Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T17:09:50.543Z Has data issue: false hasContentIssue false
  • English
  • Français

Collagen-fibril matrix properties modulate the kinetics of silica polycondensation to template and direct biomineralization

Published online by Cambridge University Press:  28 January 2016

Jennifer L. Kahn ,
Necla Mine Eren ,
Osvaldo Campanella ,
Sherry L. Voytik-Harbin  and
Jenna L. Rickus
Jennifer L. Kahn
Affiliation:
Department of Agricultural & Biological Engineering, Purdue University, West Lafayette, Indiana 47907, USA; and Physiological Sensing Facility at the Bindley Bioscience Center and Birck Nanotechnology Center, Purdue University, West Lafayette, Indiana 47907, USA
Necla Mine Eren
Affiliation:
Department of Agricultural & Biological Engineering, Purdue University, West Lafayette, Indiana 47907, USA
Osvaldo Campanella
Affiliation:
Department of Agricultural & Biological Engineering, Purdue University, West Lafayette, Indiana 47907, USA
Sherry L. Voytik-Harbin
Affiliation:
Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN 47907, USA; and Department of Basic Medical Sciences, Purdue University, West Lafayette, Indiana 47907, USA
Jenna L. Rickus*
Affiliation:
Department of Agricultural & Biological Engineering, Purdue University, West Lafayette, Indiana 47907, USA; Physiological Sensing Facility at the Bindley Bioscience Center and Birck Nanotechnology Center, Purdue University, West Lafayette, Indiana 47907, USA; and Weldon School of Biomedical Engineering, Purdue University, West Lafayette, Indiana 47907, USA
*
a) Address all correspondence to this author. e-mail: rickus@purdue.edu
Get access

Abstract

Fibrillar collagen networks template and direct biocompatible silica mineralization to produce hybrid materials for biomedical applications. Silica mineralization kinetics is critical for precision-tuning material properties, including mechanical strength, microstructure, and interface thickness. We investigated the effect of varying collagen template fibril volume fraction (0.2–0.8) and elasticity (G′ 200–1500 Pa) on silica mineralization rates. Measurement of the depletion of mono- and disilicic acids by silicomolybdic acid titration showed that silica condensation on collagen fibrils follows third-order kinetics. Resulting third-order rate constants increased linearly with storage modulus and quadratically with fibril volume fraction. A unique rheological approach used to probe the collagen template surface elasticity in real-time during silicification suggested a two-phase mechanism with high levels of surface-localized gelation in Phase 1 and high levels of bulk solution-localized gelation in Phase 2. These results provide a tool for controlling hybrid collagen-silica material properties by controlling local silica condensation rates.

Keywords

biomimetic (assembly)sol–gelkinetics
Type
Biomineralization and Biomimetics Articles
Information
Journal of Materials Research , Volume 31 , Issue 3 , 15 February 2016 , pp. 311 - 320
Copyright
Copyright © Materials Research Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Contributing Editor: Laurie Gower

References

REFERENCES

Jaroch, D., McLamore, E., Zhang, W., Shi, J., Garland, J., Banks, M.K., Porterfield, D.M., and Rickus, J.L.: Cell-mediated deposition of porous silica on bacterial biofilms. Biotechnol. Bioeng. 108, 2249–2260 (2011).CrossRefGoogle ScholarPubMed
Jaroch, D.B., Lu, J., Madangopal, R., Stull, N.D., Stensberg, M., Shi, J., Kahn, J.L., Herrera-Perez, R., Zeitchek, M., Sturgis, J., Robinson, J.P., Yoder, M.C., Porterfield, D.M., Mirmira, R.G., and Rickus, J.L.: Mouse and human islets survive and function after coating by biosilicification. Am. J. Physiol.: Endocrinol. Metab. 305, E1230–E1240 (2013).Google ScholarPubMed
Garcia, A.P., Sen, D., and Buehler, M.J.: Hierarchical silica nanostructures inspired by diatom algae yield superior deformability, toughness, and strength. Metall. Mater. Trans. A 42, 3889–3897 (2011).CrossRefGoogle Scholar
Losic, D., Mitchell, J.G., and Voelcker, N.H.: Diatomaceous lessons in nanotechnology and advanced materials. Adv. Mater. 21, 2947–2958 (2009).CrossRefGoogle Scholar
Zhao, D., Jianglin, F., Huo, Q., Melosh, N., Fredrickson, G.H., Chmelka, B.F., and Stucky, G.D.: Triblock copolymer syntheses of mesoporous silica with periodic 50 to 300 Angstrom pores. Science 279, 548–552 (1998).CrossRefGoogle ScholarPubMed
Beck, J.S., Vartuli, J.C., Roth, W.J., Leonowicz, M.E., Kresge, C.T., Schmitt, K.D., Chu, C.T-W., Olson, D.H., Sheppard, E.W., McCullen, S.B., Higgins, J.B., and Schlenker, J.L.: A new family of mesoporous molecular sieves prepared with liquid crystal templates. J. Am. Chem. Soc. 114, 10834–10843 (1992).CrossRefGoogle Scholar
Ellerby, L.M., Nishida, C.R., Nishida, F., Yamanaka, S.A., Dunn, B., Valentine, J.S., and Zink, J.I.: Encapsulation of proteins in transparent porous silicate glasses prepared by the sol-gel method. Science 255, 1113–1115 (1992).CrossRefGoogle ScholarPubMed
Brinker, C.J. and Scherer, G.W.: Sol-gel Science: The Physics and Chemistry of Sol-gel Processing (Academic Press, Boston, 1990).Google Scholar
Iler, R.K.: The Chemistry of Silica: Solubility, Polymerization, Colloid and Surface Properties and Biochemistry of Silica (Wiley-Interscience, 1979).Google Scholar
Brinker, C.J., Sehgal, R., Hietala, S.L., Deshpande, R., Smith, D.M., Loy, D., and Ashley, C.S.: Sol-gel strategies for controlled porosity inorganic materials. J. Membr. Sci. 94, 85–102 (1994).CrossRefGoogle Scholar
Tobler, D.J., Shaw, S., and Benning, L.G.: Quantification of initial steps of nucleation and growth of silica nanoparticles: An in-situ SAXS and DLS study. Geochim. Cosmochim. Acta 73, 5377–5393 (2009).CrossRefGoogle Scholar
Belton, D.J., Deschaume, O., Patwardhan, S.V., and Perry, C.C.: A solution study of silica condensation and speciation with relevance to in vitro investigations of biosilicification. J. Phys. Chem. B 114, 9947–9955 (2010).CrossRefGoogle ScholarPubMed
Patwardhan, S.V., Emami, F.S., Berry, R.J., Jones, S.E., Naik, R.R., Deschaume, O., Heinz, H., and Perry, C.C.: Chemistry of aqueous silica nanoparticle surfaces and the mechanism of selective peptide adsorption. J. Am. Chem. Soc. 134, 6244–6256 (2012).CrossRefGoogle ScholarPubMed
Coradin, T., Nassif, N., and Livage, J.: Silica-alginate composites for microencapsulation. Appl. Microbiol. Biotechnol. 61, 429–434 (2003).CrossRefGoogle ScholarPubMed
Wallace, A.F., DeYoreo, J.J., and Dove, P.M.: Kinetics of silica nucleation on carboxyl- and amine-terminated surfaces: Insights for biomineralization. J. Am. Chem. Soc. 131, 5244–5250 (2009).CrossRefGoogle ScholarPubMed
Coradin, T. and Livage, J.: Effect of some amino acids and peptides on silicic acid polymerization. Colloids Surf., B 21, 329–336 (2001).CrossRefGoogle ScholarPubMed
Hecky, R.E., Mopper, K., Kilham, P., and Degens, E.T.: The amino acid and sugar composition of diatom cell-walls. Mar. Biol. 19, 323–331 (1973).CrossRefGoogle Scholar
Shimizu, K., Cha, J., Stucky, G.D., and Morse, D.E.: Silicatein alpha: Cathepsin L-like protein in sponge biosilica. Proc. Natl. Acad. Sci. U. S. A. 95, 6234–6238 (1998).CrossRefGoogle ScholarPubMed
Sumper, M. and Brunner, E.: Learning from diatoms: Nature's tools for the production of nanostructured silica. Adv. Funct. Mater. 16, 17–26 (2006).CrossRefGoogle Scholar
Müller, W.E.G., Schröder, H.C., Burghard, Z., Pisignano, D., and Wang, X.: Silicateins-a novel paradigm in bioinorganic chemistry: Enzymatic synthesis of inorganic polymeric silica. Chem. Lett. 19, 5790–5804 (2013).Google ScholarPubMed
Birchall, J.D.: The essentiality of silicon in biology. Chem. Soc. Rev. 24, 351 (1995).CrossRefGoogle Scholar
Ehrlich, H., Deutzmann, R., Brunner, E., Cappellini, E., Koon, H., Solazzo, C., Yang, Y., Ashford, D., Thomas-Oates, J., Lubeck, M., Baessmann, C., Langrock, T., Hoffmann, R., Wörheide, G., Reitner, J., Simon, P., Tsurkan, M., Ereskovsky, A.V., Kurek, D., Bazhenov, V.V., Hunoldt, S., Mertig, M., Vyalikh, D.V., Molodtsov, S.L., Kummer, K., Worch, H., Smetacek, V., and Collins, M.J.: Mineralization of the metre-long biosilicastructures of glass sponges is templatedon hydroxylated collagen. Nat. Chem. 2, 1084–1088 (2010).CrossRefGoogle ScholarPubMed
Ono, Y., Kanekiyo, Y., Inoue, K., Hojo, J., Nango, M., and Shinkai, S.: Preparation of novel hollow fiber silica using collagen fibers as a template. Chem. Lett. 6, 475–476 (1999).CrossRefGoogle Scholar
Heinemann, S., Ehrlich, H., Knieb, C., and Hanke, T.: Biomimetically inspired hybrid materials based on silicified collagen. Int. J. Mater. Res. 98, 603–608 (2007).CrossRefGoogle Scholar
Kahn, J.L., Eren, N.M., Campanella, O., Voytik-Harbin, S.L., and Rickus, J.L.: Organic hydrogel templates for tunable mesoporous silica hybrid materials. MRS Proc. 1721, doi: 10.1556/opl.2015.38 (2015).CrossRefGoogle Scholar
Niu, L-N., Jiao, K., Qi, Y-P., Yiu, C.K.Y., Ryou, H., Arola, D.D., Chen, J-H., Breschi, L., Pashley, D.H., and Tay, F.R.: Infiltration of silica inside fibrillar collagen. Angew. Chem. Int. Ed. 50, 11688–11691 (2011).CrossRefGoogle ScholarPubMed
Shoulders, M.D. and Raines, R.T.: Collagen structure and stability. Annu. Rev. Biochem. 78, 929–958 (2009).CrossRefGoogle ScholarPubMed
Ramshaw, J.A.M., Shah, N.K., and Brodsky, B.: Gly-X-Y tripeptide frequencies in collagen: a context for host–guest triple-helical peptides. J. Struct. Biol. 122, 86–91 (1998).CrossRefGoogle ScholarPubMed
Bailey, J.L., Critser, P.J., Whittington, C., Kuske, J.L., Yoder, M.C., and Voytik-Harbin, S.L.: Collagen oligomers modulate physical and biological properties of three-dimensional self-assembled matrices. Biopolymers 95, 77–93 (2011).CrossRefGoogle ScholarPubMed
Kreger, S.T., Bell, B.J., Bailey, J., Stites, E., Kuske, J., Waisner, B., and Voytik-Harbin, S.L.: Polymerization and matrix physical properties as important design considerations for soluble collagen formulations. Biopolymers 93, 690–707 (2010).CrossRefGoogle ScholarPubMed
Kadler, K.E., Holmes, D.F., Trotter, J.A., and Chapman, J.A.: Collagen fibril formation. Biochem. J. 316, 1–11 (1996).CrossRefGoogle ScholarPubMed
Ramadass, S.K., Perumal, S., Gopinath, A., Nisal, A., Subramanian, S., and Madhan, B.: Sol–gel assisted fabrication of collagen hydrolysate composite scaffold: A novel therapeutic alternative to the traditional collagen scaffold. ACS Appl. Mater. Interfaces 6, 15015–15025 (2014).CrossRefGoogle Scholar
Jing, S., Jiang, D., Wen, S., Wang, J., and Yang, C.: Preparation and characterization of collagen/silica composite scaffolds for peripheral nerve regeneration. J. Porous Mater. 21, 699–708 (2014).CrossRefGoogle Scholar
Heinemann, S., Heinemann, C., Wenisch, S., Alt, V., Worch, H., and Hanke, T.: Calcium phosphate phases integrated in silica/collagen nanocomposite xerogels enhance the bioactivity and ultimately manipulate the osteblast/osteclast ratio in a human co-culture model. Acta Biomater. 9, 4878–4888 (2013).CrossRefGoogle Scholar
Wang, X., Schloßmacher, U., Schröder, H.C., and Müller, W.E.G.: 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 (2013).CrossRefGoogle Scholar
Niu, L-N., Jiao, K., Ryou, H., Diogenes, A., Yiu, C.K.Y., Mazzoni, A., Chen, J-H., Arola, D.D., Hargreaves, K.M., Pashley, D.H., and Tay, F.R.: Biomimetic silicification of demineralized hierarchical collagenous tissues. Biomacromolecules 14, 1661–1668 (2013).CrossRefGoogle ScholarPubMed
Brightman, A.O., Rajwa, B.P., Sturgis, J.E., McCallister, M.E., Robinson, J.P., and Voytik-Harbin, S.L.: Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers 54, 222–234 (2000).3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Marotta, M. and Martino, G.: Sensitive spectrophotometric method for the quantitative estimation of collagen. Anal. Biochem. 150, 86–90 (1985).CrossRefGoogle ScholarPubMed
ASTM F3089-14: Standard Guide for Characterization and Standardization of Polymerizable Collagen-Based Products and Associated Collagen-Cell Interactions (ASTM International, West Conshohocken, PA, 2014).Google Scholar
Coradin, T., Eglin, D., and Livage, J.: The silicomolybdic acid spectrophotometric method and its application to silicate/biopolymer interaction studies. Spectroscopy 18, 567–576 (2004).CrossRefGoogle Scholar
Harrison, C.C. and Loton, N.: Novel routes to designer silicas: Studies of the decomposition of (M+)2[Si(C6 H4O2)3]·xH2O. Faraday Trans. 91, 4287–4297 (1995).CrossRefGoogle Scholar
Whittington, C.F., Brandner, E., Teo, K.Y., Han, B., Nauman, E., and Voytik-Harbin, S.L.: Oligomers modulate interfibril branching and mass transport properties of collagen matrices. Microsc. Microanal. 19, 1323–1333 (2013).CrossRefGoogle ScholarPubMed
Nudelman, F., Pieterse, K., George, A., Bomans, P.H.H., Friedrich, H., Brylka, L.J., Hilbers, P.A.J., de With, G., and Sommerdijk, N.A.J.M.: The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 9, 1004–1009 (2010).CrossRefGoogle ScholarPubMed
Eglin, D., Shafran, K.L., Livage, J., Coradin, T., and Perry, C.C.: Comparative study of the influence of several silica precursors on collagen self-assembly and of collagen on “Si” speciation and condensation. J. Mater. Chem. 16, 4220–4230 (2006).CrossRefGoogle Scholar
Supplementary material: File

Kahn supplementary material

Table S1 and Figures S1-S2

Download Kahn supplementary material(File)
File 327.3 KB