Characterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster (<i>Pinctada fucata</i>)

Suzuki, Michio; Murayama, Emi; Inoue, Hirokazu; Ozaki, Noriaki; Tohse, Hidekazu; Kogure, Toshihiro; Nagasawa, Hiromichi

doi:10.1042/bj20040319

Cited by 187 publications

(153 citation statements)

References 25 publications

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“…A probable relationship between the chemical features of biomolecules and crystal growth control is supported by many observations showing that proteins isolated from sites of biomineralization in tissues are unusually enriched in highly acidic amino acids, notably aspartic acid and also glutamic acid (9)(10)(11)(12)(13). The Asp-rich motifs have been postulated to function by preferentially binding to cations such as Ca 2ϩ (14) during the controlled formation of minerals such as calcite (12).…”

mentioning

confidence: 75%

“…The Asp-rich motifs have been postulated to function by preferentially binding to cations such as Ca 2ϩ (14) during the controlled formation of minerals such as calcite (12). Under physiological conditions, the carboxyl groups of aspartic acid are negatively charged and are believed to engage in electrostatic interactions with Ca 2ϩ ions at the nascent crystal surface (15).…”

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confidence: 99%

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Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth

Elhadj

Yoreo

Hoyer

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

239

323

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The composition of biologic molecules isolated from biominerals suggests that control of mineral growth is linked to biochemical features. Here, we define a systematic relationship between the ability of biomolecules in solution to promote the growth of calcite (CaCO 3) and their net negative molecular charge and hydrophilicity. The degree of enhancement depends on peptide composition, but not on peptide sequence. Data analysis shows that this rate enhancement arises from an increase in the kinetic coefficient. We interpret the mechanism of growth enhancement to be a catalytic process whereby biomolecules reduce the magnitude of the diffusive barrier, E k, by perturbations that displace water molecules. The result is a decrease in the energy barrier for attachment of solutes to the solid phase. This previously unrecognized relationship also rationalizes recently reported data showing acceleration of calcite growth rates over rates measured in the pure system by nanomolar levels of abalone nacre proteins. These findings show that the growth-modifying properties of small model peptides may be scaled up to analyze mineralization processes that are mediated by more complex proteins. We suggest that enhancement of calcite growth may now be estimated a priori from the composition of peptide sequences and the calculated values of hydrophilicity and net molecular charge. This insight may contribute to an improved understanding of diverse systems of biomineralization and design of new synthetic growth modulators.biomineral ͉ calcite ͉ proteins

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mentioning

confidence: 75%

mentioning

confidence: 99%

Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth

Elhadj

Yoreo

Hoyer

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

239

323

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“…Calculations of γ assume rhombohedral nuclei. The interfacial tension 23 of calcite in solution is ∼110 mJ m −2 . Finally, these findings unlock the secret to the success of methods that identify template molecules through binding assays.…”

Section: Significancementioning

confidence: 99%

Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies

Hamm

Giuffre

Han

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

128

173

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The physical basis for how macromolecules regulate the onset of mineral formation in calcifying tissues is not well established. A popular conceptual model assumes the organic matrix provides a stereochemical match during cooperative organization of solute ions. In contrast, another uses simple binding assays to identify good promoters of nucleation. Here, we reconcile these two views and provide a mechanistic explanation for template-directed nucleation by correlating heterogeneous nucleation barriers with crystal-substrate-binding free energies. We first measure the kinetics of calcite nucleation onto model substrates that present different functional group chemistries (carboxyl, thiol, phosphate, and hydroxyl) and conformations (C11 and C16 chain lengths). We find rates are substrate-specific and obey predictions of classical nucleation theory at supersaturations that extend above the solubility of amorphous calcium carbonate. Analysis of the kinetic data shows the thermodynamic barrier to nucleation is reduced by minimizing the interfacial free energy of the system, γ. We then use dynamic force spectroscopy to independently measure calcitesubstrate-binding free energies, ΔG b . Moreover, we show that within the classical theory of nucleation, γ and ΔG b should be linearly related. The results bear out this prediction and demonstrate that low-energy barriers to nucleation correlate with strong crystal-substrate binding. This relationship is general to all functional group chemistries and conformations. These findings provide a physical model that reconciles the long-standing concept of templated nucleation through stereochemical matching with the conventional wisdom that good binders are good nucleators. The alternative perspectives become internally consistent when viewed through the lens of crystal-substrate binding.B iological systems are unique in their ability to organize minerals into functional materials with complex patterns and architectures. A substantial body of evidence suggests specialized macromolecules, particularly proteins (1, 2) and carbohydrates (3, 4), provide preferential sites for nucleation to direct the placement, timing, and orientation of crystals (5), both intra-and extracellular. Within the biomineralization community, the conventional view of biologically directed nucleation is that macromolecular matrices present an interfacial match to the crystal lattice that assists in forming the crystal nucleus. This cooperative view of directed nucleation is rooted in the collective action of multiple residues that guide the organization of ions into a configuration defining the energetic minimum for the system. A series of in vitro observations have reinforced this picture by showing that highly ordered organic monolayers can control the location and orientation of calcite crystals precipitated from solution (6). In this approach, good templates are revealed through a direct functional assay, i.e., nucleation. Over the years, this view of mineralization, both in the context of natural stru...

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“…Inhibition of Calcium Carbonate Precipitation and Calcium Binding Assay-The effect of Prisilkin-39 on calcium carbonate precipitation from its supersaturated solution was examined according to the method of Suzuki et al (13). Briefly, sample solution (10 l) was mixed with 100 l of 30 mM NaHCO 3 , pH 8.5.…”

Section: Construction Of Mantle Cdna Library-poly(a)mentioning

confidence: 99%

“…Based on a comparative analysis of currently known molluscan shell proteins according to the different shell layers in which they are present, the interesting phenomenon of an unbalanced protein distribution pattern has been discovered. It mainly embodies the fact that all of the extremely acidic shell proteins (pI Ͻ 4.5) are preferentially associated with the calcitic prismatic layer rather than the aragonitic nacreous layer (4,5,(12)(13)(14)(15)(16). Acidic matrix proteins are believed to be the major components in the soluble fraction of the shell matrix, and they exert effective control over the crystal growth because of their cation-binding capacity (17)(18)(19)(20).…”

mentioning

confidence: 99%

Cloning and Characterization of Prisilkin-39, a Novel Matrix Protein Serving a Dual Role in the Prismatic Layer Formation from the Oyster Pinctada fucata

Kong

Yan

et al. 2009

Journal of Biological Chemistry

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Molluscs form their shells out of CaCO 3 and a matrix of biomacromolecules. Understanding the role of matrices may shed some light on the mechanism of biomineralization. Here, a 1401-bp full-length cDNA sequence encoding a novel matrix protein was cloned from the mantle of the bivalve oyster, Pinctada fucata. The deduced protein (Prisilkin-39), which has a molecular mass of 39.3 kDa and an isoelectric point of 8.83, was fully characterized, and its role in biomineralization was demonstrated using both in vivo and in vitro crystal growth assays. Prisilkin-39 is a highly repetitive protein with an unusual composition of Gly, Tyr, and Ser residues. Expression of Prisilkin-39 was localized to columnar epithelial cells of the mantle edge, corresponding to the calcitic prismatic layer formation. Immunostaining in situ and immunodetection in vitro revealed the presence of a characteristic pattern of Prisilkin-39 in the organic sheet and in sheaths around the prisms. Prisilkin-39 binds tightly with chitin, an insoluble polysaccharide that forms the highly structured framework of the shell. Antibody injection in vivo resulted in dramatic morphological deformities in the inner shell surface structure, where large amounts of CaCO 3 were deposited in an uncontrolled manner. Moreover, Prisilkin-39 strictly prohibited the precipitation of aragonite in vitro. Taken together, Prisilkin-39 is the first protein shown to have dual function, involved both in the chitinous framework building and in crystal growth regulation during the prismatic layer mineralization. These observations may extend our view on the rare group of basic matrices and their functions during elaboration of the molluscan shell.

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Characterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster (Pinctada fucata)

Cited by 187 publications

References 25 publications

Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth

Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth

Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies

Cloning and Characterization of Prisilkin-39, a Novel Matrix Protein Serving a Dual Role in the Prismatic Layer Formation from the Oyster Pinctada fucata

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