Controlled copper ion release from phosphate-based glasses improves human umbilical vein endothelial cell survival in a reduced nutrient environment

Tissue Engineering - Part A

Volumn 19, Issue 3-4, 2013, Pages 548-557

  Stähli, Christoph ^a   Muja, Naser ^a   Nazhat, Showan N ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; COPPER COMPOUNDS; CYTOTOXICITY; ENDOTHELIAL CELLS; GLASS; METABOLISM; METAL IONS; NUTRIENTS; SODIUM;

APOPTOTIC ACTIVITY; BOVINE SERUM; CASPASE-3; CONTROLLED RELEASE; COPPER CONCENTRATION; COPPER IONS; DOSE-DEPENDENT MANNER; DOWN-REGULATION; ENGRAFTMENT; GROWTH CONDITIONS; GROWTH FACTOR; HIGH SENSITIVITY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; METABOLIC ACTIVITY; NUTRIENT DIFFUSION; OPTIMAL RESPONSE; VASCULARIZATION;

SCAFFOLDS (BIOLOGY);

BOVINAE;

COPPER; GLASS; ION; PHOSPHATE; TISSUE SCAFFOLD;

ARTICLE; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DELAYED RELEASE FORMULATION; DIFFUSION; DRUG EFFECT; ENDOTHELIUM CELL; HUMAN; METABOLISM; PHYSIOLOGY; UMBILICAL VEIN;

CELL SURVIVAL; CELLS, CULTURED; COPPER; CULTURE MEDIA; DELAYED-ACTION PREPARATIONS; DIFFUSION; ENDOTHELIAL CELLS; GLASS; HUMANS; IONS; PHOSPHATES; TISSUE SCAFFOLDS; UMBILICAL VEINS;

MLCS; MLOWN;

EID: 84872102716     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0223     Document Type: Article

References (49)

1. Hopkins, S.P., Bulgrin, J.P., Sims, R.L., Bowman, B., Dono-van, D.L., and Schmidt, S.P. Controlled delivery of vascular endothelial growth factor promotes neovascularization and maintains limb function in a rabbit model of ischemia. J Vasc Surg 27, 886, 1998.
2. Tabata, Y., Miyao, M., Ozeki, M., and Ikada, Y. Controlled release of vascular endothelial growth factor by use of col-lagen hydrogels. J Biomater Sci Polym Ed 11, 915, 2000.
3. Choong, C.S.N., Hutmacher, D.W., and Triffitt, J.T. Co-culture of bone marrow fibroblasts and endothelial cells on modified polycaprolactone substrates for enhanced poten-tials in bone tissue engineering. Tissue Eng 12, 2521, 2006.
4. Rouwkema, J., De Boer, J., and Van Blitterswijk, C.A. En-dothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. Tissue Eng 12, 2685, 2006.
5. Jain, R.K., Au, P., Tam, J., Duda, D.G., and Fukumura, D. Engineering vascularized tissue. Nat Biotechnol 23, 821, 2005.
6. Beach, R.S., Gershwin, M.E., and Hurley, L.S. Zinc, copper, and manganese in immune function and experimental on-cogenesis. Nutr Cancer 3, 172, 1982.
7. Rayton, J.K., and Harris, E.D. Induction of lysyl oxidase with copper - properties of an invitro system. J Biol Chem 254, 621, 1979.
8. McAuslan, B.R., and Reilly, W. Endothelial-cell phagokinesis in response to specific metal-ions. Exp Cell Res 130,147,1980.
9. Hu, G.F. Copper stimulates proliferation of human endo-thelial cells under culture. J Cell Biochem 69, 326, 1998.
10. Giavaresi, G., Torricelli, P., Fornasari, P.M., Giardino, R., Barbucci, R., and Leone, G. Blood vessel formation after soft-tissue implantation of hyaluronanbased hydrogel supple-mented with copper ions. Biomaterials 26, 3001, 2005.
11. Barralet, J., Gbureck, U., Habibovic, P., Vorndran, E., Ger-ard, C., and Doillon, C.J. Angiogenesis in calcium phosphate scaffolds by inorganic copper ion release. Tissue Eng Part A 15, 1601, 2009.
12. Gérard, C., Bordeleau, L.J., Barralet, J., and Doillon, C.J. The stimulation of angiogenesis and collagen deposition by copper. Biomaterials 31, 824, 2009.
13. Raju, K.S., Alessandri, G., Ziche, M., and Gullino, P.M. Ceruloplasmin, copper ions, and angiogenesis. J Natl Cancer Inst 69, 1183, 1982.
14. Lane, T.F., Iruela-Arispe, M.L., Johnson, R.S., and Sage, E.H. SPARC is a source of copper-binding peptides that stimulate angiogenesis. J Cell Biol 125, 929, 1994.
15. Sen, C.K., Khanna, S., Venojarvi, M., Trikha, P., Ellison, E.C., Hunt, T.K., and Roy, S. Copper-induced vascular endothelial growth factor expression and wound healing. Am J Physiol Heart Circ Physiol 282, H1821, 2002.
16. Badet, J., Soncin, F., Guitton, J.D., Lamare, O., Cartwright, T., and Barritault, D. Specific binding of angiogenin to calf pulmonary-artery endothelial-cells. Proc Natl Acad Sci U S A 86, 8427, 1989.
17. Feng, W., Ye, F., Xue, W., Zhou, Z., and Kang, Y.J. Copper regulation of hypoxia-inducible factor-1 activity. Mol Phar-macol 75, 174, 2009.
18. Yoshida, D., Ikeda, Y., and Nakazawa, S. Coppper chelation inhibits tumor angiogenesis in the experimental 9L glio-sarcoma model. Neurosurgery 37, 287, 1995.
19. Cookson, M.R., and Shaw, P.J. Oxidative stress and motor neurone disease. Brain Pathol 9, 165, 1999.
20. Hung, Y.H., Bush, A.I., and Cherny, RA. Copper in the brain and Alzheimer's disease. J Biol Inorg Chem 15, 61, 2010.
21. Robinson, N.J., and Winge, D.R. Copper metallochaperones. Annu Rev Biochem 79, 537, 2010.
22. Yu, H.S., Pastor, S.A., Lam, K.W., and Yee, R.W. Ascorbate-enhanced copper toxicity on bovine corneal endothelial-cells in vitro. Curr Eye Res 9, 177, 1990.
23. Starkebaum, G., and Harlan, J.M. Endethelial cell injury due to copper-catalyzed hydrogen-peroxide generation from homocysteine. J Clin Invest 77, 1370, 1986.
24. Hoppe, A., Güldal, N.S., and Boccaccini, A.R. A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32, 2757, 2011.
25. Gorustovich, A.A., Roether, J.A., and Boccaccini, A.R. Effect of bioactive glasses on angiogenesis: a review of in vitro and in vivo evidences. Tissue Eng Part B 16, 199, 2010.
26. Day, R.M. Bioactive glass stimulates the secretion of angio-genic growth factors and angiogenesis in vitro. Tissue Eng 11, 768, 2005.
27. Day, R.M., Maquet, V., Boccaccini, A.R., Jérôme, R., and Forbes, A. In vitro and in vivo analysis of macroporous bio-degradable poly(D,L-lactide-co-glycolide) scaffolds contain-ing bioactive glass. J Biomed Mater Res A 75A, 778, 2005.
28. Leu, A., Stieger, S.M., Dayton, P., Ferrara, K.W., and Leach, J.K. Angiogenic response to bioactive glass promotes bone healing in an irradiated calvarial defect. Tissue Eng Part A 15, 877, 2009.
29. Gerhardt, L.-C., Widdows, K.L., Erol, M.M., Burch, C.W., Sanz-Herrera, J.A., Ochoa, I., Staempfli, R., Roqan, I.S., Gabe, S., Ansari, T., and Boccaccini, A.R. The pro-angiogenic properties of multi-functional bioactive glass composite scaffolds. Biomaterials 32, 4096, 2011.
30. Keshaw, H., Georgiou, G., Blaker, J.J., Forbes, A., Knowles, J.C., and Day, R.M. Assessment of polymer/bioactive glass-composite microporous spheres for tissue regeneration ap-plications. Tissue Eng Part A 15, 1451, 2009.
31. Azevedo, M.M., Jell, G., O'Donnell, M.D., Law, R.V., Hill, R.G., and Stevens, M.M. Synthesis and characterization of hypoxia-mimicking bioactive glasses for skeletal regenera-tion. J Mater Chem 20, 8854, 2010.
32. Erol, M.M., Mourin?o, V., Newby, P., Chatzistavrou, X., Roether, JA., Hupa, L., and Boccaccini, A.R. Copper-releasing, boron-containing bioactive glass-based scaffolds coated with alginate for bone tissue engineering. Acta Bio-mater 8, 792, 2012.
33. Mulligan, A.M., Wilson, M., and Knowles, J.C. The effect of increasing copper content in phosphate-based glasses on biofilms of Streptococcus sanguis. Biomaterials 24,1797, 2003.
34. Abou Neel, E.A., Ahmed, I., Pratten, J., Nazhat, S.N., and Knowles, J.C. Characterisation of antibacterial copper re-leasing degradable phosphate glass fibres. Biomaterials 26, 2247, 2005.
35. Abou Neel, EA., Pickup, D.M., Valappil, S.P., Newport, R.J., and Knowles, J.C. Bioactive functional materials: a perspec-tive on phosphate-based glasses. J Mater Chem 19, 690, 2009.
36. Bunker, B.C., Arnold, G.W., and Wilder, J.A. Phosphate-glass dissolution in aqueous solutions. J Non Cryst Solids 64, 291, 1984.
37. Carmeliet, P. Mechanisms of angiogenesis and arteriogen-esis. Nat Med 6, 389, 2000.
38. Li, S., Xie, H., Li, S., and Kang, Y.J. Copper stimulates growth of human umbilical vein endothelial cells in a vas-cular endothelial growth factor-independent pathway. Exp Biol Med 237, 77, 2012.
39. Gaetke, L.M., and Chow, C.K. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189, 147, 2003.
40. Ueda, J., Takai, M., Shimazu, Y., and Ozawa, T. Reactive oxygen species generated from the reaction of copper(II) complexes with biological reductants cause DNA strand scission. Arch Biochem Biophys 357, 231, 1998.
41. Engleka, K.A., and Maciag, T. Inactivation of human fibro-blast growth factor-1 (FGF-1) activity by interaction with copper ions involves FGF-1 dimer formation induced by copper-catalyzed oxydation. J Biol Chem 267, 11307, 1992.
42. Griffith, C.K., Miller, C., Sainson, R.CA., Calvert, J.W., Jeon, N.L., Hughes, CC.W., and George, S.C. Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng 11, 257, 2005.
43. Karsan, A., Yee, E., Poirier, G.G., Zhou, P., Craig, R., and Harlan, J.M. Fibroblast growth factor-2 inhibits endothelial cell apoptosis by Bcl-2-dependent and independent mecha-nisms. Am J Pathol 151, 1775, 1997.
44. Kwon, Y.G., Min, J.K., Kim, K.M., Lee, D.J., Billiar, T.R., and Kim, Y.M. Sphingosine 1-phosphate protects human um-bilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J Biol Chem 276, 10627, 2001.
45. Tardito, S., Bassanetti, I., Bignardi, C., Elviri, L., Tegoni, M., Mucchino, C., Bussolati, O., Franchi-Gazzola, R., and Marchio, L. Copper binding agents acting as copper iono-phores lead to caspase inhibition and paraptotic cell death in human cancer cells. J Am Chem Soc 133, 6235, 2011.
46. Abiaka, C., Olusi, S., and Al-Awadhi, A. Reference ranges of copper and zinc and the prevalence of their deficiencies in an Arab population aged 15-80 years. Biol Trace Elem Res 91, 33, 2003.
47. Sanchez, C., Lopez-Jurado, M., Aranda, P., and Llopis, J. Plasma levels of copper, manganese and selenium in an adult population in southern Spain: influence of age, obesity and lifestyle factors. Sci Total Environ 408, 1014, 2010.
48. Aina, V., Malavasi, G., Pla, A.F., Munaron, L., and Morterra, C. Zinc-containing bioactive glasses: surface reactivity and behaviour towards endothelial cells. Acta Biomater 5, 1211, 2009.
49. Abou Neel, E.A., Ahmed, I., Blaker, J.J., Bismarck, A., Boc-caccini, A.R., Lewis, M.P., Nazhat, SN., and Knowles, J.C Effect of iron on the surface, degradation and ion release properties of phosphate-based glass fibres. Acta Biomater 1, 553, 2005.