Advertisement

Cell and Tissue Research

, Volume 339, Issue 2, pp 429–436 | Cite as

Silicatein-mediated incorporation of titanium into spicules from the demosponge Suberites domuncula

  • Filipe Natalio
  • Enrico Mugnaioli
  • Matthias Wiens
  • Xiaohong Wang
  • Heinz C. Schröder
  • Muhammad Nawaz Tahir
  • Wolfgang Tremel
  • Ute Kolb
  • Werner E. G. MüllerEmail author
Regular Article

Abstract

Primmorphs (a three-dimensional sponge primary cell culture system) have been revealed to be a cell/tissue nano-factory for the production of tailor-made hybrid nanostructures. Growth of primmorphs is stimulated by the presence of a titanium alkoxide precursor tolerating titania (TiO2) concentrations up to 250 μM. The presence and activity of silicatein in primmorphs has been analyzed by gel electrophoresis and Western blotting. Results of studies by scanning transmission electron microscopy with energy-dispersive X-ray spectroscopy have revealed silica and titania to be co-localized on nanosized spicules. Our findings suggest that the incorporation of titania into the nanosized spicule is enzymatically mediated via active silicatein in an orchestrated mechanism.

Keywords

Silicatein Primmorphs Nanomaterials Sponges Suberites domuncula (Porifera) 

References

  1. Belton DJ, Patwardhan SV, Annenkov VV, Danilovtseva EN, Perry CC (2008) From biosilicification to tailored materials: optimizing hydrophobic domains and resistance to protonation of polyamines. Proc Natl Acad Sci USA 105:5963–5968CrossRefPubMedGoogle Scholar
  2. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  3. Brinker CJ, Scherrer GW (1990) Sol-gel science: the physics and chemistry of sol-gel processing. Academic Press, LondonGoogle Scholar
  4. Custodio RM, Prokic I, Steffen R, Koziol C, Borojevic R, Brümmer F, Nickel M, Müller WEG (1998) Primmorphs generated from dissociated cells of the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech Ageing Dev 105:45–59CrossRefPubMedGoogle Scholar
  5. Hench LL, West JK (1990) The sol-gel process. Chem Rev 90:33–72CrossRefGoogle Scholar
  6. Krasko A, Lorenz B, Batel R, Schröder HC, Müller IM, Müller WEG (2000) Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem 267:4878–4887CrossRefPubMedGoogle Scholar
  7. Kröger N, Deutzmann R, Sumper M (1999) Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science 286:1129–1132CrossRefPubMedGoogle Scholar
  8. Kröger N, Deutzmann R, Bergsdorf C, Sumper M (2000) Species-specific polyamines from diatoms control silica morphology. Proc Natl Acad Sci USA 97:14133–14138CrossRefPubMedGoogle Scholar
  9. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  10. Lux A, Luxova M, Morita S, Abe J, Inanaga S (1999) Endodermal silicification in developing seminal roots of lowland and upland cultivars of rice (Oryza sativa L.). Can J Bot 77:955–960CrossRefGoogle Scholar
  11. Matsunaga S, Sakai R, Jimbo M, Kamiya H (2007) Long-chain polyamines (LCPAs) from marine sponge: possible implication in spicule formation. Chembiochem 8:1729–1735CrossRefPubMedGoogle Scholar
  12. Morse DE (1999) Silicon biotechnology: harnessing biological silica production to make new materials. Trends Biotechnol 17:230–232CrossRefGoogle Scholar
  13. Mugnaioli E, Natalio F, Schloβmacher U, Wang X, Müller WEG, Kolb U (2009) Crystalline nanorods as possible templates for the synthesis of amorphous biosilica during spicule formation in Demospongiae. Chembiochem 10:683–689CrossRefPubMedGoogle Scholar
  14. Müller WEG, Wiens M, Batel R, Steffen R, Borojevic R, Custodio RM (1999) Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula. Mar Ecol Progr Ser 178:205–219CrossRefGoogle Scholar
  15. Müller WEG, Krasko A, Le Pennec G, Steffen R, Ammar MSA, Wiens M, Müller IM, Schröder HC (2003) Molecular mechanism of spicule formation in the demosponge Suberites domuncula: silicatein-collagen–myotrophin. Prog Mol Subcell Biol 33:195–221PubMedGoogle Scholar
  16. Müller WEG, Rothenberger M, Boreiko A, Tremel W, Reiber A, Schröder HC (2005a) Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell Tissue Res 321:285–297CrossRefPubMedGoogle Scholar
  17. Müller WEG, Boreiko A, Brandt D, Osinga R, Ushijima H, Hamer B, Krasko A, Xupeng C, Müller IM, Schröder HC (2005b) Selenium affects biosilica formation in the demosponge Suberites domuncula. FEBS J 272:3838–3852CrossRefPubMedGoogle Scholar
  18. Müller WEG, Belikov S, Tremel W, Perry CC, Gieskes WWC, Boreiko A, Schröder HC (2006) Siliceous spicules in marine demosponges (example Suberites domuncula). Micron 37:107–120CrossRefPubMedGoogle Scholar
  19. Müller WEG, Schloßmacher U, Wang X, Boreiko A, Brandt D, Wolf SE, Tremel W, Schröder HC (2008) Poly(silicate)-metabolizing silicatein in siliceous spicules and silicasomes of demosponges comprises dual enzymatic activities (silica-polymerase and silica-esterase). FEBS J 275:362–370CrossRefPubMedGoogle Scholar
  20. Schröder HC, Boreiko O, Krasko A, Reiber A, Schwertner H, Müller WEG (2005) Mineralization of SaOS-2 cells on enzymatically (silicatein) modified bioactive osteoblast-stimulating surfaces. J Biomed Mater Res B Appl Biomater 75B:387–392CrossRefGoogle Scholar
  21. Schröder HC, Boreiko A, Korzhev M, Tahir MN, Tremel W, Eckert C, Ushijima H, Müller IM, Müller WEG (2006) Co-expression and functional interaction of silicatein with galectin. Matrix-guided formation of siliceous spicules in the marine demosponge Suberites domuncula. J Biol Chem 281:12001–12009CrossRefPubMedGoogle Scholar
  22. Schröder HC, Natalio F, Shukoor MI, Tremel W, Schloßmacher U, Wang X, Müller WEG (2007) Apposition of silica lamellae during growth of spicules in the demosponge Suberites domuncula: biological/biochemical studies and chemical/biomimetical confirmation. J Struct Biol 159:325–334CrossRefPubMedGoogle Scholar
  23. Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein α: cathepsin-L like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238CrossRefPubMedGoogle Scholar
  24. Shukoor MI, Natalio F, Therese HA, Tahir MN, Ksenofontov V, Panthöfer M, Eberhardt M, Theato P, Schröder HC, Müller WEG, Tremel W (2008) Fabrication of a silica coating on magnetic γ-Fe2O3 nanoparticles by an immobilized enzyme. Chem Mater 20:3567–3573CrossRefGoogle Scholar
  25. Stanford CM, Keller JC (1991) The concept of osseointegration and bone matrix expression. Crit Rev Oral Biol Med 2:83–101PubMedGoogle Scholar
  26. Stöber W, Fink A, Bohn E (1968) Controlled growth of mono-disperse silica spheres in the micron size range. J Colloid Interface Sci 26:62–69CrossRefGoogle Scholar
  27. Tahir MN, Théato P, Müller WEG, Schröder HC, Janshoff A, Zhang J, Huth J, Tremel W (2004) Formation of biosilica by immobilization of silicatein on novel functionalized surfaces. Chem Commun 24:2848–2849CrossRefGoogle Scholar
  28. Tahir MN, Théato P, Müller WEG, Schröder HC, Borejko A, Faiß S, Janshoff A, Huth J, Tremel W (2005) Formation of layered titania and zirconia catalysed by surface-bound silicatein. Chem Commun 28:5533–5535CrossRefGoogle Scholar
  29. Tahir MN, Eberhardt M, Therese HA, Kolb U, Theato P, Müller WEG, Schröder HC, Tremel W (2006) From single molecules to nanoscopically structured functional materials: Au nanocrystal growth on TiO2 nanowires controlled by surface-bound silicatein. Angew Chem Int Ed 45:4803–4809CrossRefGoogle Scholar
  30. Tolbert SH, Firouzi A, Stucky GD, Chmelka BF (1997) Magnetic field alignment of ordered silicate-surfactant composites and mesoporous silica. Science 278:264–268CrossRefGoogle Scholar
  31. Wetherbee R (2002) The diatom glasshouse. Science 298:547CrossRefPubMedGoogle Scholar
  32. Zhang X, Le Pennec G, Steffen R, Müller WEG, Zhang W (2004) Application of a MTT assay for screening nutritional factors in growth media of primary sponge cell culture. Biotechnol Prog 20:151–155CrossRefPubMedGoogle Scholar
  33. Zhou Y, Shimizu K, Cha JN, Stucky GD, Morse DE (1999) Efficient catalysis of polysiloxane synthesis by silicatein requires specific hydroxyl and imidazole functionalities. Angew Chem Int Ed 38:780–782CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Filipe Natalio
    • 1
  • Enrico Mugnaioli
    • 2
  • Matthias Wiens
    • 1
  • Xiaohong Wang
    • 3
  • Heinz C. Schröder
    • 1
  • Muhammad Nawaz Tahir
    • 4
  • Wolfgang Tremel
    • 4
  • Ute Kolb
    • 2
  • Werner E. G. Müller
    • 1
    Email author
  1. 1.Institute for Physiological Chemistry, Department of Applied Molecular BiologyJohannes-Gutenberg-Universität MainzMainzGermany
  2. 2.Institute for Physical ChemistryJohannes-Gutenberg-Universität MainzMainzGermany
  3. 3.National Research Center for GeoanalysisBeijingChina
  4. 4.Institute for Inorganic and Analytical ChemistryJohannes-Gutenberg-Universität MainzMainzGermany

Personalised recommendations