Abstract
Organic matrix from molluscan shells has the potential to regulate calcium carbonate deposition and crystallization. Control of crystal growth thus seems to depend on control of matrix protein secretion or activation processes in the mantle cells, about which little is known. Biomineralization is a highly orchestrated biological process. The aim of this work was to provide information about the source of shell matrix macromolecule production, within the external epithelium of the mantle. An in vivo approach was chosen to describe the histologic changes in the outer epithelium and in blood sinus distribution, associated with mantle cells implicated in shell matrix production. Our results characterized a topographic and time-dependent zonation of matrix proteins involved in shell biomineralization in the mantle of Haliotis.
Similar content being viewed by others
References
S. Albeck S. Weiner L Addadi (1996) ArticleTitlePolysaccharides of intracrystalline glycoproteins modulate calcite crystal growth in vitro Chem Eur J 2 278–284 Occurrence Handle1:CAS:528:DyaK28XhvVOrsbg%3D
M.J. Almeida C. Milet J. Peduzzi L. Pereira J. Haigle M. Barthelemy E Lopez (2000) ArticleTitleEffect of water-soluble matrix fraction extracted from the nacre of Pinctada maxima on the alkaline phosphatase activity of cultured fibroblasts J Exp Zool (Mol Dev Evol) 288 327–334 Occurrence Handle1:CAS:528:DC%2BD3cXovF2rtb0%3D
G. Atlan N. Balmain S. Berland B. Vidal E. Lopez (1997) ArticleTitleReconstruction of human maxillary defects with nacre powder: histological evidence for bone regeneration C R Acad Sci (Série III: Sciences de la vie) 320 253–258
G. Atlan O. Delattre S. Berland A. Le Faou G. Nabias D. Cot E Lopez (1999) ArticleTitleInterface between bone and nacre implants in sheep Biomaterials 20 1017–1022 Occurrence Handle1:CAS:528:DyaK1MXjt1yqsb0%3D Occurrence Handle10378801
L. Bedouet M.J. Schuller F. Marin C. Milet E. Lopez M Giraud (2001) ArticleTitleSoluble proteins of the nacre of the giant oyster Pinctada maxima and of the abalone Haliotis tuberculata: extraction and partial analysis of nacre proteins Comp Biochem Physiol 128 389–400 Occurrence Handle1:STN:280:DC%2BD3MzjvFCqtQ%3D%3D
A.M. Belcher X.H. Wu R.J. Christensen P.K. Hansma G.D. Stucky D.E Morse (1996) ArticleTitleControl of crystal phase switching and orientation by soluble mollusc-shell proteins Nature 381 56–58 Occurrence Handle1:CAS:528:DyaK28XislCrurY%3D
U. Bielefeld K.H. Körtje H. Rahmann W Becker (1993) ArticleTitleThe shell-forming mantle epithelium of Biomphalaria glabrata (Pulmonata): ultrastructure, permeability and cytochemistry J Molluscan Stud 59 323–338
Clavier J., Richard O. (1985). Etude sur les ormeaux dans la région de Saint-Malo. Association pour la mise en valeur du littoral de la côte d’Emeraude
M.A Crenshaw (1972) ArticleTitleThe soluble matrix from Mercenaria mercenaria shell Biomineralisation 6 6–11 Occurrence Handle1:CAS:528:DyaE2cXjsFWrsw%3D%3D
Y. Dauphin J.P. Cuif H. Mutvei A Denis (1989) ArticleTitleMineralogy, chemistry and ultrastructure of the external shell-layer in ten species of Haliotis with reference to Haliotis tuberculata (Mollusca: Archaeogastropoda) Bull Geol Inst Univ Uppsala NS 15 7–38
A Waele ParticleDe (1930) ArticleTitleIn: Mem Acad Roy de Belgique, classe des Sciences, t.X, . 31–51
G. Falini S. Albeck S. Weiner L Addadi (1996) ArticleTitleControl of aragonite or calcite polymorphism by mollusk shell macromolecules Science 271 67–69
Q.L. Feng G. Pu Y. Pei F.Z. Cui H.D. Li T.N Kim (2000) ArticleTitlePolymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell J Cryst Growth 216 459–465 Occurrence Handle1:CAS:528:DC%2BD3cXktlKltr4%3D
M. Fritz A.M. Belcher M. Radmacher G.D. Walters P.K. Hansma G.D. Stucky D.E. Morse S Mann (1994) ArticleTitleFlat pearls from biofabrication of organized composites on inorganic substrates Nature 371 49–51 Occurrence Handle1:CAS:528:DyaK2cXlslGlu70%3D
W.P.M Garaerts (1976) ArticleTitleControl of growth by the neuro-secretory hormone of the light green cells of the freshwater snail Lymnea stagnalis. Gen Comp Endocrinol 29 61–71 Occurrence Handle947221
S.J. Hattan T.M. Laue N.D Chasteen (2001) ArticleTitlePurification and characterization of a novel calcium-binding protein from the extrapallial fluid of the mollusc, Mytilus edulis J Biol Chem 276 IssueID6 4461–4468 Occurrence Handle1:CAS:528:DC%2BD3MXht1Gntr0%3D Occurrence Handle11084027
G.P. Hawkes R.W. Day M.W. Wallace K.W. Nugent A.A. Bettiol D.N. Jamieson M.C Williams (1996) ArticleTitleAnalyzing the growth and form of mollusc shell layers, in situ, by cathodoluminescence microscopy and Raman spectroscopy J Shellfish Res 15 IssueID3 659–666
I Kobayashi (1973) ArticleTitleData on the differential thermal analyses of bivalvian shells Bull Fossil Club Tokyo 7 1–4
M. Kono N. Hayashi T Samata (2000) ArticleTitleMolecular mechanisms of the nacreous layer formation in Pinctada maxima Biochem Biophys Res Commun 264 213–218
M. Lamghari M.J. Almeida S. Berland H. Huet A. Laurent C. Milet E Lopez (1999) ArticleTitleStimulation of bone marrow cells and bone formation by nacre: in vivo and in vitro studies Bone 25 91S–94S Occurrence Handle1:STN:280:DyaK1MzosFCltA%3D%3D Occurrence Handle10458284
E. Lopez B. Vidal S. Berland S. Camprasse G. Camprasse C Silve (1992) ArticleTitleDemonstration of the capacity of nacre to induce bone formation by human osteoblasts maintened in vitro Tissue Cell 24 667–679 Occurrence Handle1:STN:280:ByyD28bhvFE%3D Occurrence Handle1440586
E. Lopez S. Berland A Le Faou (1994) ArticleTitleNacre, osteogenic and osteoinductive properties Bull Inst Ocean Monaco 14 49–57
F. Marin P. Corstjens B. Gaulejac Particlede E. Vrind Jong ParticleDe P Westbroek (2000) ArticleTitleMucins and molluscan calcification: molecular characterization of mucoperlin, a novel mucin-like protein from the nacreous shell layer of the fan mussel Pinna nobilis (Bivalvia, Pteriomorpha) J Biol Chem 275 IssueID27 20667–20675 Occurrence Handle1:CAS:528:DC%2BD3cXkvVyhsbY%3D Occurrence Handle10770949
H. Miyamoto T. Miyashita M. Okushima S. Nakano T. Morita A Matsushiro (1996) ArticleTitleA carbonic anhydrase from the nacreous layer in oyster pearls Proc Natl Acad Sci USA 93 9657–9660 Occurrence Handle1:CAS:528:DyaK28XlsFeiu7s%3D Occurrence Handle8790386
F. Moutahir-Belqasmi N. Balmain M. Lieberrher S. Borzeix S. Berland M. Barthelemy J. Pedduzi C. Milet E Lopez (2001) ArticleTitleEffect of water soluble extract of nacre (Pinctada maxima) on alkaline phosphatase activity and Bcl-2 expression in primary cultured osteoblasts from neonatal rat calvaria J Mater Sci Mater Med 12 IssueID1 1–6 Occurrence Handle1:CAS:528:DC%2BD3MXht1Sltbo%3D Occurrence Handle15348370
H. Mutvei Y. Dauphin J.P Cuif (1985) ArticleTitleObservations sur l’organisation de la couche externe du test des Haliotis (Gastropoda): un cas exceptionnel de la variabilité minéralogique et microstructurale Bull Mus Nat Hist Nat Paris Ser 4 7 IssueID1 73–91
H. Nakahara M. Kakei G Bevelander (1981) ArticleTitleStudies on the formation of the crossed lamellar structure in the shell of Strombus gigas Veliger 23 IssueID3 207–211
A.S.M Saleuddin (1975) ArticleTitleAn electron microscopic study on the formation of the periostracum in Helisoma (Mollusca) Calc Tiss Res 18 297–310 Occurrence Handle1:STN:280:CSmD2c7jtFI%3D
A.S.M. Saleuddin (1976) Ultrastructural studies on the structure and formation of the periostracum in Helisoma (Mollusca) N. Watabe (Eds) The Mechanisms of Mineralization in the Invertebrates and Plants University of South Carolina Press . 309–337
T Samata (1990) ArticleTitleCa-binding glycoproteins in molluscan shells with different types of ultrastructure. Veliger 33 IssueID2 190–201
T. Samata N. Hayashi M. Kono K. Hasegawa C. Horita S Akera (1999) ArticleTitleA new matrix protein family related to the nacreous layer formation of Pinctada fucata FEBS 462 225–229 Occurrence Handle1:CAS:528:DyaK1MXnsVKlsbc%3D
T.E. Schäffer C. Ionesco-Zanetti R. Proksch M. Fritz D.A. Walters N. Almqvist C.M. Zaremba A.M. Belcher B.L. Smith G.D. Stucky D.E. Morse P.K Hansma (1997) ArticleTitleDoes abalone nacre form by heteroepitaxial nucleation or by growth trough mineral bridges ? Chem Mater 9 1731–1740
X. Shen A.M. Belcher P.K. Hansma G.D. Stucky D.E Morse (1997) ArticleTitleMolecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens J Biol Chem 272 IssueID51 32472–32481 Occurrence Handle1:CAS:528:DyaK1cXislWrtg%3D%3D Occurrence Handle9405458
K. Simkiss K.M. Wilbur (1987) Molluscs—epithelial control of matrix and minerals K. Simkiss K.M. Wilbur (Eds) Biomineralization: Cell Biology and Mineral Deposition Academic Press Inc. New york, N.Y. 230–260
D. Sud M. Auzoux-Bordenave M. Martin D. Doumenc (1998) Cell cultures from the abalone Haliotis tuberculata: a new tool for in vitro study of biomineralization . Le Gal Halverson (Eds) New Developments in Marine Biotechnology Plenum Press New York, N,Y. 165–170
D. Sud D. Doumenc E. Lopez C Milet (2001) ArticleTitleRole of water-soluble matrix fraction, extracted from the nacre of Pinctada maxima, in the regulation of cell activity in abalone mantle cell culture (Haliotis tuberculata) Tissue Cell 33 IssueID2 154–160 Occurrence Handle1:STN:280:DC%2BD3MzhvVKntg%3D%3D Occurrence Handle11392668
S. Sudo T. Fujikawa T. Nagakura T. Ohkubo K. Sakaguchi M. Tanaka K. Nakhashima T Takahashi (1997) ArticleTitleStructures of mollusc shell framework proteins Nature 387 563–564 Occurrence Handle1:CAS:528:DyaK2sXktFCisbc%3D
J.B. Thompson G.T. Paloczi J.H. Kindt M. Michenfelder B.L. Smith G.D. Stucky D.E. Morse P.K Hansma (2000) ArticleTitleDirect observation of the transition from calcite to aragonite growth as induced by abalone shell proteins Biophysics 79 3307–3312 Occurrence Handle1:CAS:528:DC%2BD3MXitFGm Occurrence Handle10.1016/S0006-3495(00)76562-3
L.P.M Timmermans (1969) ArticleTitleStudies on shell formation in molluscs Neth J Zool 19 417–523 Occurrence Handle1:CAS:528:DyaE3cXhtFyrtLs%3D
S. Weiner L Hood (1975) ArticleTitleSoluble protein of the organic matrix of mollusk shells: a potential template for shell formation Science 190 987–989 Occurrence Handle1:CAS:528:DyaE28Xls1Oisw%3D%3D Occurrence Handle1188379
S. Weiner M Traub (1984) ArticleTitleMacromolecules in mollusc shells and their functions in biomineralization Phil Trans R Soc Lond B 304 425–434 Occurrence Handle1:CAS:528:DyaL2cXhvV2iu7g%3D
I.M. Weiss S. Kaufmann K. Mann M Fritz (2000) ArticleTitlePurification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata Biochem Biophys Res Commun 267 17–21 Occurrence Handle1:CAS:528:DC%2BD3cXht1Gguw%3D%3D Occurrence Handle10623567
I.M. Weiss W. Göhring M. Fritz K Mann (2001) ArticleTitlePerlustrin, a Haliotis laevigata (abalone) nacre protein, is homologous to the insuline-like growth factor binding protein N-terminal module of verebrates Biochem Biophys Res Commun 285 244–249 Occurrence Handle1:CAS:528:DC%2BD3MXkvFOqsrw%3D Occurrence Handle11444832
K.M. Wilbur (1964) Shell formation and regeneration K.M. Wilbur C.M. Yonge (Eds) Physiology of Mollusca Academic Press New york, N.Y. 243–282
C.M. Zaremba A.M. Belcher M. Fritz Y. Li S. Mann P.K. Hansma D.E. Morse J.S. Speck G.D. Stucky (1996) ArticleTitleCritical transitions in the biofabrication of abalone shells and flat pearls Chem Mater 8 IssueID3 679–690 Occurrence Handle1:CAS:528:DyaK28Xht1Wjt7o%3D
Acknowledgments
The authors thank SMEL (Syndicat Mixte de 1’Equipement du Littoral, Blainville sur mer, France) for supplying the animals according to our requirements. Thanks are also due to Mrs. Francine Lallier for editing the text.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jolly, C., Berland, S., Milet, C. et al. Zona Localization of Shell Matrix Proteins in Mantle of Haliotis tuberculata (Mollusca, Gastropoda). Mar Biotechnol 6, 541–551 (2004). https://doi.org/10.1007/s10126-004-3129-7
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10126-004-3129-7