Hypoxia-mimicking bioactive glass/collagen glycosaminoglycan composite scaffolds to enhance angiogenesis and bone repair

Biomaterials

Volumn 52, Issue 1, 2015, Pages 358-366

  Quinlan, Elaine ^a,b   Partap, Sonia ^a,b   Azevedo, Maria M ^c   Jell, Gavin ^c,d   Stevens, Molly M ^c   O'Brien, Fergal J ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Angiogenesis; Bioactive glass; Cobalt; Collagen; Regenerative medicine; Scaffold

Indexed keywords

BONE; CELL ENGINEERING; CELL PROLIFERATION; COBALT; COLLAGEN; ENDOTHELIAL CELLS; MOBILE SECURITY; PARTICLE SIZE; PARTICLE SIZE ANALYSIS; SCAFFOLDS; SCAFFOLDS (BIOLOGY); TISSUE; TISSUE ENGINEERING; TISSUE REGENERATION; TRANSCRIPTION;

ANGIOGENESIS; BONE TISSUE ENGINEERING; BONE TISSUE REGENERATION; HYPOXIA-INDUCIBLE FACTORS; REGENERATIVE MEDICINE; TISSUE ENGINEERED CONSTRUCTS; TISSUE-ENGINEERED SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

BIOACTIVE GLASS;

CALCIUM; COBALT; GLYCOSAMINOGLYCAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN; BIOMATERIAL; COLLAGEN; GLASS; HIF1A PROTEIN, HUMAN; ION; OXYGEN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ARTICLE; BONE REMODELING; BONE TISSUE; CELL COUNT; CELL PROLIFERATION; ENDOTHELIUM CELL; HUMAN; HYPOXIA; IN VITRO STUDY; ION PAIR CHROMATOGRAPHY; OSTEOBLAST; OXYGEN CONCENTRATION; PARTICLE SIZE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; TISSUE REGENERATION; VASCULARIZATION; ANOXIA; BONE; BONE DEVELOPMENT; BONE REGENERATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; METABOLISM; PATHOLOGY; POROSITY; PROCEDURES; TISSUE ENGINEERING; TISSUE SCAFFOLD; UMBILICAL VEIN ENDOTHELIAL CELL;

ANOXIA; BIOCOMPATIBLE MATERIALS; BONE AND BONES; BONE REGENERATION; CELLS, CULTURED; COBALT; COLLAGEN; GLASS; GLYCOSAMINOGLYCANS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IONS; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOBLASTS; OSTEOGENESIS; OXYGEN; POROSITY; REGENERATIVE MEDICINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84927754012     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.006     Document Type: Article

References (57)

1. Younger E.M., Chapman M.W. Morbidity at bone graft donor sites. JOrthop Trauma 1989, 3:192-195.
2. Jones J.R., Gentleman E., Polak J. Bioactive glass scaffolds for bone regeneration. Elements 2007, 3:393-399.
3. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260:920-926.
4. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials 2004, 25:1077-1086.
5. O'Brien F.J. Biomaterials & scaffolds for tissue engineering. Mater Today 2011, 14:88-95.
6. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26:433-441.
7. Tierney C.M., Jaasma M.J., O'Brien F.J. Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations. JBiomed Mater Res Part A 2009, 91:92-101.
8. Lyons F.G., Al-Munajjed A.A., Kieran S.M., Toner M.E., Murphy C.M., Duffy G.P., et al. The healing of bony defects by cell-free collagen-based scaffolds compared to stem cell-seeded tissue engineered constructs. Biomaterials 2010, 31:9232-9243.
9. Alhag M., Farrell E., Toner M., Lee T.C., O'Brien F.J., Claffey N. Evaluation of the ability of collagen-glycosaminoglycan scaffolds with or without mesenchymal stem cells to heal bone defects in Wistar rats. Oral Maxillofac Surg 2012, 16:47-55.
10. Alhag M., Farrell E., Toner M., Claffey N., Lee T.C., O'Brien F. Evaluation of early healing events around mesenchymal stem cell-seeded collagen-glycosaminoglycan scaffold. An experimental study in Wistar rats. Oral Maxillofac Surg 2011, 15:31-39.
11. Hoppe A., Guldal N.S., Boccaccini A.R. Areview of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 2011, 32:2757-2774.
12. Maeno S., Niki Y., Matsumoto H., Morioka H., Yatabe T., Funayama A., et al. The effect of calcium ion concentration on osteoblast viability, proliferation and differentiation in monolayer and 3D culture. Biomaterials 2005, 26:4847-4855.
13. Gentleman E., Fredholm Y.C., Jell G., Lotfibakhshaiesh N., O'Donnell M.D., Hill R.G., et al. The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts invitro. Biomaterials 2010, 31:3949-3956.
14. Ahmed I., Parsons A., Jones A., Walker G., Scotchford C., Rudd C. Cytocompatibility and effect of increasing MgO content in a range of quaternary invert phosphate-based glasses. JBiomater Appl 2010, 24:555-575.
15. Hench L.L. Genetic design of bioactive glass. JEur Ceram Soc 2009, 29:1257-1265.
16. Novosel E.C., Kleinhans C., Kluger P.J. Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 2011, 63:300-311.
17. Epstein N.E. Pros, cons, and costs of INFUSE in spinal surgery. Surg Neurol Int 2011, 2:10.
18. Hamm A., Krott N., Breibach I., Blindt R., Bosserhoff A.K. Efficient transfection method for primary cells. Tissue Eng 2002, 8:235-245.
19. Trentin D., Hall H., Wechsler S., Hubbell J.A. Peptide-matrix-mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1alpha variant for local induction of angiogenesis. Proc Natl Acad Sci U S A 2006, 103:2506-2511.
20. Malda J., Klein T.J., Upton Z. The roles of hypoxia in the invitro engineering of tissues. Tissue Eng 2007, 13:2153-2162.
21. Buttyan R., Chichester P., Stisser B., Matsumoto S., Ghafar M.A., Levin R.M. Acute intravesical infusion of a cobalt solution stimulates a hypoxia response, growth and angiogenesis in the rat bladder. JUrology 2003, 169:2402-2406.
22. Kim H.H., Lee S.E., Chung W.J., Choi Y., Kwack K., Kim S.W., et al. Stabilization of hypoxia-inducible factor-1alpha is involved in the hypoxic stimuli-induced expression of vascular endothelial growth factor in osteoblastic cells. Cytokine 2002, 17:14-27.
23. Schoubben A., Blasi P., Giovagnoli S., Rossi C., Ricci M. Development of a scalable procedure for fine calcium alginate particle preparation. Chem Eng J 2010, 160:363-369.
24. Hu X., Yu S.P., Fraser J.L., Lu Z., Ogle M.E., Wang J.A., et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. JThorac Cardiovasc Surg 2008, 135:799-808.
25. Azevedo M.M., Jell G., O'Donnell M.D., Law R.V., Hill R.G., Stevens M.M. Synthesis and characterization of hypoxia-mimicking bioactive glasses for skeletal regeneration. JMater Chem 2010, 20:8854-8864.
26. Azevedo M.M., Tsigkou O., Nair R., Jones J.R., Jell G., Stevens M.M. Hypoxia inducible factor-stabilizing bioactive glasses for directing mesenchymal stem cell behavior. Tissue Eng Part A 2015, 21:382-389.
27. Murphy C.M., O'Brien F.J. Understanding the effect of mean pore size on cell activity in collagen-glycosaminoglycan scaffolds. Cell Adhes Migr 2010, 4:377-381.
28. Tierney C.M., Haugh M.G., Liedl J., Mulcahy F., Hayes B., O'Brien F.J. The effects of collagen concentration and crosslink density on the biological, structural and mechanical properties of collagen-GAG scaffolds for bone tissue engineering. JMech Behav Biomed Mater 2009, 2:202-209.
29. Haugh M.G., Jaasma M.J., O'Brien F.J. The effect of dehydrothermal treatment on the mechanical and structural properties of collagen-GAG scaffolds. JBiomed Mater Res Part A 2009, 89:363-369.
30. 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 U S A 2002, 99:9656-9661.
31. Wan C., Gilbert S.R., Wang Y., Cao X., Shen X., Ramaswamy G., et al. Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci U S A 2008, 105:686-691.
32. Street J., Winter D., Wang J.H., Wakai A., McGuinness A., Redmond H.P. Is human fracture hematoma inherently angiogenic?. Clin Orthop Relat Res 2000, 378:224-237.
33. Peters K., Unger R.E., Barth S., Gerdes T., Kirkpatrick C.J. Induction of apoptosis in human microvascular endothelial cells by divalent cobalt ions. Evidence for integrin-mediated signaling via the cytoskeleton. JMater Sci Mater Med 2001, 12:955-958.
34. Wu C., Zhou Y., Fan W., Han P., Chang J., Yuen J., et al. Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials 2012, 33:2076-2085.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
36. Namiki A., Brogi E., Kearney M., Kim E.A., Wu T., Couffinhal T., et al. Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. JBiol Chem 1995, 270:31189-31195.
37. Steinbrech D.S., Mehrara B.J., Saadeh P.B., Greenwald J.A., Spector J.A., Gittes G.K., et al. VEGF expression in an osteoblast-like cell line is regulated by a hypoxia response mechanism. Am J Physiol Cell Physiol 2000, 278:C853-C860.
38. Lieberman J.R., Daluiski A., Einhorn T.A. The role of growth factors in the repair of bone. Biology and clinical applications. JBone Jt Surg Am Volume 2002, 84-A:1032-1044.
39. Rahaman M.N., Day D.E., Bal B.S., Fu Q., Jung S.B., Bonewald L.F., et al. Bioactive glass in tissue engineering. Acta Biomater 2011, 7:2355-2373.
40. Leu A., Leach J.K. Proangiogenic potential of a collagen/bioactive glass substrate. Pharm Res 2008, 25:1222-1229.
41. Cunniffe G.M., Dickson G.R., Partap S., Stanton K.T., O'Brien F.J. Development and characterisation of a collagen nano-hydroxyapatite composite scaffold for bone tissue engineering. JMater Sci Mater Med 2010, 21:2293-2298.
42. Gleeson J.P., Plunkett N.A., O'Brien F.J. Addition of hydroxyapatite improves stiffness, interconnectivity and osteogenic potential of a highly porous collagen-based scaffold for bone tissue regeneration. Eur cells Mater 2010, 20:218-230.
43. Stacker S.A., Achen M.G. The vascular endothelial growth factor family: signalling for vascular development. Growth Factors 1999, 17:1-11.
44. Peng H., Usas A., Olshanski A., Ho A.M., Gearhart B., Cooper G.M., et al. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. Journal of bone and mineral research. Off J Am Soc Bone Mineral Res 2005, 20:2017-2027.
45. Semenza G.L. Life with oxygen. Science 2007, 318:62-64.
46. Azevedo M.M., Tsigkou O., Nair R., Jell G., Jones J., Stevens M. HIF-stabilizing bioactive glasses for directing MSC behaviour. Tissue Eng Part A 2014.
47. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992, 359:843-845.
48. Gorustovich A.A., Roether J.A., Boccaccini A.R. Effect of bioactive glasses on angiogenesis: a review of invitro and invivo evidences. Tissue Eng Part B Rev 2010, 16:199-207.
49. Kent Leach J., Kaigler D., Wang Z., Krebsbach P.H., Mooney D.J. Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration. Biomaterials 2006, 27:3249-3255.
50. Matsiko A., Levingstone T.J., O'Brien F.J., Gleeson J.P. Addition of hyaluronic acid improves cellular infiltration and promotes early-stage chondrogenesis in a collagen-based scaffold for cartilage tissue engineering. JMech Behav Biomed Mater 2012, 11:41-52.
51. Hench L.L., Polak J.M. Third-generation biomedical materials. Science 2002, 295:1014-1017.
52. Jones J.R., Tsigkou O., Coates E.E., Stevens M.M., Polak J.M., Hench L.L. Extracellular matrix formation and mineralization on a phosphate-free porous bioactive glass scaffold using primary human osteoblast (HOB) cells. Biomaterials 2007, 28:1653-1663.
53. Bergeron E., Marquis M.E., Chretien I., Faucheux N. Differentiation of preosteoblasts using a delivery system with BMPs and bioactive glass microspheres. JMater Sci Mater M 2007, 18:255-263.
54. Hattar S., Asselin A., Greenspan D., Oboeuf M., Berdal A., Sautier J.M. Potential of biomimetic surfaces to promote invitro osteoblast-like cell differentiation. Biomaterials 2005, 26:839-848.
55. Xynos I.D., Edgar A.J., Buttery L.D., Hench L.L., Polak J.M. Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass 45S5 dissolution. JBiomed Mater Res 2001, 55:151-157.
56. Alcaide M., Portoles P., Lopez-Noriega A., Arcos D., Vallet-Regi M., Portoles M.T. Interaction of an ordered mesoporous bioactive glass with osteoblasts, fibroblasts and lymphocytes, demonstrating its biocompatibility as a potential bone graft material. Acta Biomater 2010, 6:892-899.
57. Patel Z.S., Young S., Tabata Y., Jansen J.A., Wong M.E., Mikos A.G. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 2008, 43:931-940.