Abstract
The shells of molluscs are composed mainly of calcium carbonate crystals, with small amounts of matrix proteins. For more than 50 years, they have attracted attention for their unique mechanical and biological properties. Only recently, however, have researchers begun to realize that it is the matrix proteins that control the formation of calcium carbonate crystals and play key roles in their extraordinary properties, despite the fact that matrix proteins comprise less than 5% of the shell weight. This article reviews the matrix proteins identified to date from the shells of molluscs, their structural characteristics, and their roles in shell formation. Some suggestions are given for further investigation based on the summary and analysis.
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References
L Addadi S Weiner (1985) ArticleTitleInteractions between acidic proteins and crystals: stereochemical requirements in biomineralization Proc Natl Acad Sci USA 82 4110–4114
S Albeck J Aizenberg L Addadi S Weiner (1993) ArticleTitleInteractions of various skeletal intracrystalline components with calcite crystals J Am Chem Soc 115 11691–11697
MJ 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 288 327–334
MJ Almeida L Pereira C Milet J Haigle M Barbosa E Lopez (2001) ArticleTitleComparative effects of nacre water-soluble matrix and dexamethasone on the alkaline phosphatase activity of MRC-5 fibroblasts J Biomed Mater Res 57 306–312
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 Paris 320 253–258
G Atlan O Delattre S Berland A LeFaou G Nabias D Cot E Lopez (1999) ArticleTitleInterface between bone and nacre implants in sheep Biomaterials 20 1017–1022
L Bedouet MJ 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 128B 389–400
AM Belcher XH Wu RJ Christensen PK Hansma GD Stucky DE Morse (1996) ArticleTitleControl of crystal phase switching and orientation by soluble mollusc-shell proteins Nature 381 56–58
G Bevelander H Nakahara (1969) ArticleTitleAn electron microscopic study of the formation of the nacreous layer in the shell of certain bivalve mollusks Calcif Tissue Res 3 84–92
G Bevelander H Nakahara (1980) Compartment and envelope formation in the process of biological mineralization M Omori N Watabe (Eds) The Mechanisms of Biomineralization in Animals and Plants Tokai University Press Tokyo 19–27
S Blank M Arnoldi S Khoshnavaz L Treccani M Kuntz K Mann G Grathwohl M Fritz (2003) ArticleTitleThe nacre protein perlucin nucleates growth of calcium carbonate crystals J Microsc 212 280–291
JE Borbas AP Wheeler CS Sikes (1991) ArticleTitleMolluscan shell matrix phosphoproteins: correlation of degree of phosphorylation to shell mineral microstructure and to in vitro regulation of mineralization J Exp Zool 258 1–13
P Bork (1991) ArticleTitleShuffled domains in extracellular proteins FEBS Lett 286 47–54
V Boulo JP Cadoret F LeMarrec G Dorange E Mialhe (1996) ArticleTitleTransient expression of luciferase reporter gene after lipofection in oyster (Crassostrea gigas) primary cell cultures Mol Mar Biol Biotech 5 167–174
V Boulo JP Cadoret H Shike C Shimizu A Miyanohara JC Burns (2000) ArticleTitleInfection of cultured embryo cells of the Pacific oyster, Crassostrea gigas, by pantropic retroviral vectors In Vitro Cell Dev Anim 36 395–399
CE Bowen H Tang (1996) ArticleTitleConchiolin-protein in aragonite shells of mollusks Comp Biochem Physiol 115A 269–275
JT Buchanan AD Nickens RK Cooper TR Tiersch (2001a) ArticleTitleTransfection of eastern oyster (Crassostrea virginica) embryos Mar Biotechnol 3 322–335
JT Buchanan TC Cheng JF Peyre ParticleLa RK Cooper TR Tiersch (2001b) ArticleTitleIn vivo transfection of adult eastern oysters Crassostrea virginica J World Aquacult Soc 32 286–299
JP Cadoret R Debon L Cornudella V Lardans A Morvan P Roch V Boulo (1999) ArticleTitleTransient expression assays with the proximal promoter of a newly characterized actin gene from the oyster Crassostrea gigas FEBS Lett 460 81–85
MA Cariolou DE Morse (1988) ArticleTitlePurification and characterization of calcium-binding conchiolin shell peptides from the mollusc, Haliotis rufescens, as a function of development J Comp Physiol 157B 717–729
MA Crenshaw (1972) ArticleTitleThe inorganic composition of molluscan extrapallial fluid Biol Bull 143 506–512
MA Crenshaw (1980) Mechanisms of shell formation and dissolution DC Rhoads RA Lutz (Eds) Skeletal Growth of Aquatic Organisms: Biological Records of Environmental Change Plenum Press New York 115–132
JD Currey (1999) ArticleTitleThe design of mineralized hard tissues for their mechanical functions J Exp Biol 202 3285–3294
KJ Davis PM Dove JJ Yoreo (2000) ArticleTitleThe role of Mg2+ as an impurity in calcite growth Science 290 1134–1137
JE Donachy B Drake CS Sikes (1992) ArticleTitleSequence and atomic force microscopy analysis of a matrix protein from the shell of the oyster Crassostrea virginica Mar Biol 114 423–428
J Engel (1991) ArticleTitleCommon structural motifs in proteins of the extracellular matrix Curr Opin Cell Biol 3 779–785
J Engel (1996) ArticleTitleDomain organizations of modular extracellular matrix proteins and their evolution Matrix Biol 15 295–299
G Falini S Albeck S Weiner L Addadi (1996) ArticleTitleControl of aragonite or calcite polymorphism by mollusk shell macromolecules Science 271 67–69
QL Feng G Pu Y Pei FZ Cui HD Li TN Kim (2000) ArticleTitlePolymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell J Cryst Growth 216 459–465
ME Fremy (1855) ArticleTitleRecherches chimiques sur les os Ann Chim Phys 43 47–107
M Fritz DE Morse (1998) ArticleTitleThe formation of highly organized biogenic polymer/ceramic composite materials: the high performance microaluminate of molluscan nacre Curr Opin Colloid Interface Sci 3 55–62 Occurrence Handle10.1016/S1359-0294(98)80042-3
M Fritz AM Belcher M Radmacher DA Walters PK Hansma GD Stucky DE Morse S Mann (1994) ArticleTitleFlat pearls from biofabrication of organized composites on inorganic substrates Nature 371 49–51
G Fu S Valiyaveettil B Wopenka DE Morse (2005) ArticleTitleCaCO3 biomineralization: acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology Biomacromolecules 6 1289–1298
JP Gorski (1992) ArticleTitleAcidic phosphoproteins from bone matrix: a structural rationalization of their role in biomineralization Calc Tissue Int 50 391–396
BA Gotliv N Kessler JL Sumerel DE Morse N Tuross L Addadi S Weiner (2005) ArticleTitleAsprich: a novel aspartic acid-rich protein family from the prismatic shell matrix of the bivalve Atrina rigida Chembiochem 6 304–314
C Gregoire G Duchateau M Florkin (1955) ArticleTitleLa trame protidique des nacres et des perles Ann Inst Oceanogr Monaco 31 1–36
PA Guerette DG Ginzinger BHF Weber JM Gosline (1996) ArticleTitleSilk properties determined by gland-specific expression of a spider fibroin gene family Science 272 112–115
BA Halloran JE Donachy (1995) ArticleTitleCharacterization of organic matrix macromolecules from the shell of the Antarctic scallop, Adamussium colbecki Comp Biochem Physiol 111B 221–231
EL Hansen (1976) A cell line from embryos of Biomphalaria glabrata (Pulmonata) establishment and characteristics K Maramorosch (Eds) Invertebrate Tissue Culture: Research Applications Academic Press New York 75–97
SJ Hattan TM Laue ND Chasteen (2000) ArticleTitlePurification and characterization of a novel calcium-binding protein from the extrapallial fluid of the mollusc, Mytilus edulis J Biol Chem 276 4461–4468
H Hutter BE Vogel JD Plenefisch CR Norris RB Proenca J Spieth C Guo S Mastwal XP Zhu J Scheel EM Hedgecock (2000) ArticleTitleConservation and novelty in the evolution of cell adhesion and extracellular matrix genes Science 287 989–994
AP Jackson JFV Vincent RM Turner (1988) ArticleTitleThe mechanical design of nacre Proc R Soc Lond 234B 415–440
S Kamat X Su R Ballarini AH Heuer (2000) ArticleTitleStructural basis for the fracture toughness of the shell of the conch Strombus gigas Nature 405 1036–1040
DL Kaplan (1998) ArticleTitleMollusc shell structures: novel design strategies for synthetic materials Curr Opin Solid-State Mater Sci 3 232–236
J Keith S Stockwell D Ball K Remillard D Kaplan T Thannhauser R Sherwood (1993) ArticleTitleComparative analysis of macromolecules in mollusc shells Comp Biochem Physiol 105B 487–496
IW Kim DE Morse JS Evans (2004a) ArticleTitleMolecular characterization of the 30-AA N-terminal mineral interaction domain of the biomineralization protein AP7 Langmuir 20 11664–11673
IW Kim E DiMasi JS Evans (2004b) ArticleTitleIdentification of mineral modulation sequences within the nacre-associated oyster shell protein, n16 Cryst Growth Des 4 1113–1118
M Kono N Hayashi T Samata (2000) ArticleTitleMolecular mechanism of the nacreous layer formation in Pinctada maxima Biochem Biophys Res Commun 269 213–218
N Kroger C Bergsdorf M Sumper (1994) ArticleTitleA new calcium binding glycoprotein family constitutes a major diatom cell wall component EMBO J 13 4676–4683
N Kroger C Bergsdorf M Sumper (1996) ArticleTitleFrustulins: domain conservation in a protein family associated with diatom cell walls Eur J Biochem 239 259–264
M Lamghari MJ 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 25S 91S–94S
K Lewandowska HU Choi LC Rosenberg J Sasse PJ Neame LA Culp (1991) ArticleTitleExtracellular matrix adhesion-promoting activities of a dermatan sulfate proteoglycan-associated protein (22K) from bovine fetal skin J Cell Sci 99 657–668
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 maintained in vitro Tissue Cell 24 667–679
JR MacBeath DR Shackleton DJ Hulmes (1993) ArticleTitleTyrosine-rich acidic matrix protein (TRAMP) accelerates collagen fibril formation in vitro J Biol Chem 268 19826–19832
S Mann (1988) ArticleTitleMolecular recognition in biomineralization Nature 332 119–124
K Mann IM Weiss S Andre HJ Gabius M Fritz (2000) ArticleTitleThe amino-acid sequence of the abalone (Haliotis laevigata) nacre protein perlucin: detection of a functional C-type lectin domain with galactose/mannose specificity Eur J Biochem 267 5257–5264
F Marin G Luquet (2004) ArticleTitleMolluscan shell proteins C R Palevol 3 469–492
F Marin M Smith Y Isa G Muyzer P Westbroek (1996) ArticleTitleSkeletal matrices, muci, and the origin of invertebrate calcification Proc Natl Acad Sci USA 93 1554–1559
F Marin P Corstjens B Gaulejac Particlede E deVrind-De Jong 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, Pteriomorphia) J Biol Chem 275 20667–20675
F Marin L Pereira P Westbroek (2001) ArticleTitleLarge-scale fractionation of molluscan shell matrix Protein Expr Purif 23 175–179
F Marin K Groot Particlede P Westbroek (2003) ArticleTitleScreening molluscan cDNA expression libraries with anti-shell matrix antibodies Protein Expr Purif 30 246–252
F Marin R Amons N Guichard M Stigter A Hecker G Luquet P Layrolle G Alcaraz C Riondet P Westbroek (2005) ArticleTitleCaspartin and calprismin, two new proteins of the shell calcitic prisms of the Mediterranean fan mussel Pinna nobilis J Biol Chem 280 33895–33908
JC Marxen W Becker (1997) ArticleTitleThe organic shell matrix of the freshwater snail Biomphalaria glabrata Comp Biochem Physiol 118B 23–33
JC Marxen W Becker (2000) ArticleTitleCalcium binding constituents of the organic shell matrix from the freshwater snail Biomphalaria glabrata Comp Biochem Physiol 127B 235–242
JC Marxen M Hammer T Gehrke W Becker (1998) ArticleTitleCarbohydrate of the organic shell matrix and the shell-forming tissue of the snail Biomphalaria glabrata Biol Bull 194 231–240
JC Marxen M Nimtz W Becker K Mann (2003) ArticleTitleThe major soluble 19.6-kDa protein of the organic shell matrix of the freshwater snail Biomphalaria glabrata is an N-glycosylated dermatopontin Biochim Biophys Acta 1650 92–98
A Matsushiro T Miyashita (2004) ArticleTitleEvolution of hard-tissue mineralization: comparison of the inner skeletal system and the outer shell system J Bone Miner Metab 22 163–169
A Matsushiro T Miyashita H Miyamoto K Morimoto B Tonomura A Tanaka K Sato (2003) ArticleTitlePresence of protein complex is prerequisite for aragonite crystallization in the nacreous layer Mar Biotechnol 5 37–44
M Michenfelder G Fu C Lawrence JC Weaver BA Wustman L Taranto JS Evans DE Morse (2003) ArticleTitleCharacterization of two molluscan crystal-modulating biomineralization proteins and identification of putative mineral binding domains Biopolymers 70 522–533
MJ Misogianes ND Chasteen (1979) ArticleTitleA chemical and spectral characterization of the extrapallial fluid of Mytilus edulis Anal Biochem 100 324–334
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
H Miyamoto M Hamaguchi K Okoshi (2002) ArticleTitleAnalysis of genes expressed in the mantle of oyster Crassostrea gigas Fisher Sci 68 651–658
H Miyamoto M Yano T Miyashita (2003) ArticleTitleSimilarities in the structure of nacrein, the shell-matrix protein, in a bivalve and a gastropod J Moll Stud 69 87–89
H Miyamoto F Miyoshi J Kohno (2005) ArticleTitleThe carbonic anhydrase domain protein nacrein is expressed in the epithelial cells of the mantle and acts as a negative regulator in calcification in the mollusc Pinctada fucata Zool Sci 22 311–315
T Miyashita R Takagi M Okushima S Nakano H Miyamoto E Nishikawa A Matsushiro (2000) ArticleTitleComplementary DNA cloning and characterization of pearlin, a new class of matrix protein in the nacreous layer of oyster pearls Mar Biotechnol 2 409–418
T Miyashita Y Takagi H Miyamoto A Matsushiro (2002) ArticleTitleIdentical carbonic anhydrase contributes to nacreous or prismatic layer formation in Pinctada fucata (Mollusca Bivalvia) Veliger 45 250–255
AS Mount AP Wheeler RP Paradkar D Snider (2004) ArticleTitleHemocyte-mediated shell mineralization in the eastern oyster Science 304 297–300
G Moura L Vilarinho AC Santos J Machado (2000) ArticleTitleOrganic compounds in the extrapallial fluid and haemolymph of Anodonta cygnea (L.) with emphasis on the seasonal biomineralization process Comp Biochem Physiol 125B 293–306
LP Mouries MJ Almeida C Milet S Berland E Lopez (2002) ArticleTitleBioactivity of nacre water-soluble organic matrix from the bivalve mollusk Pinctada maxima in three mammalian cell types: fibroblasts, bone marrow stromal cells and osteoblasts Comp Biochem Physiol 132B 217–229
F Moutahir-Belqasmi N Balmain M Lieberrher S Borzeix S Berland M Barthelemy J Peduzzi 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 1–6
H Nakahara (1991) Nacre formation in bivalve and gastropod mollusks S Suga H Nakahara (Eds) Mechanism and Phylogeny of Mineralization in Biological Systems Springer-Verlag Tokyo 343–350
H Nakahara M Kakei G Bevelander (1980) ArticleTitleFine structure and amino acid composition of the organic envelope in the prismatic layer of some bivalve shells Venus (Jap J Malac) 39 167–177
H Nakahara G Bevelander M Kakei (1982) ArticleTitleElectron microscopic and amino acid studies on the outer and inner shell layers of Haliotis rufescens Venus (Jap J Malac) 41 33–46
O Okamoto Y Suzuki S Kimura H Shinkai (1996) ArticleTitleExtracellular matrix 22-kDa protein interacts with decorin core protein and is expressed in cutaneous fibrosis J Biochem 119 106–114
O Okamoto S Fujiwara M Abe Y Sato (1999) ArticleTitleDermatopontin interacts with transforming growth factor beta and enhances its biological activity Biochem J 337 537–541
A Oldberg A Franzen D Heinegard (1986) ArticleTitleCloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence Proc Natl Acad Sci USA 83 8819–8823
L Patthy (1996) ArticleTitleExon shuffling and other ways of module exchange Matrix Biol 15 301–310
L Patthy (1999) ArticleTitleGenome evolution and the evolution of exon shuffling—A review Gene 238 103–114
L Patthy (2003) ArticleTitleModular assembly of genes and the evolution of new functions Genetica 118 217–231
JE Pietrzak JM Bates RM Scott (1973) ArticleTitleConstituents of unionid extrapallial fluid. I. Electrophoretic and immunological studies of protein components Biol Bull 144 391–399
M Rousseau L Pereira-Mouries MJ Almeida C Milet E Lopez (2003) ArticleTitleThe water-soluble matrix fraction from the nacre of Pinctada maxima produces earlier mineralization of MC3T3-E1 mouse pre-osteoblasts Comp Biochem Physiol 135B 1–7
M Rubner (2003) ArticleTitleMaterials science: synthetic sea shell Nature 423 925–926
KW Rusenko JE Donachy AP Wheeler (1991) Purification and characterization of a shell matrix phosphoprotein from the American oyster CS Sikes AP Wheeler (Eds) Surface Reactive Peptides and Polymers: Discovery and Commercialization ACS Symposium Series 444 Washington, DC 107–124
B Sabsay WG Stetler-Stevenson JH Lechner A Veis (1991) ArticleTitleDomain structure and sequence distribution in dentin phosphophoryn Biochem J 276 699–707
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 Lett 462 225–229
I Sarashina K Endo (1998) ArticleTitlePrimary structure of a soluble matrix protein of scallop shell: implications for calcium carbonate biomineralization Am Mineralogist 83 1510–1515
I Sarashina K Endo (2001) ArticleTitleThe complete primary structure of Molluscan Shell Protein-1 (MSP-1), an acidic glycoprotein in the shell matrix of scallop Painopecten yessoensis Mar Biotechnol 3 362–369
A Sellinger PM Weiss A Nguyen Y Lu RA Assink W Gong CJ Brinker (1998) ArticleTitleContinuous self-assembly of organic-inorganic nanocomposite coatings that mimic nacre Nature 394 256–260
X Shen AM Belcher PK Hansma GD Stucky DE Morse (1997) ArticleTitleMolecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens J Biol Chem 272 32472–32481
DW Shin J Ma DH Kim (2000) ArticleTitleThe asp-rich region at the carboxyl-terminus of calsequestrin binds to Ca(2+) and interacts with triadin FEBS Lett 486 178–182
C Silve E Lopez B Vidal DC Smith S Camprasse G Camprasse G Couly (1992) ArticleTitleNacre initiates biomineralization by human osteoblasts maintained in vitro Calcif Tissue Int 51 363–369
K Simkiss (1965) ArticleTitleThe organic matrix of the oyster shell Comp Biochem Physiol 16 427–435
BL Smith TE Schaffer M Viani JB Thompson NA Frederick J Kindt A Belcher GD Stucky DE Morse PK Hansma (1999) ArticleTitleMolecular mechanistic origin of the toughness of natural adhesives, fibres and composites Nature 399 761–763
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 33 154–160
S Sudo T Fujikawa T Nagakura T Ohkubo K Sakaguchi M Tanaka K Nakashima T Takahashi (1997) ArticleTitleStructure of mollusk shell framework proteins Nature 387 563–564
M Suzuki E Murayama H Inoue N Ozaki H Tohse T Kogure H Nagasawa (2004) ArticleTitleCharacterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster, Pinctada fucata Biochem J 382 205–213
U Takeda A Utani J Wu E Adachi H Koseki M Taniguchi T Matsumoto T Ohashi M Sato H Shinkai (2002) ArticleTitleTargeted disruption of dermatopontin causes abnormal collagen fibrillogenesis J Invest Dermatol 119 678–683
Z Tang NA Kotov S Magonov B Ozturk (2003) ArticleTitleNanostructured artificial nacre Nat Mater 2 413–418
JB Thompson GT Paloczi JH Kindt M Michenfelder BL Smith G Stucky DE Morse PK Hansma (2000) ArticleTitleDirect observation of the transition from calcite to aragonite growth as induced by abalone shell proteins Biophys J 79 3307–3312 Occurrence Handle10.1016/S0006-3495(00)76562-3
D Tsukamoto I Sarashina K Endo (2004) ArticleTitleStructure and expression of an unusually acidic matrix protein of pearl oyster shells Biochem Biophys Res Commun 320 1175–1180
A Veis B Sabsay CB Wu (1991) Phosphoproteins as mediators of biomineralization CS Sikes AP Wheeler (Eds) Surface Reactive Peptides and Polymers: Discovery and Commercialization ACS Symposium Series 444 Washington, DC 72–84
K Wada T Fujinuki (1974) Biomineralization in bivalve molluscs with emphasis on the chemical composition of the extrapallial fluid N Watabe KM Wilbur (Eds) The Mechanisms of Mineralization in the Invertebrates and Plants South Carolina University Press Columbia 457–496
N Watabe KM Wilbur (1960) ArticleTitleInfluence of the organic matrix on crystal type in mollusks Nature 188 334
S Weiner (1979) ArticleTitleAspartic acid-rich proteins: major components of the soluble organic matrix of mollusk shell Calcif Tissue Int 29 163–167
S Weiner (1983) ArticleTitleMollusk shell formation: isolation of two organic matrix proteins associated with calcite deposition in the bivalve Mytilus californianus Biochemistry 22 4139–4145
S Weiner L Hood (1975) ArticleTitleSoluble protein of the organic matrix of mollusk shells: a potential template for shell formation Science 190 987–988
S Weiner W Traub (1980) ArticleTitleX-ray diffraction study of the insoluble organic matrix of mollusc shells FEBS Lett 111 311–316
S Weiner HA Lowenstam L Hood (1977) ArticleTitleDiscrete molecular weight components of the organic matrices of mollusk shells J Exp Mar Biol Ecol 30 45–51
IM Weiss S Kaufmann K Mann M Fritz (2000) ArticleTitlePurification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusk Haliotis laevigata Biochem Biophys Res Commun 267 17–21
IM Weiss W Göhring M Fritz K Mann (2001) ArticleTitlePerlustrin, 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 285 244–249
IM Weiss N Tuross L Addadi S Weiner (2002) ArticleTitleMollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite J Exp Zool 293 478–491
P Westbroek F Marin (1998) ArticleTitleA marriage of bone and nacre Nature 392 861–862
AP Wheeler (1992) Phosphoproteins of oyster (Crassostrea virginica) shell organic matrix S Suga N Watabe (Eds) Hard Tissue Mineralization and Demineralization Springer-Verlag Tokyo 171–187
AP Wheeler CS Sikes (1984) ArticleTitleRegulation of carbonate calcification by organic matrix Am Zool 24 933–944
AP Wheeler KW Rusenko JW George CS Sikes (1987) ArticleTitleEvaluation of calcium binding by molluscan shell organic matrix and its relevance to biomineralization Comp Biochem Physiol 87B 953–960
AP Wheeler KW Rusenko DM Swift CS Sikes (1988) ArticleTitleRegulation of in vitro and in vivo CaCO3 crystallization by fractions of oyster shell organic matrix Mar Biol 98 71–80
AP Wheeler KC Low CS Sikes (1991) CaCO3 crystal-binding properties of peptides and their influence on crystal growth CS Sikes AP Wheeler (Eds) Surface Reactive Peptides and Polymers: Discovery and Commercialization ACS Symposium Series 444 Washington, DC 72–84
KM Wilbur LH Jodrey (1952) ArticleTitleStudies on shell formation. I: Measurement of the rate of shell formation using Ca45 Biol Bull 103 269–276
KM Wilbur N Watabe (1963) ArticleTitleExperimental studies on calcification in mollusks and the alga Cocolithus huxleyi Ann NY Acad Sci 109 82–112
FH Wilt CE Killian BT Livingston (2003) ArticleTitleDevelopment of calcareous skeletal elements in invertebrates Differentiation 71 237–250
BA Wustman DE Morse JS Evans (2002) ArticleTitleStructural analyses of polyelectrolyte sequence domains within the adhesive elastomeric biomineralization protein lustrin A Langmuir 18 9901–9906
BA Wustman JC Weaver DE Morse JS Evans (2003) ArticleTitleCharacterization of a Ca(II)-, mineral-interactive polyelectrolyte sequence from the adhesive elastomeric biomineralization protein lustrin A Langmuir 19 9373–9381
BA Wustman DE Morse JS Evans (2004) ArticleTitleStructural characterization of the N-terminal mineral modification domains from the molluscan crystal-modulating biomineralization proteins, AP7 and AP24 Biopolymers 74 363–376
K Yano A Zarain-Herzberg (1994) ArticleTitleSarcoplasmic reticulum calsequestrins: structural and functional properties Mol Cell Biochem 135 61–70
Y Yin J Huang ML Paine VN Reinhold ND Chasteen (2005) ArticleTitleStructural characterization of the major extrapallial fluid protein of the mollusc Mytilus edulis: implications for functions Biochemistry 44 10720–10731
T Yonezawa Y Furuhata K Hirabayashi M Suzuki M Takahashi M Nishihara (2001) ArticleTitleDetection of transgene in progeny at different developmental stages following testis-mediated gene transfer Mol Reprod Dev 60 196–201
CM Zaremba AM Belcher M Fritz Y Li S Mann PK Hansma DE Morse JS Speck GD Stucky (1996) ArticleTitleCritical transitions in the biofabrication of abalone shells and flat pearls Chem Mater 8 679–690
B Zhang BA Wustman D Morse JS Evans (2002) ArticleTitleModel peptide studies of sequence regions in the elastomeric biomineralization protein, lustrin A. I. The C-domain consensus-PG-, -NVNCT-motif Biopolymers 63 358–369
Y Zhang L Xie Q Meng T Jiang R Pu L Chen R Zhang (2003) ArticleTitleA novel matrix protein participating in the nacre framework formation of pearl oyster, Pinctada fucata Comp Biochem Physiol 135B 565–573
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Zhang, C., Zhang, R. Matrix Proteins in the Outer Shells of Molluscs. Mar Biotechnol 8, 572–586 (2006). https://doi.org/10.1007/s10126-005-6029-6
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DOI: https://doi.org/10.1007/s10126-005-6029-6