Collagen/silica nanocomposites and hybrids for bone tissue engineering

Nanotechnology Reviews

Volumn 2, Issue 4, 2013, Pages 427-447

  Sarker, Bapi ^a   Lyer, Stefan ^b   Arkudas, Andreas ^b   Boccaccini, Aldo R ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Bioactivity; Collagen; Nanocomposite; Osteogenesis; Silica

Indexed keywords

BIOACTIVITY; BIOMECHANICS; BONE; COLLAGEN; NANOCOMPOSITES; SELF ASSEMBLY; SILICA; TISSUE;

BIOACTIVE MATERIAL; BONE REGENERATION; BONE TISSUE ENGINEERING; COLLAGEN SELF ASSEMBLIES; MECHANICAL LOADS; ORGANIC MATRIX; OSTEOGENESIS; SILICA PRECURSORS;

TISSUE ENGINEERING;

EID: 84921869845     PISSN: 21919089     EISSN: 21919097     Source Type: Journal    
DOI: 10.1515/ntrev-2013-0012     Document Type: Review

References (103)

1. Hench LL. Bioactive materials: the potential for tissue regeneration. J. Biomed. Mater. Res. 1998, 41, 511-518.
2. Gkioni K, Leeuwenburgh SC, Douglas TE, Mikos AG, Jansen JA. Mineralization of hydrogels for bone regeneration. Tissue Eng., Part B 2010, 16, 577-585.
3. Cao W, Hench LL. Bioactive materials. Ceram. Int. 1996, 22, 493-507.
4. Rea SM, Best SM, Bonfield W. Bioactivity of ceramic-polymer composites with varied composition and surface topography. J. Mater. Sci.: Mater. Med. 2004, 15, 997-1005.
5. Kamitakahara M, Ohtsuki C, Miyazaki T. Review paper: behavior of ceramic biomaterials derived from tricalcium phosphate in physiological condition. J. Biomater. Appl. 2008, 23, 197-212.
6. Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006, 27, 3413-3431.
7. Neumann M, Epple M. Composites of calcium phosphate and polymers as bone substitution materials. Eur. J. Trauma 2006, 32, 125-131.
8. Ara M, Watanabe M, Imai Y. Effect of blending calcium compounds on hydrolytic degradation of poly( dl-lactic acid-co-glycolic acid). Biomaterials. 2002, 23, 2479-2483.
9. Koo JH. Polymer nanocomposites: processing, characterization, and applications. McGraw-Hill: New York, USA, 2006.
10. Boccaccini AR, Erol M, Stark WJ, Mohn D, Hong Z, Mano JF. Polymer/bioactive glass nanocomposites for biomedical applications: a review. Compos. Sci. Technol. 2010, 70, 1764-1776.
11. Marelli B, Ghezzi CE, Barralet JE, Boccaccini AR, Nazhat SN. Three-dimensional mineralization of dense nanofibrillar collagen-bioglass hybrid scaffolds. Biomacromolecules 2010, 11, 1470-1479.
12. Yunos DM, Bretcanu O, Boccaccini AR. Polymer-bioceramic composites for tissue engineering scaffolds. J. Mater. Sci. 2008, 43, 4433-4442.
13. Heinemann S, Heinemann C, Ehrlich H, Meyer M, Baltzer H, Worch H, Hanke T. A novel biomimetic hybrid material made of silicified collagen: perspectives for bone replacement. Adv. Eng. Mater. 2007, 9, 1061-1068.
14. Eglin D, Maalheem S, Livage J, Coradin T. In vitro apatite forming ability of type I collagen hydrogels containing bioactive glass and silica sol-gel particles. J. Mater. Sci.: Mater. Med. 2006, 17, 161-167.
15. Yan S, Yin J, Cui L, Yang Y, Chen X. Apatite-forming ability of bioactive poly(l-lactic acid)/grafted silica nanocomposites in simulated body fluid. Colloids Surf., B 2011, 86, 218-224.
16. Lai W, Garino J, Ducheyne P. Silicon excretion from bioactive glass implanted in rabbit bone. Biomaterials 2002, 23, 213-217.
17. Heinemann S, Ehrlich H, Knieb C, Hanke T. Biomimetically inspired hybrid materials based on silicified collagen. Int. J. Mater. Res. 2007, 98, 603-608.
18. Heinemann S, Heinemann C, Bernhardt R, Reinstorf A, Nies B, Meyer M, Worch H, Hanke T. Bioactive silica-collagen composite xerogels modified by calcium phosphate phases with adjustable mechanical properties for bone replacement. Acta Biomater. 2009, 5, 1979-1990.
19. Heinemann S, Heinemann C, J a ger M, Neunzehn J, Wiesmann HP, Hanke T. Effect of silica and hydroxyapatite mineralization on the mechanical properties and the biocompatibility of nanocomposite collagen scaffolds. Appl. Mater. Interfaces 2011, 3, 4323-4331.
20. Si X, Wang Y, Ren L, Zhao N, Gong Y, Wang D-A. Novel mesoporous silica-based antibiotic releasing scaffold for bone repair. Acta Biomater. 2009, 5, 1697-1707.
21. Desimone MF, H e lary C, Rietveld IB, Bataille I, Mosser G, Giraud-Guille M-M, Livage J, Coradin T. Silica-collagen bionanocomposites as three-dimensional scaffolds for fibroblast immobilization. Acta Biomater. 2010, 6, 3998-4004.
22. Ghanaati SM, Thimm BW, Unger RE, Orth C, Kohler T, Barbeck M, M u ller R, Kirkpatrick CJ. Collagen-embedded hydroxylapatite-â-tricalcium phosphate-silicon dioxide bone substitute granules assist rapid vascularization and promote cell growth. Biomed. Mater. 2010, 5, 25004.
23. Eglin D, Shafran KL, Livage J, Coradin T, Perry CC. Comparative study of the influence of several silica precursors on collagen self-assembly and of collagen on ' Si ' speciation and condensation. J. Mater. Chem. 2006, 16, 4220-4230.
24. Alt V, Kogelmaier DV, Lips KS, Witt V, Pacholke S, Heiss C, Kampschulte M, Heinemann S, Hanke T, Schnettler R, Langheinrich AC. Assessment of angiogenesis in osseointegration of a silica-collagen biomaterial using 3D-nano-CT. Acta Biomater. 2011, 7, 3773-3779.
25. Boccaccini A, Kneser U, Arkudas A. Scaffolds for vascularized bone regeneration: advances and challenges. Expert Rev. Med. Devices 2012, 9, 457-460.
26. Vallet-Regi M, Colilla M, Gonz alez B. Medical applications of organic-inorganic hybrid materials within the field of silica-based bioceramics. Chem. Soc. Rev. 2011, 40, 596-607.
27. Luo Z, Cai K, Hu Y, Zhao L, Liu P, Duan L, Yang W. Mesoporous silica nanoparticles end-capped with collagen: redoxresponsive nanoreservoirs for targeted drug delivery. Angew. Chem. Int. Ed. 2011, 50, 640-643.
28. Heinemann S, Coradin T, Worch H, Wiesmann HP, Hanke T. Possibilities and limitations of preparing silica/collagen/hydroxyapatite composite xerogels as load-bearing biomaterials. Compos. Sci. Technol. 2011, 71, 1873-1880.
29. Lee CH, Singla A, Lee Y. Biomedical applications of collagen. Int. J. Pharm. 2001, 221, 1-22.
30. Lee E-J, Jun S-H, Kim H-E, Koh Y-H. Collagen-silica xerogel nanohybrid membrane for guided bone regeneration. J. Biomed. Mater. Res., Part A 2012, 100, 841-847.
31. Behring J, Junker R, Walboomers XF, Chessnut C, Jansen J. Toward guided tissue and bone regeneration: morphology, attachment, proliferation, and migration of cells cultured on collagen barrier membranes. A systematic review. Odontology 2008, 96, 1-11.
32. Bunyaratavej P, Wang H-L. Collagen membrane: a review. J. Periodontol. 2001, 72, 215-229.
33. Lin A, Goh M. Investigating the ultrastructure of fibrous long spacing collagen by parallel atomic force and transmission electron microscopy. Proteins 2002, 49, 378-384.
34. Stenzel K, Miyata T, Rubin A. Collagen as a biomaterial. Annu. Rev. Biophys. Bioeng. 1974, 3, 231-453.
35. Miyata T, Taira T, Noishiki Y. Collagen engineering for biomaterial use. Clin. Mater. 1992, 9, 139-148.
36. Giraud-Guille M, H e lary C, Vigier S, Nassif N. Dense fibrillar collagen matrices for tissue repair. Soft Matter 2010, 6, 4963-4967.
37. Wahl D, Czernuszka J. Collagen-hydroxyapatite composites for hard tissue repair. Eur. Cells Mater. 2006, 11, 43-56.
38. Lickorish D, Ramshaw J, Werkmeister J, Glattauer V, Howlett C. Collagen-hydroxyapatite composite prepared by biomimetic process. J. Biomed. Mater. Res., Part A 2004, 68, 19-27.
39. Song J, Kim H, Kim H. Collagen-apatite nanocomposite membranes for guided bone regeneration. J. Biomed. Mater. Res., Part B 2007, 83, 248-257.
40. Kikuchi M, Itoh S, Ichinose S, Shinomiya K, Tanaka J. Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 2011, 22, 1705-1711.
41. Kikuchi M, Ikoma T, Itoh S, Matsumoto HN, Koyama Y, Takakuda K, Shinomiya K, Tanaka J. Biomimetic synthesis of bone-like nanocomposites using the self-organization mechanism of hydroxyapatite and collagen. Compos. Sci. Technol. 2004, 64, 819-825.
42. Oprita E, Moldovan L, Craciunescu O, Buzgariu W, Tardei C, Zarnescu O. A bioactive collagen-â tricalcium phosphate scaffold for tissue engineering. Cent. Eur. J. Biol. 2006, 1, 61-72.
43. Kim HW, Song JH, Kim HE. Bioactive glass nanofiber-collagen nanocomposite as a novel bone regeneration matrix. J. Biomed. Mater. Res., Part A 2006, 79, 698-705.
44. Marelli B, Ghezzi CE, Mohn D, Stark WJ, Barralet JE, Boccaccini AR, Nazhat SN. Accelerated mineralization of dense collagennano bioactive glass hybrid gels increases scaffold stiffness and regulates osteoblastic function. Biomaterials. 2011, 32, 8915-8926.
45. Thimm BW, Unger RE, Neumann H-G, Kirkpatrick CJ. Biocompatibility studies of endothelial cells on a novel calcium phosphate/SiO 2-xerogel composite for bone tissue engineering. Biomed. Mater. 2008, 3, 15007.
46. Lee E-J, Teng S-H, Jang T-S, Peng Wang S-WY, Kim H-E, Koh Y-H. Nanostructured poly( å-caprolactone)-silica xerogel fibrous membrane for guided bone regeneration. Acta Biomater. 2010, 6, 3557-3565.
47. Li P, Ye X, Kangasniemi I, de Blieck-Hogervorst JM, Klein CP, de Groot K. In vivo calcium phosphate formation induced by sol-gel-prepared silica. J. Biomed. Mater. Res. Part A 1995, 29, 325-328.
48. Hamadouche M, Meunier A, Greenspan DC, Blanchat C, Zhong JP, Torre GPL, Sedel L. Long-term in vivo bioactivity and degradability of bulk sol-gel bioactive glasses. J. Biomed. Mater. Res., Part A 2001, 54, 560-566.
49. Balas F, Perez-Pariente J, Vallet-Regi M. In vitro bioactivity of silicon-substituted hydroxyapatites. J. Biomed. Mater. Res. Part A 2003, 66A, 364-375.
50. Hoppe A, G u ldal NS, Boccaccini AR. A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 2011, 32, 2757-2774.
51. Coradin T, Boissiere M, Livage J. Sol-gel chemistry in medicinal science. Curr. Med. Chem. 2006, 13, 99-108.
52. Heinemann S, Heinemann C, Wenisch S, Alt V, Worch H, Hanke T. Calcium phosphate phases integrated in silica/collagen nanocomposite xerogels enhance the bioactivity and ultimately manipulate the osteoblast/osteoclast ratio in a human co-culture model. Acta Biomater. 2013, 9, 4878-4888.
53. Brasack I, B o ttcher H, Hempel U. Biocompatibility of modified silica-protein composite layers. J. Sol-Gel Sci. Technol. 2000, 19, 479-482.
54. Ehrlich H, Heinemann S, Heinemann C, Simon P, Bazhenov VV, Shapkin NP, Born R, Tabachnick KR, Hanke T, Worch H. Nanostructural organization of naturally occurring composites-Part I: silica-collagen-based biocomposites. J. Nanomater. 2008, 2008, Article ID 623838.
55. Desimone MF, H e lary C, Quignard S, Rietveld IB, Bataille I, Copello GJ, Mosser G, Giraud-Guille M-M, Livage J, Meddahi-Pell e A, Coradin T. In vitro studies and preliminary in vivo evaluation of silicified concentrated collagen hydrogels. Appl. Mater. Interfaces. 2011, 3, 3831-3838.
56. Patwardhan SV, Clarson SJ, Perry CC. On the role(s) of additives in bioinspired silicification. Chem. Commun. 2005, 7, 1113-1121.
57. Coradin T, Lopez PJ. Biogenic silica patterning: simple chemistry or subtle biology? ChemBioChem. 2003, 4, 251-259.
58. Eglin D, Coradin T, Guille M-M G, Helary C, Livage J. Collagensilica hybrid materials: sodium silicate and sodium chloride effects on type I collagen fibrillogenesis. Biomed. Mater. Eng. 2005, 15, 43-50.
59. Eglin D, Mosser G, Giraud-Guille M-M, Livage J, Coradin T. Type I collagen, a versatile liquid crystal biological template for silica structuration from nano-to microscopic scales. Soft Matter 2005, 1, 129-131.
60. Li P, Nakanishi K, Kokubo T, de Groot K. Induction and morphology of hydroxyapatite, precipitated from metastable simulated body fluids on sol-gel prepared silica. Biomaterials 1993, 14, 963-968.
61. Peltola T, Jokinen M, Rahiala H, Levanen E, Rosenholm JB, Kangasniemi I. Calcium phosphate formation on porous sol-gel-derived SiO2 and CaO-P 2 O 5-SiO 2 substrates in vitro. J. Biomed. Mater. Res. 1999, 44, 12-21.
62. St o ber W, Fink A. Controlled growth of monodisperse silica spheres in the micron size range. J. Colloid Interface Sci. 1968, 26, 62-69.
63. Niu L-N, Jiao K, Qi Y-P, Nikonov S, Yiu CKY, Arola DD, Gong S-Q, El-Marakby A, Carrilho MRO, Hamrick MW, Hargreaves KM, Diogenes A, Chen J-H, Pashley DH, Tay FR. Intrafibrillar silicification of collagen scaffolds for sustained release of stem cell homing chemokine in hard tissue regeneration. FASEB J. 2012, 26, 4517-4529.
64. Hench LL. Bioceramics: from concept to clinic. J. Am. Ceram. Soc. 1991, 74, 1487-1510.
65. Shirtliff VJ, Hench LL. Bioactive materials for tissue engineering, regeneration and repair. J. Mater. Sci. 2003, 38, 4697-4707.
66. Ehrlich H, Worch H. Collagen, a huge matrix in glass-sponge flexible spicules of the meter-long Hyalonema sieboldi. In Handbook of Biomineralization. Vol.1. The Biology of Biominerals Structure Formation, B a uerlein, E, Ed., Wiley VCH: Weinheim, Germany, 2007.
67. Carturan G, Toso RD, Boninsegna S, Monte RD. Encapsulation of functional cells by sol-gel silica: actual progress and perspectives for cell therapy. J. Mater. Chem. 2004, 14, 2087-2098.
68. Desimone MF, H e lary C, Mosser G, Giraud-Guille M-M, Livage J, Coradin T. Fibroblast encapsulation in hybrid silica/collagen hydrogels. J. Mater. Chem. 2010, 20, 666-668.
69. Bell E, Ivarsson B, Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA 1979, 76, 1274-1278.
70. Yano S, Iwata K, Kurita K. Physical properties and structure of organic-inorganic hybrid materials produced by sol-gel process. Mater. Sci. Eng., C 1998, 6, 75-90.
71. Avnir D, Coradin T, Lev O, Livage J. Recent bio-applications of sol-gel materials. J. Mater. Chem. 2006, 16, 1013-1030.
72. Zhang Y, Hu L, Yu D, Gao C. Influence of silica particle internalization on adhesion and migration of human dermal fibroblasts. Biomaterials 2010, 31, 8465-8474.
73. Ye X, Zhou Y, Sun Y, Chen J, Wang Z. Structure and infrared emissivity of collagen/SiO2 composite. Appl. Surf. Sci. 2008, 254, 5975-5980.
74. Niu L-N, Jiao K, Qi Y-P, Yiu CKY, Ryou H, Arola DD, Chen J-H, Breschi L, Pashley DH, Tay FR. Infiltration of silica inside fibrillar collagen. Angew. Chem. Int. Ed. Engl. 2011, 50, 11688-11691.
75. Brinker CJ, Scherer GW. Sol-Gel Science: The Physics and Chemistry of Sol-Gel Processing. Academic: Boston, 1990.
76. Zhao Y, Trewyn BG, Slowing II, Lin VS-Y. Mesoporous Silica nanoparticle-based double drug delivery system for glucoseresponsive controlled release of insulin and cyclic AMP. J. Am. Chem. Soc. 2009, 131, 8398-8400.
77. Cai KY, Hu Y, Luo Z, Kong T, Lai M, Sui XJ, Wang YL, Yang L, Deng LH. Cell-specific gene transfection from a gene-functionalized poly( d,l-lactic acid) substrate fabricated by the layer-by-layer assembly technique. Angew. Chem. Int. Ed. 2008, 47, 7479-7481.
78. Hu Y, Cai K, Luo Z, Jandt KD. Layer-by-layer assembly of â-estradiol loaded mesoporous silica nanoparticles on titanium substrates and its implication for bone homeostasis. Adv. Mater. 2010, 22, 4146-4150.
79. Porter AE, Patel N, Skepper JN, Best SM, Bonfield W. Effect of sintered silicate-substituted hydroxyapatite on remodelling processes at the bone-implant interface. Biomaterials 2004, 25, 3303-3314.
80. Li P, Ohtsuki C, Kokubo T, Nakanishi K, Soga N, de Groot K. The role of hydrated silica, titania, and alumina in inducing apatite on implants. J. Biomed. Mater. Res., Part A 1994, 28, 7-15.
81. Li P, Ohtsuki C, Kokubo T, Nakanishi K, Soga N, Nakamura T, Yamamuro T. Effects of ions in aqueous media on hydroxyapatite induction by silica gel and its relevance to bioactivity of bioactive glasses and glass-ceramics J. Appl. Biomater. 1993, 4, 221-229.
82. Shur I, Zilberman M, Benayahu D, Einav S. Adhesion molecule expression by osteogenic cells cultured on various biodegradable scaffolds. J. Biomed. Res., Part A 2005, 75, 870-876.
83. Li J, Yun H, Gong Y, Zhao N, Zhang X. Effects of surface modification of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) (PHBHHx) on physicochemical properties and on interactions with MC3T3-E1 cells. J. Biomed. Mater. Res., Part A 2005, 75, 985-998.
84. Berry CC, Campbell G, Spadiccino A, Robertson M, Curtis ASG. The influence of microscale topography on fibroblast attachment and motility. Biomaterials 2004, 25, 5781-5788.
85. Anselme K. Osteoblast adhesion on biomaterials. Biomaterials 2000, 21, 667-681.
86. Andrade AL, Valerio P, de Goes AM, de F a tima Leite M, Domingues RZ. Influence of recovering collagen with bioactive glass on osteoblast behavior. J. Biomed. Mater. Res., Part B 2007, 83, 481-489.
87. Heinemann C, Heinemann S, Worch H, Hanke T. Development of an osteoblast/osteoclast co-culture derived by human bone marrow stromal cells and human monocytes for biomaterials testing. Eur. Cells Mater. 2011, 21, 80-93.
88. Vall es G, Gil-Garay E, Munuera L, Vilaboa N. Modulation of the cross-talk between macrophages and osteoblasts by titaniumbased particles. Biomaterials 2008, 29, 2326-2335.
89. Zhou H, Wei J, Wu X, Shi J, Liu C, Jia J, Dai C, Gan Q. The bio-functional role of calcium in mesoporous silica xerogels on the responses of osteoblasts in vitro. J. Mater. Sci: Mater. Med. 2010, 21, 2175-2185.
90. Knabe C, Driessens FCM, Planell JA, Gildenhaar R, Berger G, Reif D, Fitzner R, Radlanski RJ, Gross U. Evaluation of calcium phosphates and experimental calcium phosphate bone cements using osteogenic cultures. J. Biomed. Mater. Res. 2000, 52, 498-508.
91. Hempel U, Reinstorf A, Poppe M, Fischer U, Gelinsky M, Pompe W, Wenzel KW. Proliferation and differentiation of osteoblasts on Biocement D modified with collagen type I and citric acid. J. Biomed. Mater. Res., Part B 2004, 71, 130-143.
92. Romanello M, D ' Andrea P. Dual mechanism of intercellular communication in hobit osteoblastic cells: a role for gap-junctional hemichannels. J. Bone Miner. Res. 2001, 16, 1465-1476.
93. Xu C, Su P, Chen X, Meng Y, Yu W, Xiang AP, Wang Y. Biocompatibility and osteogenesis of biomimetic bioglass-collagen-phosphatidylserine composite scaffolds for bone tissue engineering. Biomaterials 2011, 32, 1051-1058.
94. Wang MC, Pins GD, Silver FH. Collagen fibres with improved strength for the repair of soft tissue injuries. Biomaterials 1994, 15, 507-512.
95. Hum J, Boccaccini AR. Bioactive glasses as carriers for bioactive molecules and therapeutic drugs: a review. J. Mater. Sci: Mater. Med. 2012, 23, 2317-2333.
96. Vallet-Reg i M. Ordered mesoporous materials in the context of drug delivery systems and bone tissue engineering. Chem.-Eur. J. 2006, 12, 5934-5943.
97. Vallet-Regi M. Nanostructured mesoporous silica matrices in nanomedicine. J. Intern. Med. 2010, 267, 22-43.
98. Vallet-Reg i M, Balas F, Arcos D. Mesoporous materials for drug delivery. Angew. Chem. Int. Ed. 2007, 46, 7548-7558.
99. Vallet-Reg i M, Balas F, Colilla M, Manzano M. Bone-regenerative bioceramic implants with drug and protein controlled delivery capability. Progr. Solid State Chem. 2008, 36, 163-191.
100. Tu H-L, Lin Y-S, Lin H-Y, Hung Y, Lo L-W, Chen Y-F, Mou C-Y. In vitro studies of functionalized mesoporous silica nanoparticles for photodynamic therapy. Adv. Mater. 2009, 21, 172-177.
101. Slowing II, Vivero-Escoto JL, Wu C-W, Lin VS-Y. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv. Drug Delivery Rev. 2008, 60, 1278-1288.
102. Zhao W, Gu J, Zhang L, Chen H, Shi J. Fabrication of uniform magnetic nanocomposite spheres with a magnetic core/mesoporous silica shell structure. J. Am. Chem. Soc. 2005, 127, 8916-8917.
103. Derby B. Printing and prototyping of tissues and scaffolds. Science 2012, 338, 921-926.