肺炎链球菌中0-连接的糖基转移酶GtfA及其激活子GtfB的结构和功能研究
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摘要
蛋白质O-G1cNAc糖基化修饰是一种重要的翻译后修饰形式,其在真核生物的生命过程中从基因转录、蛋白的定位、细胞内外信号调控到细胞的生长与分化、细胞间相互识别、细胞黏附、免疫保护等诸多过程中都发挥着至关重要的作用。近期的一些研究表明,O-G1cNAcylation与很多重大的慢性疾病也存在非常紧密的联系,包括糖尿病、心血管疾病、神经退行性疾病以及癌症等等。在原核生物中,特别是一些重要的人类致病菌中,发现细菌糖蛋白的O-G1cNAc修饰与其生理学和病理学过程存在着密切的联系。到目前为止,人们在结构上只鉴定出一种负责催化该类型修饰的糖基转移酶O-G1cNAc transferases (OGTs),它们具有共同的结构模式,通常N-端是由多个典型的(tetratricopeptide repeats, TPRs)34肽重复序列组成反平行的全a-螺旋结构域,而C-端具有扭曲的GT-B折叠类型的糖基转移酶核心结构域。
近些年来,在革兰氏阳性致病菌中发现一类重要的高度糖基化的黏附蛋白serine-rich repeat glycoproteins (SRRPs),它们对致病菌的黏附、免疫逃逸、增殖、生物被膜的形成以及毒理发挥过程起着关键作用。在对SRRPs糖基化修饰过程的研究中,发现了一类与众不同的OGT复合体,它负责对受体SRRP蛋白进行第一步的O-G1cNAc修饰。在肺炎链球菌中,这类OGT复合体由GtfA和GtfB两个蛋白组成,它们以UDP-G1cNAc为糖基供体,实现将G1cNAc糖基转移至肺炎链球菌中的SRRP蛋白PsrP蛋白上。
在研究中,我们在对GtfA、GtfB单独及两者之间的复合物进行了晶体学研究过程中,分别获得了衍射分辨率为2A的GtfA与UDP和G1cNAc共结晶的晶体,7A的GtfB晶体和4.5A的GtfA-GtfB复合物与产物UDP和G1cNAc共结晶的晶体。目前,已经解析了GtfA添加产物UDP和G1cNAc的复合物品体结构,发现GtfA核心结构具有经典的GT-B折叠类型,N-端由10个反平行的β-折叠片组成一个新型折叠类型的β-meader "add-on" DUF1975结构域。这种新型结构组合模式与以往单纯采用经典的GT-B折叠类型的糖基转移酶,目前己知的TPR和GT-B组合模式的hOGT/XcOGT,乃至于具有‘'add-on"结构域的GT-B折叠类型的糖基转移酶结构都存在着显著差异。我们基于结构和生化实验证实了DUF1975结构域是一种新型的蛋白相互作用模块,它对受体蛋白的识别结合及糖基化修饰功能的完成是必不可少的。对GtfA的活性位点分析发现它采用Retaining糖基转移酶所特有的结构特点,并进而鉴定了参与糖基转移酶催化活性的关键残基。通过体外糖基转移酶活性测定进行催化活性测定证明了只有完整的GtfA-GtfB复合物才具有真正的OGT活性,而关键位点的点突变会造成活性的完全丧失。进而,通过质谱分析鉴定了完全糖基化修饰后的受体SRR1,我们发现GtfA-GtfB是一类对多位点丝氨酸具有特异修饰能力的OGT。最终,基于GtfA的结构和分子模拟结果,我们提出了O-G1cNAc糖基化修饰过程中GtfA与受体可能的相互作用方式和催化机制,并基于模型进行了一系列的体内和体外糖基转移酶活性的验证,证明了模型的可信性和合理性。
综上所述,我们对GtfA-GtfB复合体在结构和酶学功能方面的研究,揭示了原核中一类参与蛋白质糖基化修饰的新型Retaining OGT;其对丝氨酸具有特异性,而且能实现连续的多位点丝氨酸的O-G1cNAc修饰；并在酶学分类上将这类OGT分类到EC2.4.1.255类别中；另外,通过体外生化和微生物体内验证分子模型的可信性,提出可能的受体结合模式和酶的反应机制。我们对这类OGT结构和功能方面的研究有望为治疗和预防革兰氏阳性致病菌感染的新型药物或疫苗开发和设计提供理论基础。
Protein glycosylation catalyzed by the O-G1cNAc transferase (OGT) plays a critical role in various biological processes in not only eukaryotes but also prokaryotes. In human, aberrant O-GlcNAcylations are correlated with many challenging diseases, including diabetes, cardiovascular disease, neurodegenerative diseases and cancer. Whereas, the O-GlcNAcylation of glycoprotein in bacteria is closely related with the physiology and pathogenesis, especially for the pathogenic bacterial strains.
Notably, serine-rich repeat glycoproteins (SRRPs) that exclusively exist in Gram-positive pathogens are a large family of surface adhesins, which are important for bacterial adhesion, immune evasion, colonization, biofilm formation and virulence. It was identified an enzyme complex, O-GlcNAc transferase (termed OGT) GtfA and its partner GtfB from Streptococcus pneumoniae, is required for the initial step of glycosylation of the serine-rich repeat protein (PsrP) by transferring the GlcNAc residue from UDP-GlcNAc to PsrP.
In this manuscript, we determined the crystal structure of GtfA in complex with GlcNAc and UDP at2.0A resolution. The GtfA structure comprises a core structure of GT-B fold and a β-meander "add-on" DUF1975domain, which reveals a novel structure of a twisted10-stranded antiparallel β-sheet for the first time. Despite of the distinct structure from the all-a tetratricopeptide repeat (TPR) units of only two structure-known OGTs (hOGT and XcOGT), DUF1975also plays a role in acceptor binding or recognition. The in vitro and in vivo O-GlcNAcylation assays proved that DUF1975domain of GtfA involves the recognition of the acceptor PsrP and its co-activator GtfB; thus is critical for the intact OGT activity. Further glycoproteomic analyses revealed that the intact GtfA-GtfB complex was specific to modify the serine residues of PrsP, and all serine could be O-GlcNAcylated. Furthermore, in order to elucidate the mechanism of PrsP O-GlcNAcylation, we also crystallized Apo GtfB as well as GtfA-GtfB complex in UDP and GlcNAc binding form which diffracted to7.0and4.5respectivly. At the meantime, a docking model of GtfA with the N-terminal18-residue peptide of the first serine-rich repeat region (SRR1) of PsrP was performed, suggesting a rational retaining catalytic mechanism that is distinguished from two structure-known inverting OGTs.
Take together, our structural and biochemical study provides insights into a novel retaining O-GlcNAc transferase complex GtfA-GtfB. We are firstly unraveled the catalytic subunit GtfA structurally, and identified a novel β-meander "add-on" DUF1975domain, which is a mediator essential to protein interaction or recognition. In addition, we are firstly elucidated GtfA-GtfB is a serine-specific OGT, despite adopting a core structure of GtfA similar to that in the GT4family, GtfA belongs to EC2.4.1.255according to the catalytic activity. Our results provide a structural basis for the rational design of therapeutic drugs and new vaccine against pneumococcal related diseases.
近些年来,在革兰氏阳性致病菌中发现一类重要的高度糖基化的黏附蛋白serine-rich repeat glycoproteins (SRRPs),它们对致病菌的黏附、免疫逃逸、增殖、生物被膜的形成以及毒理发挥过程起着关键作用。在对SRRPs糖基化修饰过程的研究中,发现了一类与众不同的OGT复合体,它负责对受体SRRP蛋白进行第一步的O-G1cNAc修饰。在肺炎链球菌中,这类OGT复合体由GtfA和GtfB两个蛋白组成,它们以UDP-G1cNAc为糖基供体,实现将G1cNAc糖基转移至肺炎链球菌中的SRRP蛋白PsrP蛋白上。
在研究中,我们在对GtfA、GtfB单独及两者之间的复合物进行了晶体学研究过程中,分别获得了衍射分辨率为2A的GtfA与UDP和G1cNAc共结晶的晶体,7A的GtfB晶体和4.5A的GtfA-GtfB复合物与产物UDP和G1cNAc共结晶的晶体。目前,已经解析了GtfA添加产物UDP和G1cNAc的复合物品体结构,发现GtfA核心结构具有经典的GT-B折叠类型,N-端由10个反平行的β-折叠片组成一个新型折叠类型的β-meader "add-on" DUF1975结构域。这种新型结构组合模式与以往单纯采用经典的GT-B折叠类型的糖基转移酶,目前己知的TPR和GT-B组合模式的hOGT/XcOGT,乃至于具有‘'add-on"结构域的GT-B折叠类型的糖基转移酶结构都存在着显著差异。我们基于结构和生化实验证实了DUF1975结构域是一种新型的蛋白相互作用模块,它对受体蛋白的识别结合及糖基化修饰功能的完成是必不可少的。对GtfA的活性位点分析发现它采用Retaining糖基转移酶所特有的结构特点,并进而鉴定了参与糖基转移酶催化活性的关键残基。通过体外糖基转移酶活性测定进行催化活性测定证明了只有完整的GtfA-GtfB复合物才具有真正的OGT活性,而关键位点的点突变会造成活性的完全丧失。进而,通过质谱分析鉴定了完全糖基化修饰后的受体SRR1,我们发现GtfA-GtfB是一类对多位点丝氨酸具有特异修饰能力的OGT。最终,基于GtfA的结构和分子模拟结果,我们提出了O-G1cNAc糖基化修饰过程中GtfA与受体可能的相互作用方式和催化机制,并基于模型进行了一系列的体内和体外糖基转移酶活性的验证,证明了模型的可信性和合理性。
综上所述,我们对GtfA-GtfB复合体在结构和酶学功能方面的研究,揭示了原核中一类参与蛋白质糖基化修饰的新型Retaining OGT;其对丝氨酸具有特异性,而且能实现连续的多位点丝氨酸的O-G1cNAc修饰；并在酶学分类上将这类OGT分类到EC2.4.1.255类别中；另外,通过体外生化和微生物体内验证分子模型的可信性,提出可能的受体结合模式和酶的反应机制。我们对这类OGT结构和功能方面的研究有望为治疗和预防革兰氏阳性致病菌感染的新型药物或疫苗开发和设计提供理论基础。
Protein glycosylation catalyzed by the O-G1cNAc transferase (OGT) plays a critical role in various biological processes in not only eukaryotes but also prokaryotes. In human, aberrant O-GlcNAcylations are correlated with many challenging diseases, including diabetes, cardiovascular disease, neurodegenerative diseases and cancer. Whereas, the O-GlcNAcylation of glycoprotein in bacteria is closely related with the physiology and pathogenesis, especially for the pathogenic bacterial strains.
Notably, serine-rich repeat glycoproteins (SRRPs) that exclusively exist in Gram-positive pathogens are a large family of surface adhesins, which are important for bacterial adhesion, immune evasion, colonization, biofilm formation and virulence. It was identified an enzyme complex, O-GlcNAc transferase (termed OGT) GtfA and its partner GtfB from Streptococcus pneumoniae, is required for the initial step of glycosylation of the serine-rich repeat protein (PsrP) by transferring the GlcNAc residue from UDP-GlcNAc to PsrP.
In this manuscript, we determined the crystal structure of GtfA in complex with GlcNAc and UDP at2.0A resolution. The GtfA structure comprises a core structure of GT-B fold and a β-meander "add-on" DUF1975domain, which reveals a novel structure of a twisted10-stranded antiparallel β-sheet for the first time. Despite of the distinct structure from the all-a tetratricopeptide repeat (TPR) units of only two structure-known OGTs (hOGT and XcOGT), DUF1975also plays a role in acceptor binding or recognition. The in vitro and in vivo O-GlcNAcylation assays proved that DUF1975domain of GtfA involves the recognition of the acceptor PsrP and its co-activator GtfB; thus is critical for the intact OGT activity. Further glycoproteomic analyses revealed that the intact GtfA-GtfB complex was specific to modify the serine residues of PrsP, and all serine could be O-GlcNAcylated. Furthermore, in order to elucidate the mechanism of PrsP O-GlcNAcylation, we also crystallized Apo GtfB as well as GtfA-GtfB complex in UDP and GlcNAc binding form which diffracted to7.0and4.5respectivly. At the meantime, a docking model of GtfA with the N-terminal18-residue peptide of the first serine-rich repeat region (SRR1) of PsrP was performed, suggesting a rational retaining catalytic mechanism that is distinguished from two structure-known inverting OGTs.
Take together, our structural and biochemical study provides insights into a novel retaining O-GlcNAc transferase complex GtfA-GtfB. We are firstly unraveled the catalytic subunit GtfA structurally, and identified a novel β-meander "add-on" DUF1975domain, which is a mediator essential to protein interaction or recognition. In addition, we are firstly elucidated GtfA-GtfB is a serine-specific OGT, despite adopting a core structure of GtfA similar to that in the GT4family, GtfA belongs to EC2.4.1.255according to the catalytic activity. Our results provide a structural basis for the rational design of therapeutic drugs and new vaccine against pneumococcal related diseases.
引文
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