HcN57, A Novel Unusual Acidic Silk-Like Matrix Protein from Hyriopsis cumingii, Participates in Framework Construction and Nacre Nucleation During Nacreous Layer Formation

IF 2.6 3区 生物学 Q3 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Can Jin, Fangmengjie Wei, Jiayi Zhang, Xiaoyang Tan, Taixia Fan, Wen Luo, Jiale Li
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Abstract

In the classic molecular model of nacreous layer formation, unusual acidic matrix proteins rich in aspartic acid (Asp) residues are essential for nacre nucleation due to their great affinity for binding calcium. However, the acidic matrix proteins discovered in the nacreous layer so far have been weakly acidic with a high proportion of glutamate. In the present study, several silk-like matrix proteins, including the novel matrix protein HcN57, were identified in the ethylenediaminetetraacetic acid-soluble extracts of the nacreous layer of Hyriopsis cumingii. HcN57 is a highly repetitive protein that consists of a high proportion of alanine (Ala, 34.4%), glycine (Gly, 22.5%), and serine (Ser, 11.4%). It forms poly Ala blocks, GlynX repeats, an Ala-Gly repeat, and a Ser-Ala-rich region, exhibiting significant similarity to silk proteins found in spider species. The expression of HcN57 was specifically located in the dorsal epithelial cells of the mantle pallium and mantle center. Notably, expression of HcN57 was relatively high during nacreous layer regeneration and pearl nacre deposition, suggesting HcN57 is a silk matrix protein in the nacreous layer. Importantly, HcN57 also contains a certain content of Asp residues, making it an unusual acidic matrix protein present in the nacreous layer. These Asp residues are mainly distributed in three large hydrophilic acidic regions, which showed inhibitory activity against aragonite deposition and morphological regulation of calcite in vitro. Moreover, HcN57-dsRNA injection resulted in failure of nacre nucleation in vivo. Taken together, our results show that HcN57 is a bifunctional silk protein with poly Ala blocks and Gly-rich regions that serve as space fillers within the chitinous framework to prevent crystallization at unnecessary nucleation sites and Asp-rich regions that create a calcium ion supersaturated microenvironment for nucleation in the center of nacre tablets. These observations contribute to a better understanding of the mechanism by which silk proteins regulate framework construction and nacre nucleation during nacreous layer formation.

Abstract Image

Abstract Image

HcN57,一种来自拟南芥的新型异常酸性丝状基质蛋白,在珍珠层形成过程中参与框架构建和珍珠层成核。
在珍珠质层形成的经典分子模型中,富含天冬氨酸(Asp)残基的不寻常酸性基质蛋白因其与钙结合的强大亲和力而对珍珠质成核至关重要。然而,迄今为止在珍珠质层中发现的酸性基质蛋白都是弱酸性的,谷氨酸比例较高。本研究在乙二胺四乙酸可溶性提取物中发现了几种丝状基质蛋白,包括新型基质蛋白HcN57。HcN57是一种高度重复的蛋白质,由高比例的丙氨酸(Ala,34.4%)、甘氨酸(Gly,22.5%)和丝氨酸(Ser,11.4%)组成。它形成了多Ala块、GlynX重复序列、一个Ala-Gly重复序列和一个Ser-Ala富集区,与在蜘蛛物种中发现的丝蛋白非常相似。HcN57 的表达特异性地分布在被膜和被膜中心的背侧上皮细胞中。值得注意的是,在珍珠层再生和珍珠层沉积过程中,HcN57的表达量相对较高,这表明HcN57是珍珠层中的一种丝基质蛋白。重要的是,HcN57还含有一定含量的Asp残基,使其成为珍珠质层中一种不同寻常的酸性基质蛋白。这些Asp残基主要分布在三个大的亲水性酸性区域,在体外对文石沉积和方解石形态调节具有抑制活性。此外,注射 HcN57-dsRNA 会导致体内珍珠岩成核失败。综上所述,我们的研究结果表明,HcN57是一种具有双重功能的丝蛋白,其多Ala块和富含Gly的区域可作为壳质框架内的空间填充物,防止在不必要的成核点结晶,而富含Asp的区域则可为珍珠质片中心的成核创造一个钙离子过饱和的微环境。这些观察结果有助于更好地理解丝蛋白在珍珠质层形成过程中调节框架构建和珍珠质成核的机制。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Marine Biotechnology
Marine Biotechnology 工程技术-海洋与淡水生物学
CiteScore
4.80
自引率
3.30%
发文量
95
审稿时长
2 months
期刊介绍: Marine Biotechnology welcomes high-quality research papers presenting novel data on the biotechnology of aquatic organisms. The journal publishes high quality papers in the areas of molecular biology, genomics, proteomics, cell biology, and biochemistry, and particularly encourages submissions of papers related to genome biology such as linkage mapping, large-scale gene discoveries, QTL analysis, physical mapping, and comparative and functional genome analysis. Papers on technological development and marine natural products should demonstrate innovation and novel applications.
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