Molecular cloning and characterization of first organic matrix protein from sclerites of red coral, Corallium rubrum

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19367-19376

  Debreuil, Julien ^a   Tambutté, Éric ^a   Zoccola, Didier ^a   Deleury, Emeline ^b,c   Guigonis, Jean Marie ^c,d,e   Samson, Michel ^c   Allemand, Denis ^a   Tambutté, Sylvie ^a  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^b Institut Sophia Agrobiotech   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d Laboratoire TIRO   (France)

^e CENTRE ANTOINE LACASSAGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; CORALLIUM RUBRUM; DATA SETS; EDMAN DEGRADATION; EXPRESSED SEQUENCE TAGS; IMMUNOLABELING; ISOLATION AND CHARACTERIZATION; MOLECULAR CLONING; OPEN READING FRAME; ORGANIC MATRIX; PEPTIDE SEQUENCES; PHOSPHORYLATED PROTEINS; RED CORAL; SIGNAL PEPTIDE;

AMINO ACIDS; BIOMINERALIZATION; CLONING; DEGRADATION; MASS SPECTROMETRY; PHOSPHORYLATION;

PROTEINS;

EDETIC ACID; MATRIX PROTEIN; SCLERITIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY LABELING; ARTICLE; BIOMINERALIZATION; CONTROLLED STUDY; CORAL; CORALLIUM RUBRUM; EXOSKELETON; EXPRESSED SEQUENCE TAG; ISOELECTRIC POINT; MASS SPECTROMETRY; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; SCLERITE; SEQUENCE HOMOLOGY; TRANSCRIPTOMICS;

AMINO ACID SEQUENCE; ANIMALS; ANTHOZOA; CLONING, MOLECULAR; DATABASES, PROTEIN; EXTRACELLULAR MATRIX PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS;

ALCYONARIA; ANTHOZOA; CORALLIUM RUBRUM;

EID: 84861752030     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.352005     Document Type: Article

References (82)

1. Estroff, L. A. (2008) Introduction: biomineralization. Chem. Rev. 108, 4329-4331
2. Lowenstam, H. A., and Weiner, S. (1989) On Biomineralization, pp. 7-16, Oxford University Press, New York
3. Marin, F., Luquet, G., Marie, B., and Medakovic, D. (2008) Molluscan shell proteins: primary structure, origin, and evolution. Curr. Top. Dev. Biol. 80, 209-276
4. Mann, S. (2001) Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry (Compton, R. G., Davies, S. G., and Evans, J., eds) pp. 6-23, Oxford University Press, New York
5. Dubois, P., and Chen, C. P. (1989) in Echinoderm Studies (Jangoux, M., and Lawrence, J. M., eds) pp. 109-178, Rotterdam
6. Ehrlich, H., Koutsoukos, P. G., Demadis, K. D., Pokrovsky, O. S. (2009) Principles of demineralization: modern strategies for the isolation of organic frameworks. Part II. Decalcification. Micron 40, 169-193
7. Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. (1982) Mechanical Design in Organisms, Princeton University Press, Princeton, NJ
8. Harvell, C. D., and Fenical, W. (1989) Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.): intracolony localization of defense. Limnol. Oceanogr. 34, 382-389
9. Lewis, J. C., and Wallis, E. V. (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol. Bull. 181, 275-288
10. Bayer, F. M. (1961) The Shallow-water Octocorallia of the West Indian Region, Martinus Nijhoff, The Hague
11. Vargas, S., Breedy, O., Siles, F., and Guzman, H. M. (2010) How many kinds of sclerite? Towards a morphometric classification of gorgoniid microskeletal components. Micron 41, 158-164
12. Tescione, G. (1973) The Italians and Their Coral Fishing, Fausto Fiorentino, Napoli
13. Allemand, D. (1993) The biology and skeletogenesis of the Mediterranean red coral: a review. Precious Corals Octocoral Res. 2, 19-39
14. Morel, J.-P., Rondi-Costanzo, C., and Ugolini, D. (2000) Corallo di Ieri, Corallo di Oggi (Bari, ed), Centro Universitario Europeo per i beni culturali, Ravello Edipuglia
15. Weinberg, S. (1976) Revision of the common octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia 24, 63-103
16. Mateu, G., Traveria, A., Fontarnau, R., and Masso, C. (1986) Biodiagénesis mineralògica del Corallium rubrum (L.). Bol. Inst. Esp. Oceanogr. 3, 1-12
17. Grillo, M. C., Goldberg, W. M., and Allemand, D. (1993) Skeleton and sclerite formation in the precious red coral Corallium rubrum. Mar. Biol. 117, 119-128
18. Allemand, D., and Grillo, M.-C. (1992) Biocalcification mechanism in gorgonians: 45Ca uptake and deposition by the Mediterranean red coral Corallium rubrum. J. Exp. Zool. 262, 237-246
19. Lacaze-Duthiers, H. (1864) Histoire Naturelle du Corail, pp. 110-124, J. B. Baillière et Fils, Paris
20. Debreuil, J., Tambutté, S., Zoccola, D., Segonds, N., Techer, N., Allemand, D., and Tambutté, E. (2011) Comparative analysis of the soluble organic matrix of axial skeleton and sclerites of Corallium rubrum: insights for biomineralization. Comp. Biochem. Physiol. B 159, 40-48
21. Allemand, D., Cuif, J.-P., Watabe, N., Oishi, M., and Kawaguchi, T. (1994) Bulletin Institut Océanographique Monaco 14, 129-139
22. Cölfen, H., and Antonietti, M. (2005) Mesocrystals: inorganic superstructures made by highly parallel crystallization and controlled alignment. Angew. Chem. Int. Ed. 44, 5576-5591 (Pubitemid 41312141)
23. Floquet, N., and Vielzeuf, D. (2011) Mesoscale twinning and crystallographic registers in biominerals. Am. Mineralogist 96, 1228-1237
24. Borelli, G., Mayer-Gostan, N., Merle, P. L., De Pontual, H., Boeuf, G., Allemand, D., and Payan, P. (2003) Composition of biomineral organic matrices with special emphasis on turbot (Psetta maxima) otolith and endolymph. Calcif. Tissue Int. 72, 717-725 (Pubitemid 36917327)
25. Dauphin, Y. (2006) Mineralizing matrices in the skeletal axes of two Corallium species (Alcyonacea). Comp. Biochem. Physiol. A 145, 54-64
26. Merlin, J. C., and Dele, M. L. (1983) Etude par spectroscopie Raman de résonance de la pigmentation des squelettes calcaires de certains coraux. Bull. Soc. Zool. Fr. 108, 289-301
27. Cvejic, J., Tambutté, S., Lotto, S., Mikov, M., Slacanin, I., and Allemand, D. (2007) Determination of canthaxanthin in the red coral (Corallium rubrum) from Marseilles by HPLC combined with UV and MS detection. Mar. Biol. 152, 855-862 (Pubitemid 47301244)
28. Fritsch, E., and Karampelas, S. (2008) Comment on Determination of canthaxanthin in the red coral (Corallium rubrum) from Marseille by HPLC combined with UV and MS detection. Mar. Biol. 154, 929 -930
29. Rahman, M. A., and Isa, Y. (2005) Characterization of proteins from the matrix of spicules from the alcyonarian, Lobophytum crassum. J. Exp. Mar. Biol. Ecol. 321, 71-82 (Pubitemid 40793543)
30. Rahman, M. A., Isa, Y., and Uehara, T. (2005) Blood-based proteomics for personalized medicine: examples from neurodegenerative disease. Proteomics 5, 1-9
31. Rahman, M. A., Isa, Y., and Uehara, T. (2006) Studies on two closely related species of octocorallians: biochemical and molecular characteristics of the organic matrices of endoskeletal sclerites. Mar. Biotechnol. 8, 415-424 (Pubitemid 44221551)
32. Rahman, M. A., Isa, Y., Takemura, A., and Uehara, T. (2006) Analysis of proteinaceous components of the organic matrix of endoskeletal sclerites from the alcyonarian Lobophytum crassum. Calcif. Tissue Int. 78, 178-185
33. Rahman, M. A., Oomori, T., and Uehara, T. (2008) Carbonic anhydrase in calcified endoskeleton: novel activity in biocalcification in alcyonarian. Mar. Biotechnol. 10, 31-38 (Pubitemid 351207787)
34. Rahman, M. A., and Oomori, T. (2008) Structure, crystallization, and mineral composition of sclerites in the alcyonarian coral. J. Crystal. Growth 310, 3528-3534
35. Kingsley, R. J., Tsuzaki, M., Watabe, N., and Mechanic, G. L. (1990) Collagen in the spicule organic matrix of the gorgonian Leptogorgia virgulata. Biol. Bull. 179, 207-213
36. Kingsley, R. J., Melaro, E. W., Coe, K. E., Flory, M. R., Skorupa, A. M., and Harclerode, K. A. (1996) Mechanisms of the annual cycling of organicmatrix collagen from spicules of the gorgonian Leptogorgia virgulata. Invert. Biol. 115, 89-98
37. Kingsley, R. J., and Watabe, N. (1982) Ultrastructural investigation of spicule formation in the gorgonian Leptogorgia virgulata (Lamarck) (Coelenterata: Gorgonacea). Cell Tissue Res. 223, 325-334 (Pubitemid 12118684)
38. Kingsley, R. J., and Watabe, N. (1983) Analysis of proteinaceous components of the organic matrices of spicules from the gorgonian Leptogorgia virgulata. Comp. Biochem. Physiol. B 76, 443-447
39. Kingsley, R. J., and Watabe, N. (1989) The dynamics of spicule calcification in whole colonies of the gorgonian Leptogorgia virgulata Lam. (Coelenterata, Gorgonacea). J. Exp. Mar. Biol. Ecol. 133, 57-65
40. Samata, T., Kingsley, R. J., and Watabe, N. (1989) Ca-binding glycoprotein from the spicules of the octocoral Leptogorgia virgulata. Comp. Biochem. Physiol. B 94, 651-654
41. Goldberg, W. M. (1988) Chemistry, histochemistry, and microscopy of the organic matrix of spicules from a gorgonian coral. Histochem. Cell Biol. 89, 163-170
42. Rahman, A., Oomori, T., and Wörheide, G. (2011) Calcite formation in soft coral sclerites is determined by a single reactive extracellular protein. J. Biol. Chem. 286, 31638-31649
43. Fukuda, I., Ooki, S., Fujita, T., Murayama, E., Nagasawa, H., Isa, Y., and Watanabe, T. (2003) Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton. Biochem. Biophys. Res. Commun. 304, 11-17 (Pubitemid 36434186)
44. Tambutté, S., Tambutté, É., Zoccola, D., and Allemand, D. (2007) in Handbook of Biomineralization: The Biology of Biominerals Structure Formation (Baeuerlein, E., ed) pp. 243-259, Wiley-VCH, New York
45. Allemand, D., Tambutté, É., Zoccola, D., and Tambutté, S. (2011) in Coral Reefs: An Ecosystem in Transition (Dubinsky, Z., and Stambler, N., eds) pp. 119-150, Springer, The Netherlands
46. Tambutté, S., Holcomb, M., Ferrier-Pagès, C., Reynaud, S., Tambutté, É., Zoccola, D., and Allemand, D. (2011) Coral biomineralization: from the gene to the environment. J. Exp. Mar. Biol. Ecol. 408, 58-78
47. Debreuil, J., Tambutté, S., Zoccola, D., Segonds, N., Techer, N., Marschal, C., Allemand, D., Kosuge, S., and Tambutté, É. (2011) Specific organic matrix characteristics in skeletons of Corallium species. Mar. Biol. 158, 2765-2774
48. Puverel, S., Tambutté, E., Pereira-Mouriès, L., Zoccola, D., Allemand, D., and Tambutté, S. (2005) Soluble organic matrix of two scleractinian corals: partial and comparative analysis. Comp. Biochem. Physiol. B 141, 480-487 (Pubitemid 40982008)
49. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)
50. Zoccola, D., Tambutté, E., Sénégas-Balas, F., Michiels, J. F., Failla, J. P., Jaubert, J., and Allemand, D. (1999) Cloning of a calcium channel α1 subunit from the reef-building coral, Stylophora pistillata. Gene 227, 157-167 (Pubitemid 29104851)
51. Moya, A., Tambutté, S., Bertucci, A., Tambutté, E., Lotto, S., Vullo, D., Supuran, C. T., Allemand, D., and Zoccola, D. (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J. Biol. Chem. 283, 25475-25484
52. Jain, E., Bairoch, A., Duvaud, S., Phan, I., Redaschi, N., Suzek, B. E, Martin, M. J, McGarvey, P., and Gasteiger, E. (2009) Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 10, 136
53. Geer, L. Y., Marchler-Bauer, A., Geer, R. C., Han, L., He, J., He, S., Liu, C., Shi, W., and Bryant, S. H. (2010) The NCBI BioSystems database. Nucleic Acids Res. 38, D492-496
54. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat. Protocols 2, 953-971 (Pubitemid 46745592)
55. Horton, P., Park, K. J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., and Nakai, K. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587
56. Schägger, H. (2006) Tricine-SDS-PAGE. Nat. Protocols 1, 16-22
57. Kozak, M. (1984) Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 12, 857-872
58. Mankad, R. V., Gimelbrant, A. A., and McClintock, T. S. (1998) Consensus translational initiation sites of marine invertebrate phyla. Biol. Bull. 195, 251-254 (Pubitemid 29049784)
59. Weiner, S. (1986) Organization of extracellularly mineralized tissues: a comparative study of biological crystal growth. CRC Crit. Rev. Biochem. 20, 365-408
60. Treccani, L., Khoshnavaz, S., Blank, S., von Roden, K., Schulz, U., Weiss, I. M., Mann, K., Radmacher, M., and Fritz, H. M. (2005) in Biopolymers Online (Fahnestock, S. R., and Steinbüchel, A., eds) pp. 289-298, Wiley-VCH, New York
61. Ameye, L., De Becker, G., Killian, C., Wilt, F., Kemps, R., Kuypers, S., and Dubois, P. (2001) Proteins and saccharides of the sea urchin organic matrix of mineralization: characterization and localization in the spine skeleton. J. Struct. Biol. 134, 56-66
62. Luquet, G., and Marin, F. (2004) Biomineralisations in crustaceans: storage strategies. Comptes Rendus Palevol. 3, 515-534 (Pubitemid 39393732)
63. Mann, K., Poustka, A. J., and Mann, M. (2010) Phosphoproteomes of Strongylocentrotus purpuratus shell and tooth matrix: identification of a major acidic sea urchin tooth phosphoprotein, phosphodontin. Proteome Sci. 8, 1-14
64. Furuhashi, T., Schwarzinger, C., Miksik, I., Smrz, M., and Beran, A. (2009) Molluscan shell evolution with review of shell calcification hypothesis. Comp. Biochem. Physiol. B 154, 351-371
65. Borbas, J. E., Wheeler, A. P., and Sikes, C. S. (1991) Molluscan shell matrix phosphoproteins: correlation of degrees of phosphorylation to shell mineral microstructure and to in vitro regulation of mineralization. J. Exp. Zool. 258, 1-13
66. Hecker, A., Testenière, O., Marin, F., and Luquet, G. (2003) Phosphorylation of serine residues is fundamental for the calcium-binding ability of Orchestin, a soluble matrix protein from crustacean calcium storage structures. FEBS Lett. 535, 49-54 (Pubitemid 36126354)
67. Testenière, O., Hecker, A., Le Gurun, S., Quennedey, B., Graf, F., and Luquet, G. (2002) Characterization and spatiotemporal expression of orchestin, a gene encoding an ecdysone-inducible protein from a crustacean organic matrix. Biochem. J. 361, 327-335 (Pubitemid 34174499)
68. Sarashina, I., and Endo, K. (2001) The complete primary structure of molluscan shell protein 1 (MSP-1), an acidic glycoprotein in the shell matrix of the scallop Patinopecten yessoensis. Mar. Biotechnol. 3, 362-369 (Pubitemid 32925892)
69. Allemand, D., Tambutté, E., Girard, J. P., and Jaubert, J. (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin J. Exp. Biol. 201, 2001-2009 (Pubitemid 28338748)
70. Weiner, S., Traub, W., and Lowenstam, M. A. (1983) in Biomineralization and Biological Metal Accumulation (Westbrock, P., and De Jong, E. W., eds) pp. 205-224, Reidel Publishing Company, Dordrecht, The Netherlands
71. Kingsley, R. J., and Watabe, N. (1982) Ultrastructure of the axial region in Leptogorgia virgulata (Cnidaria: Gorgonaceae). Trans. Am. Microsc. Soc. 101, 325-339
72. Weiner, S., and Addadi, L. (1997) Design strategies in mineralized biological materials. J. Mater. Chem. 5, 689-702 (Pubitemid 127730043)
73. Marin, F., and Luquet, G. (2004) Molluscan shell proteins. Comptes Rendus Palevol. 3, 469-492 (Pubitemid 39379315)
74. Marie, B., Le Roy, N., Zanella-Cléon, I., Becchi, M., and Marin, F. (2011) Molecular evolution of mollusc shell proteins: insights from proteomic analysis of the edible mussel Mytilus. J. Mol. Evol. 72, 531-546
75. Marie, B., Trinkler, N., Zanella-Cleon, I., Guichard, N., Becchi, M., Paillard, C., and Marin, F. (2011) Proteomic identification of novel proteins from the calcifying shell matrix of the Manila clam Venerupis philippinarum. Mar. Biotechnol. 13, 955-962
76. Marie, B., Zanella-Cléon, I., Guichard, N., Becchi, M., and Marin, F. (2011) Novel proteins from the calcifying shell matrix of the Pacific oyster Crassostrea gigas. Mar. Biotechnol. 13, 1159-1168
77. Sethmann, I., Helbig, U., and Worheide, G. (2007) Octocoral sclerite ultrastructures and experimental approach to underlying biomineralisation principles. Cryst. Eng. Comm. 9, 1262-1268
78. Segev, N., Tokarev, A. A., and Alfonso, A. (2009) in Trafficking Inside Cells Pathways, Mechanisms, and Regulation (Segev, N., ed) pp. 1-12, Landes Bioscience and Springer Science+Business Media, New York
79. Capasso, J. M., Keenan, T. W., Abeijon, C., and Hirschberg, C. B. (1989) Mechanism of phosphorylation in the lumen of the Golgi apparatus: translocation of adenosine 5′-triphosphate into Golgi vesicles from rat liver and mammary gland. J. Biol. Chem. 264, 5233-5240 (Pubitemid 19092941)
80. Anitei, M., and Hoflack, B. (2011) Exit from the trans-Golgi network: from molecules to mechanisms. Curr. Opin. Cell Biol. 23, 443-451
81. Allemand, D., and Bénazet-Tambutté, S. (1996) Dynamics of calcification in the Mediterranean red coral, Corallium rubrum (Linnaeus) (Cnidaria, Octocorallia). J. Exp. Zool. 276, 270-278 (Pubitemid 27016713)
82. Marschal, C., Garrabou, J., Harmelin, J. G., and Pichon, M. (2004) A new method for measuring growth and age in the precious red coral Corallium rubrum (L.). Coral Reefs 23, 423-432 (Pubitemid 39320605)