Dual Roles of the Lysine-Rich Matrix Protein (KRMP)-3 in Shell Formation of Pearl Oyster, Pinctada fucata

Liang, Jian; Xu, Guangrui; Xie, Jun; Lee, Ilsun; Xiang, Liang; Wang, Hongzhong; Zhang, Guiyou; Xie, Liping; Zhang, Rongqing

doi:10.1371/journal.pone.0131868

Cited by 32 publications

(33 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The extracted matrix proteins can be classified as soluble proteins and insoluble proteins after the decalcification treatment by EDTA. Even though the insoluble matrix proteins were generally thought to be structural proteins that are responsible for the formation of the organic framework, some of these proteins have been reported to participate in the regulation of shell biomineralization (30,43). Here, we observed that the matrix protein Shematrin-2 is present in the EISM of shell nacreous and prismatic layers and in the extrapallial fluid where shell biomineralization occurs (Fig.…”

Section: Transcriptional Regulation Of Matrix Protein Shematrin-2mentioning

confidence: 65%

Transcriptional regulation of the matrix protein Shematrin-2 during shell formation in pearl oyster

Yan

Gao

Xie

et al. 2018

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

The molluscan shell is a fascinating biomineral consisting of a highly organized calcium carbonate composite. Biomineralization is elaborately controlled and involves several macromolecules, especially matrix proteins, but little is known about the regulatory mechanisms. The matrix protein Shematrin-2, expression of which peaks in the mantle tissues and in the shell components of the pearl oyster Pinctada fucata, has been suggested to be a key participant in biomineralization. Here, we expressed and purified Shematrin-2 from P. fucata and explored its function and transcriptional regulation. An in vitro functional assay revealed that Shematrin-2 binds the calcite, aragonite, and chitin components of the shell, decreases the rate of calcium carbonate deposition, and changes the morphology of the deposited crystal in the calcite crystallization system. Furthermore, we cloned the Shematrin-2 gene promoter, and analysis of its sequence revealed putative binding sites for the transcription factors CCAAT enhancer-binding proteins (Pf-C/EBPs) and nuclear factor-Y (NF-Y). Using transient co-transfection and reporter gene assays, we found that cloned and recombinantly expressed Pf-C/EBP-A and Pf-C/EBP-B greatly and dose-dependently up-regulate the promoter activity of the Shematrin-2 gene. Importantly, Pf-C/EBP-A and Pf-C/EBP-B knockdowns decreased Shematrin-2 gene expression and induced changes in the innersurface structures in prismatic layers that were similar to those of antibody-based Shematrin-2 inhibition. Altogether, our data reveal that the transcription factors Pf-C/EBP-A and Pf-C/EBP-B up-regulate the expression of the matrix protein Shematrin-2 during shell formation in P. fucata, improving our understanding of the transcriptional regulation of molluscan shell development at the molecular level.

show abstract

Section: Transcriptional Regulation Of Matrix Protein Shematrin-2mentioning

confidence: 65%

Transcriptional regulation of the matrix protein Shematrin-2 during shell formation in pearl oyster

Yan

Gao

Xie

et al. 2018

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

show abstract

“…The organic materials include matrix proteins, polysaccharides, lipids and other small molecules. And the matrix proteins are proved to be involved in calcium carbonate nucleation, polymorphs selection, crystal orientation, and have been extensively studied (Liang et al, 2015; Miyamoto et al, 1996; Ponce and Evans, 2011; Takeuchi et al, 2008). It has been demonstrated that many matrix protein genes were upregulated after shell damage stimulation (Kong et al, 2009; Lin et al, 2014) and some SMPs have been proved to promote nucleation of calcium carbonate, such as PfY2 (Yan et al, 2017), Alv (Kong et al, 2018) and Prismalin-14 (Suzuki et al, 2004).…”

Section: Resultsmentioning

confidence: 99%

Direct control of shell regeneration by the mantle tissue in the pearl oysterPinctada fucatavia accelerating CaCO3 nucleation

Huang

Liu

Jiang

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

28Molluscan bivalves rapidly repair the damaged shells to prevent further injury. However, it 29 remains unclear how this process is precisely controlled. In this study, we applied scanning 30 electronic microscopy, transmission electronic microscopy and histochemical analysis to 31 examine the detailed shell regeneration process of the pearl oyster Pinctada fucata. It was found 32 that the shell damage caused the mantle tissue to retract, which resulted in dislocation of the 33 mantle zones to their correspondingly secreted shell layers. However, the secretory repertoires 34 of the different mantle zones remained unchanged. As a result, the dislocation of the mantle 35 tissue dramatically affected the shell morphology, and the unusual presence of the submarginal 36 zone on the nacreous layers caused de novo precipitation of prismatic layers on the nacreous 37 layers. Real-time PCR revealed that the expression of the shell matrix proteins (SMPs) were 38 significantly upregulated, which was confirmed by the thermal gravimetric analysis (TGA) of 39 the newly formed shell. The increased matrix secretion accelerated CaCO3 nucleation thus 40 promoting shell deposition. Taken together, our study revealed the close relationship between 41 the physiological activities of the mantle tissue and the morphological change of the 42 regenerated shells. 43

show abstract

“…In vitro crystal growth experiments [29] were performed to test the effects of rWLP on the morphology of calcite and aragonite crystals. The rWLP was incubated in a freshly prepared saturated solution of calcium carbonate [30] on a siliconized cover glass with or without magnesium chloride.…”

Section: Functional Analysis Of Rwlpmentioning

confidence: 99%

“…The inhibition of the rWLP on calcium carbonate precipitation was tested using the methods provided by Liang et al [29] with minor modifications. Briefly, a 10 mM calcium chloride solution containing rWLP at various concentrations (10, 30, and 50 μg/mL) was dropped into a 96-well plate, and the plate was placed in a closed desiccator.…”

Section: Functional Analysis Of Rwlpmentioning

confidence: 99%

“…In addition, WLP contains 39 (26.5%) charged amino acids (S2 Table). The charged amino acids of SMPs were proposed to play important roles in biomineralization, either by forming a "calcium bridge" with calcium ions or by interacting with negatively charged carbonate ions [29,[38][39][40]. The abundant Gln and charged amino acids of WLP indicate the function of this protein in biomineralization.…”

Section: Plos Onementioning

confidence: 99%

See 1 more Smart Citation

Molecular characterization of a whirlin-like protein with biomineralization-related functions from the shell of Mytilus coruscus

et al. 2020

View full text Add to dashboard Cite

Mollusc shells are produced from calcified skeletons and have excellent mechanical properties. Shell matrix proteins (SMPs) have important functions in shell formation. A 16.6 kDa whirlin-like protein (WLP) with a PDZ domain was identified in the shell of Mytilus coruscus as a novel SMP. In this study, the expression, function, and location of WLP were analysed. The WLP gene was highly expressed and specifically located in the adductor muscle and mantle. The expression of recombinant WLP (rWLP) was associated with morphological change, polymorphic change, binding ability, and crystallization rate inhibition of the calcium carbonate crystals in vitro. In addition, an anti-rWLP antibody was prepared, and the results from immunohistochemistry and immunofluorescence analyses revealed the specific location of the WLP in the mantle, adductor muscle, and myostracum layer of the shell, suggesting multiple functions for WLP in biomineralization, muscle-shell attachment, and muscle attraction. Furthermore, results from a pull-down analysis revealed 10 protein partners of WLP in the shell matrices and a possible network of interacting WLPs in the shell. In addition, in this study, one of the WLP partners, actin, was confirmed to have the ability to bind WLP. These results expand the understanding of the functions of PDZ-domain-containing proteins in biomineralization and provide clues for determining the mechanisms of myostracum formation and muscle-shell attachment. OPEN ACCESS Citation: Jiang Y, Sun Q, Fan M, Zhang X, Shen W, Xu H, et al. (2020) Molecular characterization of a whirlin-like protein with biomineralization-related functions from the shell of Mytilus coruscus. PLoS ONE 15(4): e0231414. https://doi.org/10.

show abstract

Dual Roles of the Lysine-Rich Matrix Protein (KRMP)-3 in Shell Formation of Pearl Oyster, Pinctada fucata

Cited by 32 publications

References 44 publications

Transcriptional regulation of the matrix protein Shematrin-2 during shell formation in pearl oyster

Transcriptional regulation of the matrix protein Shematrin-2 during shell formation in pearl oyster

Direct control of shell regeneration by the mantle tissue in the pearl oysterPinctada fucatavia accelerating CaCO3 nucleation

Molecular characterization of a whirlin-like protein with biomineralization-related functions from the shell of Mytilus coruscus

Contact Info

Product

Resources

About