A collagen-hydroxyapatite scaffold allows for binding and co-delivery of recombinant bone morphogenetic proteins and bisphosphonates

Acta Biomaterialia

Volumn 10, Issue 5, 2014, Pages 2250-2258

  Murphy, Ciara M ^a,b   Schindeler, Aaron ^a,b   Gleeson, John P ^c   Yu, Nicole Y C ^a,b   Cantrill, Laurence C ^a,b   Mikulec, Kathy ^a   Peacock, Lauren ^a   O'Brien, Fergal J ^c,d   Little, David G ^a,b  

^a CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^b University of Sydney   (Australia)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Bisphosphonate; Collagen; Hydroxyapatite; rhBMP 2; Zoledronic acid

Indexed keywords

BIOMIMETICS; BONE; HYDROXYAPATITE; RECOMBINANT PROTEINS; SCAFFOLDS (BIOLOGY); SURGERY;

'CURRENT; BISPHOSPHONATES; BONE HEALING; BONE MORPHOGENETIC PROTEINS; CO DELIVERIES; COLLAGEN-BASED SCAFFOLDS; HUMAN BONE MORPHOGENETIC PROTEIN; RHBMP-2; TISSUES ENGINEERINGS; ZOLEDRONIC ACID;

COLLAGEN;

COLLAGEN; HYDROXYAPATITE; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; ZOLEDRONIC ACID; ACID PHOSPHATASE; BISPHOSPHONIC ACID DERIVATIVE; BONE MORPHOGENETIC PROTEIN; FLUORESCENT DYE; ISOENZYME; RECOMBINANT PROTEIN; TARTRATE-RESISTANT ACID PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BONE MASS; CONTROLLED STUDY; DRUG BINDING; DRUG DELIVERY SYSTEM; DRUG RELEASE; ELUTION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SCINTILLATION COUNTING; X RAY; X RAY SYSTEM; ANIMAL; BONE; BONE DEVELOPMENT; CELL DEATH; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; OSTEOCLAST; POROSITY; PROSTHESIS IMPLANTATION; RADIOGRAPHY; TISSUE SCAFFOLD; WISTAR RAT;

RATTUS;

ACID PHOSPHATASE; ANIMALS; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; CELL DEATH; COLLAGEN; DIPHOSPHONATES; DRUG DELIVERY SYSTEMS; DURAPATITE; FLUORESCENT DYES; HUMANS; ISOENZYMES; MALE; MICE; OSTEOCLASTS; OSTEOGENESIS; POROSITY; PROSTHESIS IMPLANTATION; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; TISSUE SCAFFOLDS; X-RAY MICROTOMOGRAPHY;

EID: 84898057085     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.01.016     Document Type: Article

References (57)

1. D.G. Little, M. Ramachandran, and A. Schindeler The anabolic and catabolic responses in bone repair J Bone Joint Surg Br 89 2007 425 433
2. P.V. Giannoudis, H. Dinopoulos, and E. Tsiridis Bone substitutes: an update Injury 36 2005 S20 S27
3. F. Hughes, J. Collyer, M. Stanfield, and S. Goodman The effects of bone morphogenetic protein-2,-4, and-6 on differentiation of rat osteoblast cells in vitro Endocrinology 136 1995 2671 2677
4. K. Itoh, N. Udagawa, T. Katagiri, S. Iemura, N. Ueno, and H. Yasuda et al. Bone morphogenetic protein 2 stimulates osteoclast differentiation and survival supported by receptor activator of nuclear factor-κB ligand Endocrinology 142 2001 3656 3662
5. H. Kaneko, T. Arakawa, H. Mano, T. Kaneda, A. Ogasawara, and M. Nakagawa et al. Direct stimulation of osteoclastic bone resorption by bone morphogenetic protein (BMP)-2 and expression of BMP receptors in mature osteoclasts Bone 27 2000 479 486
6. M. Ito Assessment of bone quality - present and future Clin Calcium 14 2004 27 32
7. B.B. Pradhan, H.W. Bae, E.G. Dawson, V.V. Patel, and R.B. Delamarter Graft resorption with the use of bone morphogenetic protein: lessons from anterior lumbar interbody fusion using femoral ring allografts and recombinant human bone morphogenetic protein-2 Spine 31 2006 E277 E284
8. D. Little, M. McDonald, R. Bransford, C. Godfrey, and N. Amanat Manipulation of the anabolic and catabolic responses with OP-1 and zoledronic acid in a rat critical defect model J Bone Miner Res 20 2005 2044 2052
9. D.G. Little, M. Ramachandran, and A. Schindeler The anabolic and catabolic responses in bone repair J Bone Joint Surg Br 89-B 2007 425 433
10. N. Yu, A. Schindeler, L. Peacock, K. Mikulec, J. Fitzpatrick, and A. Ruys et al. Modulation of anabolic and catabolic responses via a porous polymer scaffold manufactured using thermally induced phase separation Eur Cell Mater 25 2013 190 203
11. N.Y.C. Yu, A. Schindeler, L. Peacock, K. Mikulec, P.A. Baldock, and A.J. Ruys et al. In vivo local co-delivery of recombinant human bone morphogenetic protein-7 and pamidronate via poly-d, l-lactic acid Eur Cell Mater 20 2010 431 442
12. D.G. Little, M. McDonald, R. Bransford, C.B. Godfrey, and N. Amanat Manipulation of the anabolic and catabolic responses with OP-1 and zoledronic acid in a rat critical defect model J Bone Miner Res 20 2005 2044 2052
13. J.H. Lin Bisphosphonates: a review of their pharmacokinetic properties Bone 18 1996 75 85
14. M.J. Rogers, S. Gordon, H. Benford, F. Coxon, S. Luckman, and J. Monkkonen et al. Cellular and molecular mechanisms of action of bisphosphonates Cancer 88 2000 2961 2978
15. F.P. Coxon, H.L. Benford, R.G. Russell, and M.J. Rogers Protein synthesis is required for caspase activation and induction of apoptosis by bisphosphonate drugs Mol Pharmacol 54 1998 631 638
16. F.P. Coxon, K. Thompson, A.J. Roelofs, F.H. Ebetino, and M.J. Rogers Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells Bone 42 2008 848 860
17. G.H. Nancollas, R. Tang, R.J. Phipps, Z. Henneman, S. Gulde, and W. Wu et al. Novel insights into actions of bisphosphonates on bone: differences in interactions with hydroxyapatite Bone 38 2006 617 627
18. R. Russell, N. Watts, F. Ebetino, and M. Rogers Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy Osteoporosis Int 19 2008 733 759
19. L. Gong, K. Hoshi, S. Ejiri, T. Nakajima, S. Shingaki, and H. Ozawa Bisphosphonate incadronate inhibits maturation of ectopic bone induced by recombinant human bone morphogenetic protein 2 J Bone Miner Metab 21 2003 5 11
20. J. Monkkonen, J. Simila, and M.J. Rogers Effects of tiludronate and ibandronate on the secretion of proinflammatory cytokines and nitric oxide from macrophages in vitro Life Sci 62 1998 PL95 PL102
21. D. Thiebaud, A. Sauty, P. Burckhardt, P. Leuenberger, L. Sitzler, and J.R. Green et al. An in vitro and in vivo study of cytokines in the acute-phase response associated with bisphosphonates Calcif Tissue Int 61 1997 386 392
22. R.E. Marx, Y. Sawatari, M. Fortin, and V. Broumand Bisphosphonate-induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk factors, recognition, prevention, and treatment J Oral Maxillofac Surg 63 2005 1567 1575
23. C. Jeppsson, J. Astrand, M. Tagil, and P. Aspenberg A combination of bisphosphonate and BMP additives in impacted bone allografts Acta Orthop Scand 74 2003 483 489
24. O. Belfrage, G. Flivik, M. Sundberg, U. Kesteris, and M. Tagil Local treatment of cancellous bone grafts with BMP-7 and zoledronate increases both the bone formation rate and bone density: a bone chamber study in rats Acta Orthop 82 2011 228 233
25. S. Yang, K.F. Leong, Z. Du, and C.K. Chua The design of scaffolds for use in tissue engineering. Part I. Traditional factors Tissue Eng 7 2001 679 689
26. T. Jiang, W.I. Abdel-Fattah, and C.T. Laurencin In vitro evaluation of chitosan/poly(lactic acid-glycolic acid) sintered microsphere scaffolds for bone tissue engineering Biomaterials 27 2006 4894 4903
27. O'Brien FJ, Gleeson J, Plunkett NA, A collagen/hydroxyapatite composite scaffold, and the process for the production thereof. Patent WO 2008/096334 A2, 2008.
28. D. Wahl, and J. Czernuszka Collagen-hydroxyapatite composites for hard tissue repair Eur Cell Mater 11 2006 43 56
29. C.T. Tierney, M.J. Jaasma, and F.J. O'Brien Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations J Biomed Mater Res 91 2009 92 101
30. B. Wu, Q. Zheng, X. Guo, Y. Wu, Y. Wang, and F. Cui Preparation and ectopic osteogenesis in vivo of scaffold based on mineralized recombinant human-like collagen loaded with synthetic BMP-2-derived peptide Biomed Mater 3 2008 044111
31. M.G. Haugh, C.M. Murphy, R.C. McKiernan, C. Altenbuchner, and F.J. O'Brien Crosslinking and mechanical properties significantly influence cell attachment, proliferation, and migration within collagen glycosaminoglycan scaffolds Tissue Eng A 17 2011 1201 1208
32. F.J. O'Brien, B.A. Harley, I.V. Yannas, and L.J. Gibson The effect of pore size on cell adhesion in collagen-GAG scaffolds Biomaterials 26 2005 433 441
33. F.J. O'Brien, B.A. Harley, M.A. Waller, I.V. Yannas, L.J. Gibson, and P.J. Prendergast The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering Technol Health Care 15 2007 3 17
34. C.M. Murphy, M.G. Haugh, and F.J. O'Brien The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering Biomaterials 31 2010 461 466
35. A.A. Sawyer, S.J. Song, E. Susanto, P. Chuan, C.X.F. Lam, and M.A. Woodruff et al. The stimulation of healing within a rat calvarial defect by mPCL-TCP/collagen scaffolds loaded with rhBMP-2 Biomaterials 30 2009 2479 2488
36. J.P. Gleeson, N.A. Plunkett, and F.J. O'Brien Addition of hydroxyapatite improves stiffness, interconnectivity and osteogenic potential of a highly porous collagen-based scaffold for bone tissue regeneration Eur Cells Mater 20 2010 218 230
37. M. Geiger, R.H. Li, and W. Friess Collagen sponges for bone regeneration with rhBMP-2 Adv Drug Deliv Rev 55 2003 1613 1629
38. M.A. Lawson, Z. Xia, B.L. Barnett, J.T. Triffitt, R.J. Phipps, and J.E. Dunford et al. Differences between bisphosphonates in binding affinities for hydroxyapatite J Biomed Mater Res B: Appl Biomater 92B 2010 149 155
39. F.J. O'Brien, B.A. Harley, I.V. Yannas, and L. Gibson Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds Biomaterials 25 2004 1077 1086
40. M.G. Haugh, M.J. Jaasma, and F.J. O'Brien The effect of dehydrothermal treatment on the mechanical and structural properties of collagen-GAG scaffolds J Biomed Mater Res A 89 2009 363 369
41. B.J. Cole, M.P. Bostrom, T.L. Pritchard, D.R. Sumner, E. Tomin, and J.M. Lane et al. Use of bone morphogenetic protein 2 on ectopic porous coated implants in the rat Clin Orthop Relat Res 345 1997 219 228
42. M.A. Scott, B. Levi, A. Askarinam, A. Nguyen, T. Rackohn, and K. Ting et al. Brief review of models of ectopic bone formation Stem Cells Dev 21 2012 655 667
43. A. Schindeler, and D.G. Little Osteoclasts but not osteoblasts are affected by a calcified surface treated with zoledronic acid in vitro Biochem Biophys Res Commun 338 2005 710 716
44. H.J. Seeherman, X.J. Li, M.L. Bouxsein, and J.M. Wozney RhBMP-2 induces transient bone resorption followed by bone formation in a nonhuman primate core-defect model J Bone Joint Surg Am 92 2010 411 426
45. M. Tagil, P. Aspenberg, and J. Astrand Systemic zoledronate precoating of a bone graft reduces bone resorption during remodeling Acta Orthop 77 2006 23 26
46. D.G. Little, M. McDonald, R. Bransford, C.B. Godfrey, and N. Amanat Manipulation of the anabolic and catabolic responses with OP-1 and zoledronic acid in a rat critical defect model J Bone Miner Res 20 2005 2044 2052
47. A.K. Harding, P. Aspenberg, M. Kataoka, D. Bylski, and M. Tagil Manipulating the anabolic and catabolic response in bone graft remodeling: synergism by a combination of local BMP-7 and a single systemic dosis of zoledronate J Orthop Res 26 2008 1245 1249
48. T. Jakobsen, J. Baas, J.E. Bechtold, B. Elmengaard, and K. Soballe Soaking morselized allograft in bisphosphonate can impair implant fixation Clin Orthop Relat Res 463 2007 195 201
49. M. Geiger, R.H. Li, and W. Friess Collagen sponges for bone regeneration with rhBMP-2 Adv Drug Deliv Rev 55 2003 1613 1629
50. W. Friess Collagen-biomaterial for drug delivery Eur J Pharm Biopharm 45 1998 113 136
51. K.B. Lee, C.E. Taghavi, S.S. Murray, K.J. Song, G. Keorochana, and J.C. Wang BMP induced inflammation: a comparison of rhBMP-7 and rhBMP-2 J Orthop Res 30 2012 1985 1994
52. K.V. Brown, B. Li, T. Guda, D.S. Perrien, S.A. Guelcher, and J.C. Wenke Improving bone formation in a rat femur segmental defect by controlling bone morphogenetic protein-2 release Tissue Eng A 17 2011 1735 1746
53. D.A. Wahl, E. Sachlos, C. Liu, and J.T. Czernuszka Controlling the processing of collagen-hydroxyapatite scaffolds for bone tissue engineering J Mater Sci Mater Med 18 2007 201 209
54. S. Dey, and S. Pal Evaluation of collagen-hydroxyapatite scaffold for bone tissue engineering C. Lim, J.H. Goh, 13th International conference on biomedical engineering 2009 Springer Berlin 1267 1270
55. W.J. Chen, S. Jingushi, G. Hirata, Y. Matsumoto, and Y. Iwamoto Intramuscular bone induction by the simultaneous administration of recombinant human bone morphogenetic protein 2 and bisphosphonate for autobone graft Tissue Eng 10 2004 1652 1661
56. W.J. Chen, S. Jingushi, K. Jingushi, and Y. Iwamoto In vivo banking for vascularized autograft bone by intramuscular inoculation of recombinant human bone morphogenetic protein-2 and beta-tricalcium phosphate J Orthop Sci 11 2006 283 288
57. T. Jakobsen, J. Baas, J.E. Bechtold, B. Elmengaard, and K. Soballe The effect of soaking allograft in bisphosphonate: a pilot dose-response study Clin Orthop Relat Res 468 2010 867 874