M. Hakkarainen, K. Arvidson, K. Mustafa, A.C. Albertsson, In vitro and in vivo degradation profile of aliphatic polyesters subjected to electron beam sterilization, Acta Biomater. 7 (2011) 2035-2046.
46. O. Jeon, S.J. Song, H.S. Yang, S.H. Bhang, S.W. Kang, M.A. Sung, J.H. Lee, B.S. Kim, Long-term delivery enhances in vivo osteogenic efficacy of bonemorphogenetic protein-2 compared to short-term delivery, Biochem. Biophys. Res. Commun. 369 (2008) 774-780.
47. J. Mona, C.J. Kuo, E. Perevedentseva, A.V. Priezzhev, C.L. Cheng, Adsorption of human blood plasma on nanodiamond and its influence on activated partial thromboplastin time, Diam. Relat. Mater. 39 (2013) 73-77.
48. M. Mehta, K. Schmidt-Bleek, G.N. Duda, D.J. Mooney, Biomaterial delivery of morphogens to mimic the natural healing cascade in bone, Adv. Drug Deliv. Rev. 64 (2012) 1257-1276.
49. K. Goldberg, A. Krueger, T. Meinhardt, W. Kroutil, B. Mautner, A. Liese, Novel immobilization routes for the covalent binding of an alcohol dehydrogenase from Rhodococcus ruber DSM 44541, Tetrahedron Asymmetry 19 (2008) 1171-1173.
50. M. Okamoto, J. Murai, H. Yoshikawa, N. Tsumaki, Bone morphogenetic proteins in bone stimulate osteoclasts and osteoblasts during bone development, J. Bone Miner. Res. Off. J. Am. Soc. Bone Miner. Res. 21 (2006) 1022-1033.
51. S. Granholm, P. Henning, C. Lindholm, U.H. Lerner, Osteoclast progenitor cells present in significant amounts in mouse calvarial osteoblast isolations and osteoclastogenesis increased by BMP-2, Bone 52 (2013) 83-92.
52. Z. Huang, E.R. Nelson, R.L. Smith, S.B. Goodman, The sequential expression profiles of growth factors from osteoprogenitors [correction of osteroprogenitors] to osteoblasts in vitro, Tissue Eng. 13 (2007) 2311-2320.
53. E. Birmingham, G.L. Niebur, P.E. McHugh, G. Shaw, F.P. Barry, L.M. McNamara, Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche, Eur. Cells Mater. 23 (2012) 13-27.
54. M.C. Simmonds, J.V.E. Brown, M.K. Heirs, J.P.T. Higgins, R.J. Mannion, M.A. Rodgers, L.A. Stewart, Safety and effectiveness of recombinant human bone morphogenetic protein-2 for spinal fusion: a meta-analysis of individual-participant data, Ann. Intern. Med. 158 (2013) 877- +.
55. V.E. Santo, M.E. Gomes, J.F. Mano, R.L. Reis, Controlled release strategies for bone, cartilage, and osteochondral engineering-Part II: challenges on the evolution from single to multiple bioactive factor delivery, Tissue Eng. B Rev. 19 (2013) 327-352.
56. Y. Liu, K. de Groot, E.B. Hunziker, BMP-2 liberated frombiomimetic implant coatings induces and sustains direct ossifi cation in an ectopic rat model, Bone 36 (2005) 745-757.
57. S. Jo, S. Kim, T.H. Cho, E. Shin, S.J. Hwang, I. Noh, Effects of recombinant human bone morphogenic protein-2 and human bone marrow-derived stromal cells on in vivo bone regeneration of chitosan-poly(ethylene oxide) hydrogel, J. Biomed. Mater. Res. A 101 (2013) 892-901.
58. M. Pelaez, C. Susin, J. Lee, T. Fiorini, F.C. Bisch, D.R. Dixon, J.C. McPherson, A.N. Buxton III, U.M. Wikesjo, Effect of rhBMP-2 dose on bone formation/maturation in a rat critical-size calvarial defect model, J. Clin. Periodontol. 41 (2014) 827-836.
59. F.C.J. van deWatering, J. van den Beucken, S.P. van der Woning, A. Briest, A. Eek, H. Qureshi, L. Winnubst, O.C. Boerman, J.A. Jansen, Non-glycosylated BMP-2 can induce ectopic bone formation at lower concentrations compared to glycosylated BMP-2, J. Control. Release 159 (2012) 69-77.