Development of a morphogenetically active scaffold for three-dimensional growth of bone cells: Biosilica-alginate hydrogel for SaOS-2 cell cultivation

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 11, 2015, Pages E39-E50

  Müller, Werner E G ^a   Schröder, Heinz C ^a   Feng, Qingling ^b   Schlossmacher, Ute ^a   Link, Thorben ^a   Wang, Xiaohong ^a,c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b TSINGHUA UNIVERSITY   (China)

^c INSTITUTE OF MINERAL RESOURCES   (China)

Author keywords

Alginate; Biosilica; BMP 2; Carbonic anhydrase 1; Collagen 1; Hydrogel; SaOS 2 cells; Silica

Indexed keywords

ALGINATE; BIOCOMPATIBILITY; BONE; CARBONIC ANHYDRASE; COLLAGEN; CYTOLOGY; GENE EXPRESSION; HYDROGELS; HYDROXYAPATITE; SCAFFOLDS (BIOLOGY); SIGNAL ENCODING; SILICATES; SOL-GEL PROCESS; SOL-GELS;

ALGINATE HYDROGELS; BIOSILICA; BONE CELLS; BONE MORPHOGENETIC PROTEIN-2; CARBONIC ANHYDRASE 1; COLLAGEN 1; GENES ENCODING; NA-ALGINATE; SAOS-2 CELLS; THREE-DIMENSIONAL GROWTH;

SILICA;

BIOSILICA ALGINATE HYDROGEL; BONE MORPHOGENETIC PROTEIN 2; CARBONATE DEHYDRATASE I; COLLAGEN TYPE 1; HYDROXYAPATITE; POLYMER; UNCLASSIFIED DRUG; ALGINIC ACID; BIOMATERIAL; BMP2 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; COLLAGEN; CYTOKINE; HYDROGEL; RECOMBINANT PROTEIN; SILICATE; SILICON DIOXIDE;

ARTICLE; BIOPRINTING; BMP 2 GENE; BONE CELL; CARBONIC ANHYDRASE 1 GENE; CELL COUNT; CELL PROLIFERATION; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; COLLAGEN 1 GENE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TISSUE SCAFFOLD; BONE; BONE DEVELOPMENT; CELL SURVIVAL; CHEMISTRY; HYDROGEL; METABOLISM; OSTEOBLAST; PHYSIOLOGY; TUMOR CELL LINE;

ALGINATES; BIOCOMPATIBLE MATERIALS; BIOPRINTING; BONE AND BONES; BONE MORPHOGENETIC PROTEIN 2; CARBONIC ANHYDRASES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN; CYTOKINES; DURAPATITE; HUMANS; HYDROGELS; OSTEOBLASTS; OSTEOGENESIS; POLYMERS; RECOMBINANT PROTEINS; SILICATES; SILICON DIOXIDE; TISSUE SCAFFOLDS;

EID: 84946498089     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1745     Document Type: Article

References (84)

1. Aebischer P, Buchser E, Joseph J, et al. 1994; Transplantation in humans of encapsulated xenogeneic cells without immunosuppression: a preliminary report. Transplantation 58: 1275-1277.
2. Andersen T, Strand BL, Formo K, et al. 2012; Alginates as biomaterials in tissue engineering. Carbohydr Chem 37: 227-258.
3. Anderson HC, Hsu HHT, Raval P, et al. 1998; Bone-inducing agent in Saos-2 cell extracts and secretions. Cells Mater 8: 89-98.
4. Badami AS, Kreke MR, Thompson MS, et al. 2006; Effect of fiber diameter on spreading, proliferation, and differentiation of osteoblastic cells on electrospun poly(lactic acid) substrates. Biomaterials 27: 596-606.
5. Belton DJ, Deschaume O, Perry CC. 2012; An overview of the fundamentals of the chemistry of silica with relevance to biosilicification and technological advances. FEBS J 279: 1710-1720.
6. Biskobing DM, Fan D, Fan X, et al. 1997; Induction of carbonic anhydrase II expression in osteoclast progenitors requires physical contact with stromal cells. Endocrinology 138: 4852-4857.
7. Blackwood KA, Bock N, Dargaville TR, et al. 2012; Scaffolds for growth factor delivery as applied to bone tissue engineering. Intern J Polymer Sci DOI:10.1155/2012/174942.
8. Boes L, Boesebeck H, Ulrich SD, et al. 2009; Collagen-based osteoinductive bone void filler for mistreatment in osteochondritis dissecans and osteonecrosis. J Bone Joint Surg Br 91B(supp II): 332.
9. de Camargo Bittencourt RA, Hamilton RP, FelisbinoI SL, et al. 2009; Chondrocyte cultures in tridimensional scaffold: alginate hydrogel. Acta Ortop Bras 17: 242-246.
10. Cargill B, Godart P, Lavrov N, et al. 2011; Using carbonic anhydrase and silica nanomaterials in carbon dioxide mitigation. Group Research Study at Rutgers University; http://nickphillips2011.com/resources/2010GSET-NanoPaper.pdf
11. Carlisle EM. 1972; Silicon: an essential element for the chick. Science 178: 619-621.
12. Carlisle EM. 1986; Silicon as an essential trace element in animal nutrition. In Silicon Biochemistry, Evered D, O'Connor M (eds). CIBA Foundation Symposium No. 121. Wiley: Chichester; 123-136.
13. Chang X, Zheng Y, Yang Q, et al. 2012; Carbonic anhydrase I is involved in the process of bone formation and is susceptible to ankylosing spondylitis. Arthritis Res Ther 27 14(4): R176; DOI: 10.1186/ar3929.
14. Chen A, Haddad D, Wang R. 2009; Analysis of Chitosan-Alginate Bone Scaffolds. Technical Report, Rutgers University, New Jersey Governor's School of Engineering & Technology.
15. Cheng SL, Yang JW, Rifas L, et al. 1994; Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 134: 277-286.
16. Curnow P, Bassette P, Kisailus D, et al. 2005; Enzymatic synthesis of layered titanium phosphates at low temperature and neutral pH by cell-surface display of silicatein-α. J Am Chem Soc 127: 15749-15755.
17. Duan B, Hockaday LA, Kang KH, et al. 2013; 3D Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res A 101: 1255-1264.
18. Dumitrescu AL. 2011; Bone grafts and bone graft substitutes in periodontal therapy. In Chemicals in Surgical Periodontal Therapy. Springer: Berlin; 73-144.
19. Epple M. 2007; Biomimetic bone substitution materials. In Biomineralisation: Medical and Clinical Aspects, Epple M, Baeuerlein E (eds). Wiley-VCH: Weinheim; 81-95.
20. Fogh J, Fogh JM, Orfeo T. 1977; One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst 59: 221-226.
21. Freshney RI. 2000; Specialized cells. In Culture of Animal Cells: A Manual of Basic Technique, 4th edn. Wiley-Liss: New York; 367-370.
22. Goren A, Dahan N, Goren E, et al. 2010; Encapsulated human mesenchymal stem cells: a unique hypoimmunogenic platform for long-term cellular therapy. FASEB J 24: 22-31.
23. Grayson WL, Chao PH, Marolt D, et al. 2008; Engineering custom-designed osteochondral tissue grafts. Trends Biotechnol 26: 181-189.
24. Han P, Wu C, Xiao Y. 2013; The effect of silicate ions on proliferation, osteogenic differentiation and cell signalling pathways (WNT and SHH) of bone marrow stromal cells. Biomater Sci 1: 379-392.
25. Hassell T, Gleave S, Butler M. 1991; Growth inhibition in animal cell culture. The effect of lactate and ammonia. Appl Biochem Biotechnol 30: 29-41.
26. Haug A, Smidsrod O. 1970; Selectivity of some anionic polymers for divalent metal ions. Acta Chem Scand 24: 843-854.
27. Hausser HJ, Brenner RE. 2005; Phenotypic instability of SaOS-2 cells in long-term culture. Biochem Biophys Res Commun 333: 216-222.
28. Huang Z, Tian J, Yu B, et al. 2009; A bone-like nano-hydroxyapatite-collagen loaded injectable scaffold. Biomed Mater 4: 055005.
29. Hutmacher DW, Sittinger M, Risbud MV. 2004; Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends Biotechnol 22: 354-362.
30. Jugdaohsingh R, Anderson SH, Tucker KL, et al. 2002; Dietary silicon intake and absorption. Am J Clin Nutr 75: 887-893.
31. Jugdaohsingh R 2007; Silicon and bone health. J Nutr Health Aging 11: 99-110.
32. 2 in Azospirillum brasilense Sp7. BMC Microbiol 10: 184; DOI: 10.1186/1471-2180-10-184.
33. Khalil S, Sun W. 2009; Bioprinting endothelial cells with alginate for 3D tissue constructs. J Biomech Eng 131: 111002; DOI: org/10.1115/1.3128729.
34. Kubantseva N, Hartel RW, Swearingen PA. 2004; Factors affecting solubility of calcium lactate in aqueous solutions. J Dairy Sci 87: 863-867.
35. Kuo CK, Ma PX. 2001; Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: part 1. Structure, gelation rate and mechanical properties. Biomaterials 22: 511-521.
36. Kwon YJ, Peng CA. 2002; Calcium-alginate gel bead crosslinked with gelatin as microcarrier for anchorage-dependent cell culture. Biotechniques 33: 212-214.
37. Langenbach F, Berr K, Naujoks C, et al. 2011; Generation and differentiation of microtissues from multipotent precursor cells for use in tissue engineering. Nat Protoc 6: 1726-1735.
38. Lieberman JR, Daluiski A, Stevenson S, et al. 1999; The effect of regional gene therapy with bone morphogenetic protein-2-producing bone-marrow cells on the repair of segmental femoral defects in rats. J Bone Joint Surg Am 81: 905-917.
39. Lin HY, Yeh CT. 2010; Alginate-crosslinked chitosan scaffolds as pentoxifylline delivery carriers. J Mater Sci Mater Med 21: 1611-1620.
40. Link T, Wang XH, Schlossmacher U, et al. 2013; An approach to a biomimetic bone scaffold: Increased expression of BMP-2 and of osteoprotegerin in SaOS-2 cells grown onto silica-biologized 3D printed scaffolds. RSC Adv (in press).
41. Martinsen A, Skjåk-Bræk G, Smidsrød O. 1989; Alginate as immobilization material: I. Correlation between chemical and physical properties of alginate gel beads. Biotechnol Bioeng 33: 79-89.
42. Milligan AJ, Morel FMM. 2002; A proton buffering role for silica in diatoms. Science 297: 1848-1850.
43. Mironov V, Boland T, Trusk T, et al. 2003; Organ printing: computer-aided jet-based 3D tissue engineering. Trends Biotechnol 21: 157-161.
44. Morse DE. 1999; Silicon biotechnology: harnessing biological silica production to construct new materials. Trends Biotechnol 17: 230-232.
45. Müller WEG, Engel S, Wang XH, et al. 2008; Bioencapsulation of living bacteria (Escherichia coli) with poly(silicate) after transformation with silicatein-α gene. Biomaterials 29: 771-779.
46. Müller WEG, Schröder HC, Krasko A. 2004; US Patent No. US20070218044. Decomposition and modification of silicate and silicone by silicase and use of the reversible enzyme; 15 April 2004.
47. Müller WEG, Wang XH, Cui FZ, et al. 2009; Sponge spicules as blueprints for the biofabrication of inorganic-organic composites and biomaterials. Appl Microbiol Biotechnol 83: 397-413.
48. Müller WEG, Wang XH, Schröder HC, et al. 2010; A cryptochrome-based photosensory system in the siliceous sponge Suberites domuncula (Demospongiae). FEBS J 277: 1182-1201.
49. Nandi SK, Roy S, Mukherjee P, et al. 2010; Orthopaedic applications of bone graft and graft substitutes: a review. Indian J Med Res 132: 15-30.
50. Nickel J, Dreyer MK, Kirsch T, et al. 2001; The crystal structure of the BMP-2-BMPR-IA complex and the generation of BMP-2 antagonists. J Bone Joint Surg 83: S7-14.
51. Niyibizi C, Eyre DR. 1994; Structural characteristics of cross-linking sites in type V collagen of bone chain specificities and heterotypic links to type I collagen. Eur J Biochem 224: 943-950.
52. Novikova LN, Mosahebi A, Wiberg M, et al. 2006; Alginate hydrogel and matrigel as potential cell carriers for neurotransplantation. J Biomed Mater Res A 77: 242-252.
53. Oliveira JM, Rodrigues MT, Silva SS, et al. 2006; Novel hydroxyapatite-chitosan bilayered scaffold for osteochondral tissue-engineering applications: scaffold design and its performance when seeded with goat bone marrow stromal cells. Biomaterials 27: 6123-6137.
54. Pfaffl MW. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2002-2007.
55. Pozzolini M, Valisano L, Cerrano C, et al. 2010; Influence of rocky substrata on three-dimensional sponge cells model development. In Vitro Cell Dev Biol Animal 46: 140-147.
56. Qin L, Han T, Zhang Q, et al. 2008; Antiosteoporotic chemical constituents from Er-Xian Decoction, a traditional Chinese herbal formula. J Ethnopharmacol 118: 271-279.
57. Rao NN, Gómez-Garcia MR, Kornberg A. 2009; Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78: 605-647.
58. Sachs L. 1984; Angewandte Statistik. Springer: Berlin; 242.
59. Schlossmacher U, Wiens M, Schröder HC, et al. 2011; Silintaphin-1: interaction with silicatein during structure guiding biosilica formation. FEBS J 278: 1145-1155.
60. Schreiber RE, Blease K, Ambrosio A, et al. 2005; Bone induction by AdBMP-2/collagen implants. J Bone Joint Surg Am 87: 1059-1068.
61. Schröder HC, Krasko A, Le Pennec G, et al. 2003; Silicase, an enzyme which degrades biogenous amorphous silica: contribution to the metabolism of silica deposition in the demosponge Suberites domuncula. In Silicon Biomineralization: Biology-Biochemistry-Molecular Biology-Biotechnology, Müller WEG (ed.). Springer: Berlin; Progr Molec Subcell Biol 33: 249-268.
62. Schröder HC, Müller WEG. 1999; Inorganic Polyphosphates: Biochemistry, Biology, Biotechnology, vol 23. Springer Verlag: Berlin, Heidelberg.
63. Schröder HC, Wang XH, Manfrin A, et al. 2012a; Silicatein: acquisition of structure-guiding and structure-forming properties during maturation from the pro-silicatein to the silicatein form. J Biol Chem 287: 22196-22205.
64. Schröder HC, Wang XH, Wiens M, et al. 2012b; Silicate modulates the crosstalk between osteoblasts (SaOS-2) and osteoclasts (RAW 264.7 cells): inhibition of osteoclast growth and differentiation. J Cell Biochem 113: 3197-3206.
65. Schwartz MA, Assoian RK. 2001; Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J Cell Sci 114: 2553-2560.
66. Schwarz K, Milne DB. 1972; Growth-promoting effects of silicon in rats. Nature 239: 333-334.
67. Shimizu K, Cha J, Stucky GD, et al. 1998; Silicatein-α: cathepsin l-like protein in sponge biosilica. Proc Natl Acad Sci USA 95: 6234-6238.
68. Shoichet MS, Li RH, White ML, et al. 1996; Stability of hydrogels used in cell encapsulation: an in vitro comparison of alginate and agarose. Biotechnol Bioeng 50: 374-381.
69. Silva-Correia J, Miranda-Gonçalves V, Salgado AJ, et al. 2012; Angiogenic potential of gellan gum-based hydrogels for application in nucleus pulposus regeneration: in vivo study. Tissue Eng Part A 18: 1203-1212.
70. Supuran CT. 2008; Carbonic anhydrases - an overview. Curr Pharmaceut Design 14: 603-614.
71. Toender JE, Borchert M. 2012; US Patent Application No. 20120021480. Use of enzymes having silicase activity, 26 January 2012.
72. Tsuji K, Bandyopadhyay A, Harfe BD, et al. 2006; BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet 38: 1424-1429.
73. Viguet-Carrin S, Garnero P, Delmas PD. 2006; The role of collagen in bone strength. Osteoporos Int 17: 319-336.
74. Wang XH, Schröder HC, Diehl-Seifert B, et al. 2012a; Dual effect of inorganic polymeric phosphate/polyphosphate on osteoblasts and osteoclasts in vitro. J Tissue Eng Regen Med (in press).
75. Wang XH, Schröder HC, Wang K, et al. 2012b; Genetic, biological and structural hierarchies during sponge spicule formation: from soft sol-gels to solid 3D silica composite structures. Soft Matter 8: 9501-9518.
76. Wang XH, Schröder HC, Wiens M, et al. 2012c; Bio-silica and bio-polyphosphate: applications in biomedicine (bone formation). Curr Opin Biotechnol 23: 570-578.
77. Wang XH, Schlossmacher U, Schröder HC, et al. 2013; Biologically-induced transition of bio-silica sol to mesoscopic gelatinous flocs: a biomimetic approach to a controlled fabrication of bio-silica structures. Soft Matter 9: 654-664.
78. Wiens M, Wang XH, Natalio F, et al. 2010a; Bioinspired fabrication of bio-silica-based bone substitution materials. Adv Eng Mater 12: B438-450.
79. Wiens M, Wang XH, Schlossmacher U, et al. 2010b; Osteogenic potential of bio-silica on human osteoblast-like (SaOS-2) cells. Calcif Tissue Int 87: 513-524.
80. Wiens M, Wang XH, Schröder HC, et al. 2010c; The role of biosilica in the osteoprotegerin:RANKL ratio in human osteoblast-like cells. Biomaterials 31: 7716-7725.
81. Workman VL, Dunnett SB, Kille P, et al. 2007; Microfluidic chip-based synthesis of alginate microspheres for encapsulation of immortalized human cells. Biomicrofluidics 1: 014105; DOI: 10.1063/1.2431860.
82. Wüst S, Müller R, Hofmann S. 2011; Controlled positioning of cells in biomaterials - approaches towards 3D tissue printing. J Funct Biomater 2: 119-154.
83. Zhang J, Wang M, Cha JM, et al. 2009; The incorporation of 70s bioactive glass to the osteogenic differentiation of murine embryonic stem cells in 3D bioreactors. J Tissue Eng Regen Med 3: 63-71.
84. Zhu Z, Xue LM, Han T, et al. 2010; Antiosteoporotic effects and proteomic characterization of the target and mechanism of an Er-Xian Decoction on osteoblastic UMR-106 and osteoclasts induced from RAW264.7. Molecules 15: 4695-4710.