一类新型纤维状蛋白质及其对生物矿化的调控作用研究
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摘要
双壳纲贝壳韧带是一类由蛋白质和文石纤维组成的天然有机—无机复合生物材料,在生物中主要起连接两个壳瓣并打开贝壳的功能。当闭壳肌收缩使贝壳关闭时,韧带储存有弹性能；当闭壳肌松弛时,韧带中储存的弹性能使贝壳打开。因此,贝壳韧带还是一类天然的弹性生物材料。对其结构、组成和性能等进行深入研究,可为高性能仿生材料的合成提供模板和科学依据。本文以我国北部湾常见的双壳纲大竹蛏和辐射荚蛏韧带为重点研究对象,以尖紫蛤韧带作对比研究。首先采用扫描电子显微镜、粉末X-射线衍射、傅立叶变换红外光谱和氨基酸分析对三种韧带的结构及化学组成进行研究,并运用静力学基本理论对韧带的受力情况进行分析。接着重点对在大竹蛏和辐射荚蛏韧带中新发现的纤维状蛋白质进行了较详细的研究。采用基质辅助激光解吸电离串联飞行时间质谱和液相色谱-电喷雾串联质谱对这种蛋白质进行鉴定,分析其组装机理；以傅立叶变换红外光谱对蛋白质二级结构进行测定并分析结构与功能的关系。然后以辐射荚蛏韧带纤维状蛋白质为模板在体外进行仿生矿化研究,探索韧带文石纤维的矿化机理。最后以荧光显微镜和荧光分光光度计对韧带的天然荧光进行初步探索。
本文获得以下几方面主要成果：
(1)建立了韧带新的三层结构模型。发现韧带内层文石纤维(直径100-200nm)是由大量的文石纳米颗粒相互粘结形成,纤维具有两种定向,即靠近背侧部,纤维由两侧向中轴线方向聚集,从前端向后端倾斜生长,并逐渐向腹侧面弯曲,最后垂直于腹侧面。首次发现韧带内层中存在的普遍公认的“生长线”是由断裂的“之”字形文石纤维形成,并认为这种“之”字形结构是韧带受到长期反复自外向内的压应力造成的。
(2)发现大竹蛏和辐射荚蛏韧带中的纤维状蛋白质Solenin和K58(直径120-150nm)是一类同源于KRT1和KRT9的新型纤维状蛋白质。认为两者都是由同源于KRT9的Ⅰ型蛋白质单体和同源于KRT1的Ⅱ型蛋白质单体以平行排列的方式先形成异质二聚体,再相互交错以反平行排列方式形成四聚体,然后逐步组装成异质多聚体中间丝,最后再自组装成蛋白质纤维。这种纤维是物种为适应快速挖洞的生活习性而进化形成。
(3) Solenin和K58吸水后可发生膨胀使弹性显著增加。蛋白质链中亲水性氨基酸残基与水分子之间形成的氢键,以及结构中"SGGG"、"SYGSGG"、"GGGGG"和“GGG”重复序列形成的“甘氨酸环”是这种膨胀性和弹性的主要来源。而Solenin和K58的高β-折叠结构含量(分别为41.76%和46.20%),赋予它们良好的抗拉强度和抗化学试剂腐蚀性能。
(4)在常温常压不添加任何其它物质的情况下,以K58为基底,经由ACC相变途径合成获得了纯度95-100%的由大量纳米棒构成的文石超结构。这种纳米棒与韧带文石纤维形貌十分相似,都是由文石晶体颗粒以相同的结晶学定向相互粘结形成。认为K58表面酸性氨基酸残基的羧基具有与文石晶格相似的短程有序,从而使诱导形成的无定形碳酸钙(ACC)具有类似的短程有序,最终导致ACC择优相变成文石晶体。首次提出辐射荚蛏韧带内层文石纤维的形成是由K58控制的观点。
(5)提出了一种新的文石纳米棒和超结构形成模式：即ACC先相变形成无序的文石纳米晶体。晶体不断生长融合,在内能和界面自由能的作用下,晶体发生旋转以获得相同的结晶学定向,并相互粘结形成纳米棒。通过布朗运动,胶体状的ACC以二维方式不断粘结在纳米棒四周并逐渐转变成更多的纳米棒,最终纳米棒聚集形成各种文石超结构。这种非传统的结晶模式为结晶学理论提供了重要的补充。
(6)首次发现韧带内层中存在能产生蓝色、黄色、绿色和红色荧光的物质,并测得其最大激发波长为380nm,最大发射波长约为467nm。认为荧光的产生与内层酸不溶性蛋白质有关,而内层的Ca2+对荧光有增强作用。
Bivalve ligament is a kind of natural organic-inorganic biocomposite materials that comprise of proteins and aragonite fibers. It functions to connect the two valves and serves to open them in living organism. When the abductor muscles of the organism contract and the valves close, elastic energy is stored in the ligament; when the abductor muscles relax, this energy causes the valves open. Therefore, bivalve ligament is also a kind of natural elastic biomaterials. Thoroughly studying on ligament structure, composition, and properties can provide not only scientific data, but also templates for synthesizing of high performance biomimetic materials. This article focus on ligaments of bivalve Solen grandis and Siliqua radiata, as compared with that of bivalve Sanguinolaria acuta, those of which are the common species from Beibu Gulf in South China. Firstly, microstructures and chemical compositions of these ligaments were investigated by scanning electron microscope, powder X-ray diffraction, Fourier transform infrared spectroscopy, and amino acid composition analysis; the forces which act on ligaments were also analyzed using the statics basic axioms. Then, main attentions and detailed studies were paid to the novel fibrous proteins discovered from S. grandis and S. radiata ligaments. The proteins were identified by matrix assisted laser desoiption ionization tandem time of flight mass spectrometry and liquid chromatography electrospray ionization tandem mass spectrometry, and their assembly mechanism were also analyzed. Using Fourier transform infrared spectroscopy, we determined the secondary structures of the proteins and analyzed their structure-function relationships. To investigate the mineralization mechanism of aragonite fibers in ligaments, biomimetic mineralization research was carried out using fibrous protein from S. radiata ligament as a template in vitro. Finally, the natural fluorescence of ligaments was preliminarily studied using fluorescence microscope and fluorescence spectrophotometer.
Main conclusions of this work are drawn as follows:
(1) We established a novel three layer structural model of bivalve ligament and found that aragonite fibers (with diameter of100-200nm) in inner layer of ligaments are formed by lots of attached anagonite nanoparticles. These fibers show two different orientations, i.e., fibers at dorsal part arrange from two laterals to central axis and orient posteriorly inclining almost parallel to dorsal surface; then, they turn gradually to ventral part and orient vertical to ventral surface. In addition, we first found that the accepted "growth lines" in inner layer of ligaments are formed by fractured "zigzag" aragonite fibers. These "zigzag" structures, we believe, result from the long-term repeated compressive stress acting on ligaments.
(2) We discovered that fibrous protein Solenin and K58of S. grandis and S. radiata ligament, respectively, are a new type of fibrous proteins, and both of them are homologous to keratin type Ⅱ cytoskeletal1(KRT1) and type Ⅰ cytoskeletal9(KRT9). The proteins assemble initially by type Ⅰ and type Ⅱ monomers homologous to KRT9and KRT1, respectively, to form heterodimers in parallel manner; then, heterodimers join side by side in a staggered antiparallel manner to form tetramers; after that, heteropolymer intermediate filaments are formed gradually, and finally they self-assemble into protein fibers. We consider that these fibers are evolved to adapt the rapid burrowing life habits of those species.
(3) Solenin and K58show remarkable expansibility and elasticity after absorbing water. These properties are coming mainly from the hydrogen bonds that formed between water molecules and hydrophilic amino acids in the protein, and from the "Glycine-loops" formed by "SGGG","SYGSGG","GGGGG", and "GGG" repeat sequences. While, the high β-sheet contents of Solenin (41.76%) and K58(46.20%) give the proteins excellent tensile strength and corrosion resistance properties.
(4) With no additives and using K58as substrate, we obtained almost pure (95-100%) aragonite superstructures with lots of nanorods via transformation of ACC at ambient conditions. These nanorods, which are formed by attached aragonite crystals in the same crystallographic orientation, show morphology strikingly similar to aragonite fibers in ligaments. We believe the carboxyl groups of acidic amino acid residues of K58, which have short-range order similar to aragonite lattice, induce short-range order amorphous calcium carbonate (ACC) formation, resulting in the preferential transformation of ACC into aragonite. Meanwhile, we first propose that the formation of aragonite fibers in S. radiata ligament is controlled by K58.
(5) We propose a new formation mode of aragonite nanorods and superstructures. Firstly, ACCs transform into disordered aragonite nanocrystals. Then, these crystals grow gradually, fuse with each other, rotate to get the same crystallographic orientation with driving force coming from the decrease of internal energy and removing of surface energy, and attach to form a nanorod. After that, colloidal ACCs attach to the rod in a2D maner by Brownian motion and evolve into more nanorods. Finally, aragonite superstructures with various morphologies are formed by continual aggregating of nanorods. This unconventional crystallization mode provides an important supplement for theory of crystallography.
(6) We first discover that the inner layer of S. grandis, S. radiata, and S. acuta ligaments contain substances that can emit blue, yellow, green, and red fluorescence. The maximum excitation and emission wavelengths of these substances are380and467nm, respectively. We consider that this fluorescence is closely related to acid insoluble proteins in the inner layers of the ligaments, and it can be highlighted by Ca2+
本文获得以下几方面主要成果：
(1)建立了韧带新的三层结构模型。发现韧带内层文石纤维(直径100-200nm)是由大量的文石纳米颗粒相互粘结形成,纤维具有两种定向,即靠近背侧部,纤维由两侧向中轴线方向聚集,从前端向后端倾斜生长,并逐渐向腹侧面弯曲,最后垂直于腹侧面。首次发现韧带内层中存在的普遍公认的“生长线”是由断裂的“之”字形文石纤维形成,并认为这种“之”字形结构是韧带受到长期反复自外向内的压应力造成的。
(2)发现大竹蛏和辐射荚蛏韧带中的纤维状蛋白质Solenin和K58(直径120-150nm)是一类同源于KRT1和KRT9的新型纤维状蛋白质。认为两者都是由同源于KRT9的Ⅰ型蛋白质单体和同源于KRT1的Ⅱ型蛋白质单体以平行排列的方式先形成异质二聚体,再相互交错以反平行排列方式形成四聚体,然后逐步组装成异质多聚体中间丝,最后再自组装成蛋白质纤维。这种纤维是物种为适应快速挖洞的生活习性而进化形成。
(3) Solenin和K58吸水后可发生膨胀使弹性显著增加。蛋白质链中亲水性氨基酸残基与水分子之间形成的氢键,以及结构中"SGGG"、"SYGSGG"、"GGGGG"和“GGG”重复序列形成的“甘氨酸环”是这种膨胀性和弹性的主要来源。而Solenin和K58的高β-折叠结构含量(分别为41.76%和46.20%),赋予它们良好的抗拉强度和抗化学试剂腐蚀性能。
(4)在常温常压不添加任何其它物质的情况下,以K58为基底,经由ACC相变途径合成获得了纯度95-100%的由大量纳米棒构成的文石超结构。这种纳米棒与韧带文石纤维形貌十分相似,都是由文石晶体颗粒以相同的结晶学定向相互粘结形成。认为K58表面酸性氨基酸残基的羧基具有与文石晶格相似的短程有序,从而使诱导形成的无定形碳酸钙(ACC)具有类似的短程有序,最终导致ACC择优相变成文石晶体。首次提出辐射荚蛏韧带内层文石纤维的形成是由K58控制的观点。
(5)提出了一种新的文石纳米棒和超结构形成模式：即ACC先相变形成无序的文石纳米晶体。晶体不断生长融合,在内能和界面自由能的作用下,晶体发生旋转以获得相同的结晶学定向,并相互粘结形成纳米棒。通过布朗运动,胶体状的ACC以二维方式不断粘结在纳米棒四周并逐渐转变成更多的纳米棒,最终纳米棒聚集形成各种文石超结构。这种非传统的结晶模式为结晶学理论提供了重要的补充。
(6)首次发现韧带内层中存在能产生蓝色、黄色、绿色和红色荧光的物质,并测得其最大激发波长为380nm,最大发射波长约为467nm。认为荧光的产生与内层酸不溶性蛋白质有关,而内层的Ca2+对荧光有增强作用。
Bivalve ligament is a kind of natural organic-inorganic biocomposite materials that comprise of proteins and aragonite fibers. It functions to connect the two valves and serves to open them in living organism. When the abductor muscles of the organism contract and the valves close, elastic energy is stored in the ligament; when the abductor muscles relax, this energy causes the valves open. Therefore, bivalve ligament is also a kind of natural elastic biomaterials. Thoroughly studying on ligament structure, composition, and properties can provide not only scientific data, but also templates for synthesizing of high performance biomimetic materials. This article focus on ligaments of bivalve Solen grandis and Siliqua radiata, as compared with that of bivalve Sanguinolaria acuta, those of which are the common species from Beibu Gulf in South China. Firstly, microstructures and chemical compositions of these ligaments were investigated by scanning electron microscope, powder X-ray diffraction, Fourier transform infrared spectroscopy, and amino acid composition analysis; the forces which act on ligaments were also analyzed using the statics basic axioms. Then, main attentions and detailed studies were paid to the novel fibrous proteins discovered from S. grandis and S. radiata ligaments. The proteins were identified by matrix assisted laser desoiption ionization tandem time of flight mass spectrometry and liquid chromatography electrospray ionization tandem mass spectrometry, and their assembly mechanism were also analyzed. Using Fourier transform infrared spectroscopy, we determined the secondary structures of the proteins and analyzed their structure-function relationships. To investigate the mineralization mechanism of aragonite fibers in ligaments, biomimetic mineralization research was carried out using fibrous protein from S. radiata ligament as a template in vitro. Finally, the natural fluorescence of ligaments was preliminarily studied using fluorescence microscope and fluorescence spectrophotometer.
Main conclusions of this work are drawn as follows:
(1) We established a novel three layer structural model of bivalve ligament and found that aragonite fibers (with diameter of100-200nm) in inner layer of ligaments are formed by lots of attached anagonite nanoparticles. These fibers show two different orientations, i.e., fibers at dorsal part arrange from two laterals to central axis and orient posteriorly inclining almost parallel to dorsal surface; then, they turn gradually to ventral part and orient vertical to ventral surface. In addition, we first found that the accepted "growth lines" in inner layer of ligaments are formed by fractured "zigzag" aragonite fibers. These "zigzag" structures, we believe, result from the long-term repeated compressive stress acting on ligaments.
(2) We discovered that fibrous protein Solenin and K58of S. grandis and S. radiata ligament, respectively, are a new type of fibrous proteins, and both of them are homologous to keratin type Ⅱ cytoskeletal1(KRT1) and type Ⅰ cytoskeletal9(KRT9). The proteins assemble initially by type Ⅰ and type Ⅱ monomers homologous to KRT9and KRT1, respectively, to form heterodimers in parallel manner; then, heterodimers join side by side in a staggered antiparallel manner to form tetramers; after that, heteropolymer intermediate filaments are formed gradually, and finally they self-assemble into protein fibers. We consider that these fibers are evolved to adapt the rapid burrowing life habits of those species.
(3) Solenin and K58show remarkable expansibility and elasticity after absorbing water. These properties are coming mainly from the hydrogen bonds that formed between water molecules and hydrophilic amino acids in the protein, and from the "Glycine-loops" formed by "SGGG","SYGSGG","GGGGG", and "GGG" repeat sequences. While, the high β-sheet contents of Solenin (41.76%) and K58(46.20%) give the proteins excellent tensile strength and corrosion resistance properties.
(4) With no additives and using K58as substrate, we obtained almost pure (95-100%) aragonite superstructures with lots of nanorods via transformation of ACC at ambient conditions. These nanorods, which are formed by attached aragonite crystals in the same crystallographic orientation, show morphology strikingly similar to aragonite fibers in ligaments. We believe the carboxyl groups of acidic amino acid residues of K58, which have short-range order similar to aragonite lattice, induce short-range order amorphous calcium carbonate (ACC) formation, resulting in the preferential transformation of ACC into aragonite. Meanwhile, we first propose that the formation of aragonite fibers in S. radiata ligament is controlled by K58.
(5) We propose a new formation mode of aragonite nanorods and superstructures. Firstly, ACCs transform into disordered aragonite nanocrystals. Then, these crystals grow gradually, fuse with each other, rotate to get the same crystallographic orientation with driving force coming from the decrease of internal energy and removing of surface energy, and attach to form a nanorod. After that, colloidal ACCs attach to the rod in a2D maner by Brownian motion and evolve into more nanorods. Finally, aragonite superstructures with various morphologies are formed by continual aggregating of nanorods. This unconventional crystallization mode provides an important supplement for theory of crystallography.
(6) We first discover that the inner layer of S. grandis, S. radiata, and S. acuta ligaments contain substances that can emit blue, yellow, green, and red fluorescence. The maximum excitation and emission wavelengths of these substances are380and467nm, respectively. We consider that this fluorescence is closely related to acid insoluble proteins in the inner layers of the ligaments, and it can be highlighted by Ca2+
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