Proteomic analysis of the organic matrix of the abalone Haliotis asinina calcified shell

Springer Science and Business Media LLC - Tập 8 - Trang 1-11 - 2010
Benjamin Marie1, Arul Marie2, Daniel J Jackson3, Lionel Dubost2, Bernard M Degnan4, Christian Milet5, Frédéric Marin1
1UMR 5561 CNRS Biogéosciences, Université de Bourgogne, Dijon, France
2Département RDDM, Plateforme de Spectrométrie de Masse et de Protéomique/FRE3206 CNRS, Molécules de Communication et Adaptations des Micro-organismes, M.N.H.N, Paris, France
3Courant Research Center Geobiology, Georg-August-University of Göttingen, Göttingen, Germany
4School of Biological Sciences, University of Queensland, Queensland, Australia
5UMR 7208 BOREA, M.N.H.N., Paris, France

Tóm tắt

The formation of the molluscan shell is regulated to a large extent by a matrix of extracellular macromolecules that are secreted by the shell forming tissue, the mantle. This so called "calcifying matrix" is a complex mixture of proteins and glycoproteins that is assembled and occluded within the mineral phase during the calcification process. While the importance of the calcifying matrix to shell formation has long been appreciated, most of its protein components remain uncharacterised. Recent expressed sequence tag (EST) investigations of the mantle tissue from the tropical abalone (Haliotis asinina) provide an opportunity to further characterise the proteins in the shell by a proteomic approach. In this study, we have identified a total of 14 proteins from distinct calcified layers of the shell. Only two of these proteins have been previously characterised from abalone shells. Among the novel proteins are several glutamine- and methionine-rich motifs and hydrophobic glycine-, alanine- and acidic aspartate-rich domains. In addition, two of the new proteins contained Kunitz-like and WAP (whey acidic protein) protease inhibitor domains. This is one of the first comprehensive proteomic study of a molluscan shell, and should provide a platform for further characterization of matrix protein functions and interactions.

Tài liệu tham khảo

Addadi L, Joester D, Nudelman F, Weiner S: Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem Rev 2006, 12: 980–987.

Shen X, Belcher AM, Hansma PK, Stucky GD, Morse DE: Molecular cloning and characterization of lustrin-A, a matrix protein from shell and pearl nacre of Haliotis rufescens . J Biol Chem 1997, 272: 32472–32481. 10.1074/jbc.272.51.32472

Mann K, Weiss IM, André S, Gabius HJ, Fritz M: The amino acid sequence of the abalone ( Haliotis laevigata ) nacre protein perlucin. Eur J Biochem 2000, 267: 5257–5264. 10.1046/j.1432-1327.2000.01602.x

Weiss IM, Göhring W, Fritz M, Mann K: Perlustrin, a Haliotis laevigata (abalone) nacre protein, is homologous to the insulin-like growth factor binding protein N-terminal module of vertebrates. Biochem Biophys Res Commun 2001, 285: 244–249. 10.1006/bbrc.2001.5170

Michenfelder M, Fu G, Lawrence C, Weaver JC, Wustman BA, Taranto L, Evans JS, Morse DE: Characterization of two molluscan crystal-modulating biomineralization proteins and identification of putative mineral binding domains. Biopolymers 2003, 70: 522–533. erratum in Biopolymers 2004, 73:291 10.1002/bip.10536

Treccani L, Mann K, Heinemann F, Fritz M: Perlwapin, an abalone nacre protein with three four-disulfide core (whey acidic protein) domains, inhibits the growth of calcium carbonate crystals. Biophys J 2006, 91: 2601–2608. 10.1529/biophysj.106.086108

Mann K, Siedler F, Treccani L, Heinemann F, Fritz M: Perlinhibin, a cysteine-, histidine-, and arginine-rich miniprotein from abalone ( Haliotis laevigata ) nacre, inhibits in vitro calcium carbonate crystallization. Biophys J 2007, 93: 1246–1254. 10.1529/biophysj.106.100636

Jackson DJ, McDougall C, Green KM, Simpson F, Wörheide G, Degnan BM: A rapidly evolving secretome builds and patterns a sea shell. BMC Biol 2006, 4: 40. 10.1186/1741-7007-4-40

Jackson DJ, Wörheide G, Degnan BM: Dynamic expression of ancient and novel molluscan shell genes during ecological transitions. BMC Evol Biol 2007, 7: 160. 10.1186/1471-2148-7-160

Jackson DJ, McDougall C, Woodcroft B, Moase P, Ross RA, Kube M, Reinhardrt R, Rokhsar DS, Montagnani C, Joubert C, Piquemal D, Degnan BM: Parallel evolution of nacre building gene sets in molluscs. Mol Biol Evol 2010, 27: 591–608. 10.1093/molbev/msp278

Marin F, Luquet G, Marie B, Medakovic D: Molluscan shell proteins: primary structure, origin, and evolution. Curr Top Dev Biol 2008, 80: 209–276. full_text

Marie B, Luquet G, Pais De Barros JP, Guichard N, Morel S, Alcaraz G, Bollache L, Marin F: The shell matrix of the unionid freshwater mussel Unio pictorum (Paleoheterodonta, Unionoida): Involvement of acidic polysaccharides from glycoproteins in nacre mineralization. FEBS J 2007, 274: 2933–2945. 10.1111/j.1742-4658.2007.05825.x

Mann K, Macek B, Olsen J: Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 2006, 6: 3801–3810. 10.1002/pmic.200600120

Marie B, Marin F, Marie A, Bédouet L, Dubost L, Alcaraz G, Milet C, Luquet G: Evolution of nacre: biochemistry and proteomics of the shell organic matrix of the cephalopod Nautilus macromphalus . ChemBioChem 2009, 10: 1495–1506. 10.1002/cbic.200900009

Barton S, Jacak R, Khare SD, Ding F, Dokholyan NV: The length dependence of the polyQ-mediated protein aggregation. J Biol Chem 2007, 282: 25487–25492. 10.1074/jbc.M701600200

Manoli F, Kanakis J, Malkaj P, Dalas E: The effect of amino acids on the crystal growth of calcium carbonate. J Crystal Growth 2002, 236: 363–370. 10.1016/S0022-0248(01)02164-9

Miyamoto H, Miyashita T, Okushima M, Nakano S, Morita T, Matsushiro A: A carbonic anhydrase from the nacreous layer in oyster pearls. Proc Natl Acad Sci 1996, 93: 9657–9660. 10.1073/pnas.93.18.9657

Sudo S, Fujikawa T, Nagakura T, Ohkubo T, Sakagushi K, Tanaka M, Nakashima K, Takahashi T: Structures of mollusc shell framework proteins. Nature 1997, 387: 563–564. 10.1038/42391

Sarashina I, Endo K: Primary structure of a soluble matrix protein of scallop shell: implications for calcium carbonate biomineralization. Am Mineral 1998, 83: 1510–1515.

Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H: An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 2009, 325: 1388–90. 10.1126/science.1173793

Korf I, Yandell M, Bedell J: BLAST. O'Reilly Media publisher; 2005:368.

Bédouet L, Duplat D, Marie A, Dubost L, Berland S, Rousseau M, Milet C, Lopez E: Heterogeneity of proteinase inhibitors in the water-soluble organic matrix from the oyster nacre. Mar Biotechnol 2007, 9: 437–449. 10.1007/s10126-007-7120-y

Liu HL, Liu SF, Ge YJ, Liu J, Wang XY, Xie LP, Zhang RQ, Wang Z: Identification and characterization of a biomineralization related gene PFMG1 highly expressed in the mantle of Pinctada fucata . Biochemistry 2007, 46: 844–851. 10.1021/bi061881a

Mann K, Poustka AJ, Mann M: The sea urchin ( Strongylocentrotus purpuratus ) test and spine proteomes. Proteome Science 2008, 6: 22. 10.1186/1477-5956-6-22

Mann K, Poustka AJ, Mann M: In-depth, high-accuracy proteomics of sea urchin tooth organic matrix. Proteome Science 2008, 6: 33. 10.1186/1477-5956-6-33

Yamakoshi Y: Dentinogenesis and dentin sialophosphoprotein (DSPP). J Oral Biosci 2009, 51: 134. 10.2330/joralbiosci.51.134

Gregorio-King CC, McLeod JL, Collier FM, Collier GR, Bolton KA, Van Der Meer GJ, Apostolopoulos J, Kirkland MA: MERP-1 : a mammalial ependymin-related protein gene differentially expressed in hematopoietic cells. Gene 2002, 286: 249–257. 10.1016/S0378-1119(02)00434-1

Ganss B, Hoffmann W: Calcium binding to sialic acids and its effect on the conformation of ependymins. Eur J Biochem 1993, 217: 275–280. 10.1111/j.1432-1033.1993.tb18243.x

Shashoua VE, Hesse GW, Milinazzo B: Evidence for the in vivo polymerization of ependymin: a brain extracellular glycoprotein. Brain Res 1990, 522: 181–190. 10.1016/0006-8993(90)91460-X

Esles JA, Lindberg DR, Wray C: Evolution of large body size in abalone ( Haliotis ): patterns and implications. Paleobiology 2005, 31: 591–606.

Takeuchi T, Endo K: Biphasic and dually coordinated expression of the genes encoding major shell matrix proteins in the pearl oyster Pinctada fucata . Mar Biotechnol 2006, 8: 52–61. 10.1007/s10126-005-5037-x

Miyazaki Y, Usui T, Kajikawa A, Hishiyama H, Matsuzawa N, Nishida T, Machii A, Samata T: Daily oscillation of gene expression associated with nacreous layer formation. Front Mater Sci China 2008, 2: 162–166. 10.1007/s11706-008-0027-3

Miyazaki YN, Nishida T, Aoki H, Samata T: Expression of genes responsible for biomineralization of Pinctada fucata during development. Comp Biochem Physiol B 2009, 155: 241–248. 10.1016/j.cbpb.2009.11.009

Mann K, Wilt F, Poustka AJ: Proteomic analysis of sea urchin ( Strongylocentrotus purpuratus ) spicule matrix. Proteome Science 2010, 8: 33. 10.1186/1477-5956-8-33

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