Analysis of the axial filament in spicules of the demosponge Geodia cydonium: Different silicatein composition in microscleres (asters) and megascleres (oxeas and triaenes)

European Journal of Cell Biology

Volumn 86, Issue 8, 2007, Pages 473-487

  Müller, Werner E G ^a   Schloßmacher, Ute ^a   Eckert, Carsten ^a   Krasko, Anatoli ^a   Boreiko, Alexandra ^a   Ushijima, Hiroshi ^b   Wolf, Stephan E ^a   Tremel, Wolfgang ^a   Müller, Isabel M ^a   Schröder, Heinz C ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Collagen; Geodia cydonium; Morphogenesis; Porifera; Silicatein; Sponges

Indexed keywords

ENZYME; SILICATEIN ALPHA; SILICATEIN BETA; SILICATEIN GAMMA; UNCLASSIFIED DRUG;

ARTICLE; ELECTRON MICROSCOPY; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; GENE IDENTIFICATION; GEODIA CYDONIUM; MORPHOLOGY; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SKELETON; SPONGE (PORIFERA); SYNTHESIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

DEMOSPONGIAE; GEODIA CYDONIUM; HEXACTINELLIDA; PORIFERA; SUBERITES DOMUNCULA; TETHYA AURANTIUM;

EID: 34547104008     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2007.06.002     Document Type: Article

References (62)

1. Arndt, W., 1935. Die Tierwelt der Nord- und Ostsee, vol. IIIa. Porifera. Akademische Verlagsgesellschaft, Leipzig, pp. IIIa2-IIIa2140.
2. Bailey A.J. Comparative studies on the nature of the cross-links stabilizing the collagen fibres of invertebrates, cyclostomes and elasmobranchs. FEBS Lett. 18 (1971) 154-158
3. Blumbach B., Diehl-Seifert B., Seack J., Steffen R., Müller I.M., and Müller W.E.G. Cloning and expression of new receptors belonging to the immunoglobulin superfamily from the marine sponge Geodia cydonium. Immunogenetics 49 (1999) 751-763
4. Cha J.N., Shimizu K., Zhou Y., Christianssen S.C., Chmelka B.F., Stucky G.D., and Morse D.E. Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proc. Natl. Acad. Sci. USA 96 (1999) 361-365
5. Coligan J.E., Dunn B.M., Speicher D.W., and Wingfield P.T. Current Protocols in Protein Science (1998), Wiley, New York pp. 10.4.1-10.4.36
6. Compton S., and Jones C.G. Mechanism of dye response and interference in the Bradford protein assay. Anal. Biochem. 151 (1985) 369-374
7. Croce G., Frache A., Milanesio M., Marchese L., Causa M., Viterbo D., Barbaglia A., Bolis V., Bavestrello G., Cerrano C., Benatti U., Pozzolini M., Giovine M., and Amenitsch H. Structural characterization of siliceous spicules from marine sponges. Biophys. J. 86 (2004) 526-534
8. Dayhoff M.O., Schwartz R.M., and Orcutt B.C. A model of evolutionary change in protein. In: Dayhoff M.O. (Ed). Atlas of Protein Sequence and Structure (1978), Nat. Biomed. Research Foundation, Washington, DC 345-352
9. Diehl-Seifert B., Kurelec B., Zahn R.K., Dorn A., Jerecevic B., Uhlenbruck G., and Müller W.E.G. Attachment of sponge cells to collagen substrata: effect of a collagen assembly factor. J. Cell Sci. 79 (1985) 271-285
10. Donati V. Auszug seiner Natur-Geschichte des Adriatischen Meeres (1753), C.P. Franckens, Halle
11. Eckert C., Schröder H.C., Brandt D., Perovic-Ottstadt S., and Müller W.E.G. A histochemical and electron microscopic analysis of the spiculogenesis in the demosponge Suberites domuncula. J. Histochem. Cytochem. 54 (2006) 1031-1040
12. 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 (2006) 4220-4230
13. Ehrlich H., and Worch H. Collagen, a huge matrix in glass-sponge flexible spicules of the meter-long Hyalonema sieboldi. In: In Bäuerlein E. (Ed). Handbook of Biomineralization, vol. 1. The Biology of Biominerals Structure Formation (2007), Wiley-VCH, Weinheim 23-41
14. Ehrlich H., Ereskovskii A.V., Drozdov A.L., Krylova D.D., Hanke T., Meissner H., Heinemann S., and Worch H. A modern approach to demineralization of spicules in glass sponges (Porifera: Hexactinellida) for the purpose of extraction and examination of the protein matrix. Russ. J. Mar. Sci. 32 (2006) 186-193
15. Evans R. A description of Ephydatia blembingia with an account of the formation and structure of the gemmule. Q. J. Microsc. Sci. 44 (1900) 71-109
16. Exposito J.Y., Cluzel C., Garrone R., and Lethias C. Evolution of collagens. Anat. Rec. 268 (2002) 302-316
17. Felsenstein J. PHYLIP, ver. 3.5 (1993), University of Washington, Seattle
18. Garrone R. Phylogenesis of Connective Tissue (1978), Karger, Basel
19. Garrone R., Vacelet J., Pavans de Ceccatty M., Junqua S., and Robert L. Une formation collagène particulière: les filaments des éponges cornies Ircinia. Étude ultrastructurale, physico-chimique et biochimique. J. Microsc. 17 (1973) 241-260
20. Grebenjuk V.A., Kuusksalu A., Kelve M., Schütze J., Schröder H.C., and Müller W.E.G. Induction of (2′-5′)oligoadenylate synthetase in the marine sponges Suberites domuncula and Geodia cydonium by the bacterial endotoxin lipopolysaccharide. Eur. J. Biochem. 269 (2002) 1382-1392
21. Imhoff J.M., and Garrone R. Solubilization and characterization of Chondrosia reniformis sponge collagen. Connect. Tissue Res. 11 (1983) 193-197
22. Junqua S., Robert L., Garrone R., Pavans de Ceccatty M., and Vacelet J. Biochemical and morphological studies on collagens of horny sponges Ircinia filaments compared to spongines. Connect. Tissue Res. 2 (1974) 193-203
23. Krasko A., Batel R., Schröder H.C., Müller I.M., and Müller W.E.G. Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur. J. Biochem. 267 (2000) 4878-4887
24. Krasko A., Schröder H.C., Batel R., Grebenjuk V.A., Steffen R., Müller I.M., and Müller W.E.G. Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA Cell Biol. 21 (2002) 67-80
25. Kruse M., Müller I.M., and Müller W.E.G. Early evolution of metazoan serine/threonine and tyrosine kinases: identification of selected kinases in marine sponges. Mol. Biol. Evol. 14 (1997) 1326-1334
26. Kruse M., Leys S.P., Müller I.M., and Müller W.E.G. Phylogenetic position of the Hexactinellida within the phylum Porifera based on amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J. Mol. Evol. 46 (1998) 721-728
27. Lieberkühn N. Zur Entwicklungsgeschichte der Spongillen. Arch. Anat. Physiol. (1856) 399-414
28. Linné, C., 1788. Systema Naturae; Tomus I, Pars VI. G.E. Beer, Lipsiae.
29. McBride O.W., and Harrington W.F. Evidence for disulfide cross-linkages in an invertebrate collagen. J. Biol. Chem. 240 (1965) 4545-4547
30. Minchin E.A. Sponge-spicules. Erg. Fortschr. Zool. 2 (1909) 171-274
31. Müller W.E.G., Borejko A., Brandt D., Osinga R., Ushijima H., Hamer B., Krasko A., Xupeng C., Müller I.M., and Schröder H.C. Selenium affects biosilica formation in the demosponge Suberites domuncula: effect on gene expression and spicule formation. FEBS J. 272 (2005) 3838-3852
32. Müller W.E.G., Rothenberger M., Boreiko A., Tremel W., Reiber A., and Schröder H.C. Formation of siliceous spicules in the marine demosponge Suberites domuncula. Cell Tissue Res. 321 (2005) 285-297
33. Müller W.E.G., Belikov S.I., Tremel W., Perry C.C., Gieskes W.W.C., Boreiko A., and Schröder H.C. Siliceous spicules in marine demosponges (example Suberites domuncula). Micron 37 (2006) 107-120
34. Müller W.E.G., Kaluzhnaya O.V., Belikov S.I., Rothenberger M., Schröder H.C., Reiber A., Kaandorp J.A., Manz B., Mietchen D., and Volke F. Magnetic resonance imaging of the siliceous skeleton of the demosponge Lubomirskia baicalensis. J. Struct. Biol. 153 (2006) 31-41
35. Müller W.E.G., Wang X., Belikov S.I., Tremel W., Schloßmacher U., Natoli A., Brandt D., Boreiko A., Tahir M.N., Müller I.M., and Schröder H.C. Formation of siliceous spicules in demosponges: example Suberites domuncula. In: Bäuerlein E. (Ed). Handbook of Biomineralization, vol. 1: The Biology of Biominerals Structure Formation (2006), Wiley-VCH, Weinheim 59-82
36. Müller W.E.G., Wang X., Belikov S.I., Wiens M., Grebenjuk V.A., Boreiko A., Schloßmacher U., and Schröder H.C. Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene 395 (2007) 62-71
37. Müller, W.E.G., Boreiko, A., Schloßmacher, U., Wang, X., Tahir, M.N., Tremel, W., Brandt, D., Kaandorp, J.A., Schröder, H.C., 2007b. Fractal-related assembly of the axial filament in the demosponge Suberites domuncula: relevance to biomineralization and the formation of biogenic silica. Biomaterials; in press. doi:10.1016/j.biomaterials.2007.06.030.
38. Murr M.M., and Morse D.E. Fractal intermediates in the self-assembly of silicatein filaments. Proc. Natl. Acad. Sci. USA 102 (2005) 11657-11662
39. Nicholas, K.B., Nicholas Jr., H.B., 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. Version 1.1.004. 〈http://www.nrbsc.org/gfx/genedoc/index.html〉.
40. Pancer Z., Kruse M., Müller I., and Müller W.E.G. On the origin of adhesion receptors of metazoa: cloning of the integrin α subunit cDNA from the sponge Geodia cydonium. Mol. Biol. Evol. 14 (1997) 391-398
41. Pfeifer K., Haasemann M., Gamulin V., Bretting H., Fahrenholz F., and Müller W.E.G. S-type lectins occur also in invertebrates: high conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydonium. Glycobiology 3 (1993) 179-184
42. Pisera A. Some aspects of silica deposition in lithistid demosponge desmas. Microsc. Res. Technol. 62 (2003) 336-355
43. Schmidt O. Die Spongien des Adriatischen Meeres (1862), Wilhelm Engelmann, Leipzig
44. Schröder H.C., Krasko A., Batel R., Skorokhod A., Pahler S., Kruse M., Müller I.M., and Müller W.E.G. Stimulation of protein (collagen) synthesis in sponge cells by a cardiac myotrophin-related molecule from Suberites domuncula. FASEB J. 14 (2000) 2022-2031
45. Schröder H.C., Boreiko A., Korzhev M., Tahir M.N., Tremel W., Eckert C., Ushijima H., Müller I.M., and Müller W.E.G. 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 (2006) 12001-12009
46. Schröder H.C., Natalio F., Shukoor I., Tremel W., Schloßmacher U., Wang X., and Müller W.E.G. Apposition of silica lamellae during growth of spicules in the demosponge Suberites domuncula: biological/biochemical studies and chemical/biomimetical confirmation. J. Struct. Biol. (2007) 10.1016/j.jsb.2007.01.007 (E-pub ahead of print)
47. Schulze F.E., and von Lendenfeld R. Die Bezeichnung der Spongiennadeln (1889), Georg Reimer, Berlin
48. Sethmann I., and Wörheide G. Structure and composition of calcareous sponge spicules: a review and comparison to structurally related biominerals. Micron (2007) 10.1016/j.micron.2007.01.006 (E-pub ahead of print)
49. Shimizu K., Cha J., Stucky G.D., and Morse D.E. Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc. Natl. Acad. Sci. USA 95 (1998) 6234-6238
50. Simpson T.L. The Cell Biology of Sponges (1984), Springer, New York
51. Simpson T.L., Langenbruch P.F., and Scalera-Liaci L. Silica spicules and axial filaments of the marine sponge Stelletta grubii (Porifera, Demospongia). Zoomorphology 105 (1985) 375-382
52. Sollas W.J. Report on the Tetractinellida. In: Wyville Thomson C. (Ed). Report on the Scientific Results of the Voyage of HMS Challenger during the Years 1873-76 (1888), Eyre & Spottiswooode, London
53. Stanley P.E., and Kricka L.J. Bioluminescence and Chemiluminescence: Current Status (1990), Wiley, New York
54. Swatschek D., Schatton W., Kellermann J., Müller W.E.G., and Kreuter J. Marine sponge collagen: isolation, characterisation and effects on the skin parameters surface - pH, moisture and sebum. Eur. J. Pharm. Biopharm. 53 (2002) 107-113
55. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
56. Towbin H., Özbey O., and Zingel O. An immunoblotting method for high-resolution isoelectric focusing of protein isoforms on immobilized pH gradients. Electrophoresis 22 (2001) 1887-1893
57. Uriz M.J. Family Geodiidae, Gray, 1867. In: Hooper J.N.A., and van Soest R.W.M. (Eds). Systema Porifera: A Guide to the Classification of Sponges (2002), Kluwer Academic/Plenum Publishers, New York 134-140
58. Uriz M.J., Turon X., Becerro M.A., and Agell G. Siliceous spicules and skeletal frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions. Microsc. Res. Tech. 62 (2003) 279-299
59. von Lendenfeld R. Untersuchungen über die Skelettbildungen der Kieselschwämme. Denkschr. Math.-Naturwiss. Klasse Akad. Wien. 88 (1912) 693-709
60. Weaver J.C., and Morse D.E. Molecular biology of demosponge axial filaments and their role in biosilicification. Microsc. Res. Tech. 62 (2003) 256-367
61. Wiens M., Koziol C., Hassanein H.M.A., Batel R., and Müller W.E.G. Expression of the chaperones 14-3-3 and HSP70 induced by PCB 118 (2,3′,4,4′,5-pentachlorobiphenyl) in the marine sponge Geodia cydonium. Mar. Ecol. Prog. Ser. 165 (1998) 247-257
62. Zhou Y., Shimizu K., Cha J.N., Stucky G.D., and Morse D.E. Efficient catalysis of polysiloxane synthesis by silicatein α requires specific hydroxyl and imidazole functionalities. Angew. Chem. [Int. Ed.] 38 (1999) 780-782