近江牡蛎类立克次体与宿主相互作用的分子生物学研究
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摘要
宿主与病原的相互作用是国际微生物感染免疫学前沿领域的重要命题。类立克次体是一类严格细胞内寄生的革兰氏阴性微生物,导致养殖牡蛎的大量死亡,但对于其分子生物学和致病机理知之甚少。本研究主要采用类立克次体菌体细胞和外膜蛋白诱导刺激近江牡蛎宿主,系统探索了类立克次体病原与宿主的相互作用：即类立克次体菌体细胞诱导宿主核转录因子CREB, LITAF的免疫功能与机理及类立克次体外膜蛋白ompR诱导刺激后宿主的分子免疫反应机制以及信号传导途径。
取类立克次体诱导刺激后的近江牡蛎血淋巴细胞,采用TRIzol法提取RNA,制备cDNA模板。根据CREB蛋白的保守结构特征设计了兼并寡聚核苷酸引物,采用RT-PCR和RACE PCR技术首次在双壳贝类中获得了Ca-CREB的全长cDNA序列。该cDNA序列含有一个1068 bp的读码框,编码一个39.3 kDa的蛋白,该蛋白具有转录因子CREB的特征性结构,与无脊椎动物海兔和蜗牛的CREB同源性较高,相似度分别为56%和58%。组织半定量RT-PCR结果表明：Ca-CREB在各组织中均有表达,但在血细胞和鳃中的表达量明显高于其它组织,预示该基因可能与免疫调节有关。通过构建重组表达质粒pET-CREB,在大肠杆菌中对Ca-CREB进行了诱导表达、蛋白纯化并制备了多克隆抗体,同时利用凝胶阻滞技术(EMSA)对重组蛋白的活性进行了研究。随后采用Real time RT-PCR、Western blotting和EMSA技术探讨了Ca-CREB在类立克次体诱导刺激条件下的激活机理及功能。结果表明：①Ca-CREB在大肠杆菌中得到了高效表达,获得的重组蛋白具有特异的DNA结合活性,制备的兔多克隆抗体的效价为1:12000。②在类立克次体诱导刺激不同时间段内,血淋巴细胞中Ca-CREB的基因表达水平没有显著差异,而Ca-CREB的DNA结合活性和磷酸化水平得到了明显提高,这表明核转录因子Ca-CREB在类立克次体诱导的宿主免疫反应中具有功能,且这种功能的激活发生在转录后水平上。接着,我们分别从表达载体、胶浓度及电泳条件等方面着手,对Ca-CREB原核表达产物比预测蛋白分子量偏大的原因进行了分析,结果表明：不同的表达载体及胶浓度对Ca-CREB融合蛋白在SDS-PAGE中表现的分子量大小没有影响,而不同SDS-PAGE体系分离融合蛋白时产生了融合分子量偏小的现象,推测不同的SDS-PAGE体系与分子量偏差的产生有关。
鉴于类立克次体在菌体细胞水平上能够诱导刺激宿主发生上述免疫反应,为深入探讨类立克次体在蛋白分子水平上是否能够诱导刺激宿主的分子免疫反应机制及信号传导途径,本实验通过基因组测序方法获得了首个贝类类立克次体病原的外膜蛋白ompR基因并研究了其免疫功能。该基因全长531bp,编码176个氨基酸,预测的蛋白分子量和等电点分别为19.76 KDa和9.76。核酸和氨基酸序列分析表明该蛋白具有细菌外膜蛋白的特征,与人Q热立克次体和潮虫立克次体外膜蛋白ompH具有20%-27%的相似性。随后以上述同样方法进行了ompR重组蛋白的表达、纯化和多克隆抗体的制备。在功能研究上,采用实时定量PCR、EMSA等技术手段分析了ompR诱导刺激后,宿主多个免疫相关因子的免疫反应机制及信号传导,结果显示：①该蛋白得到了成功地表达,制备的多克隆抗体与近江牡蛎类立克次体的总外膜蛋白产生了特异性的免疫反应,在目的蛋白位置出现了单一的免疫反应条带,表明已经获得了类立克次体外膜蛋白ompR。②ompR诱导刺激后,宿主免疫相关因子Myd88和TNF-α的表达水平发生了明显变化,而TGF-β基因的表达水平不受影响；在转录后水平上的调控表现为刺激后血淋巴细胞中P38的磷酸化水平明显地增加,JNK的磷酸化水平急剧下降,而ERK的磷酸化水平无变化；同时核转录因子NF-κB的DNA结合活性的明显增加,而P38激酶抑制剂可显著地抑制该结合活性。
在前面研究基础上,我们进一步克隆鉴定了近江牡蛎的LITAF(LPS-induced TNF-α),并对其功能进行了初步研究。Ca-LITAF全长750 bp,具有一个348 bp的读码框,编码一个分子量大小约为12.5 kDa的蛋白。该蛋白具有Zn2+结合区(CXXC和HXCXXC)和LITAF结构域等特征性结构,与其它动物的LITAF蛋白的相似度介于33%和96%之间,其中与无脊椎动物太平洋长牡蛎和扇贝的LITAF蛋白具较高同源性,同属一个亚群。实时定量PCR结果显示：Ca-LITAF在各被检组织中均有表达,在鳃和血淋巴细胞的表达量要高于其它组织,类立克次体诱导刺激后血淋巴细胞中Ca-LITAF的表达明显增强,表明Ca-LITAF与病原诱导的宿主免疫反应有关。综合上述结果,病原/MAPKs/NF-κB (CREB)信号途径可能存在于牡蛎天然免疫系统中,对抵抗外来病原的入侵起着重要作用。
Currently, interaction between pathogen and host is a key topic in the frontier of microbiology and immunology in the world. Rickettsia-like organisms (RLOs) are obligate intracellular Gram-negative bacteria and caused mass mortality of oysters. However, little is known about the molecular biology and pathogenesis of rickettsia-like organism The studies on the molecular biology of pathogen rickettsia-like organism interaction with its host, oyster Crassostrea ariakensis were carried out in this scientific dissertation including the immune function and mechanism of transcription factors CREB and LITAF of oyster responsed to RLO stimulation, and signal pathways involved in the host defense under the induction of RLO outer membrane protein ompR.
RNA was extracted from hemocytes of oyster stimulated by RLO using TRIzol method and was reverse transcribed into cDNA. Degenerate oligonucleotide primers were designed for RT-PCR and RACE-PCR. Here, we first report that a homologue of CREB, Ca-CREB, was identified and functionally characterized in bivalves. The full-length cDNA of Ca-CREB contains an ORF of 1068 bp encoding a 39.3 kDa protein. Amino acid sequence analysis revealed that Ca-CREB shares conserved signature motifs with other CREB proteins and is highly homologous to Lymnaea stagnalis (56%) and Aplysia californica (58%). The expression level of Ca-CREB in various tissues was investigated by RT-PCR. The results showed that Ca-CREB was ubiquitously expressed in all examined tissues, and expression levels in gills and hemocytes were higher than the others, suggesting that may be involved in immune responses. To investigate the biological activity and functions of Ca-CREB, the recombinant plasmids (pET-CREB) were constructed and identified by sequencing, then transformed into competent cells for expression. The recombinant fusion proteins were purified by affinity chromatography, then the antiserum against New Zealand White rabbits was prepared and the activity of recombinant protein was determined by EMSA. The results of SDS-PAGE. real time RT-PCR.Western blotting and EMSA showed that:①recombinant protein Ca-CREB was successfully expressed in E. coli and purified fusion protein had the specific DNA binding activity.②no obvious changes in the expression level of Ca-CREB in the hemocytes were found after RLO challenge while DNA binding activity and the phosphorylation level of CREB were remarkably modified. The results demonstrated that Ca-CREB was regulated at the protein level, instead of the mRNA level, after RLO stimulation, suggesting that Ca-CREB is involved in immune responses against RLO. To find out the cause of the different migration in the molecular weight of recombinant protein Ca-CREB analyzed by SDS-PAGE method, another experiment was performed from different aspects such as vectors, the concentration of gels and the conditions of electrophoresis. According to our study, different expression vectors and concentrations of gels had no effects on the different migration while different electrophoresis system did.
Condering that the host immune responses has been elicited by RLO which was confirmed as above, we decided to carry out the further experiments to investigate whether or not some proteins from RLO could be involved in the immune responses. So it was considered to start a project on studies of the protein of RLO, especially the outer membrane protein of RLO. A DNA fragment of 531 bp encoding ompR was obtained by sequencing the genomic DNA of rickettsia-like organism. It encodes 176 amino acid residues containing a signal peptide and a transmembrane region. Theoretical isoelectric point and molecular weight for this protein are 9.76 and 19.76 kDa, respectively. Comparison of ompR in overall sequence with ompH proteins of Rickettsia grylli, Coxiella burnetii and Thiomicrospira crunogena revealed a similarity ranging from 20%to 27%. Construction of the recombinant plasmid pET-ompR, purification of the recombinant protein and preparation of the antibody against recombinant ompR protein was conducted as described above. The results showed that:①the recombinant ompR was successfully expressed in E. coli cells, a specific immunoreactive band was detected when anti-ompR antibody was opposed to the total outer membrane proteins of RLO.②The expression level of TNF-a and Myd88 in hemocytes was induced by ompR, whereas TGF-(3 was not; a rapid and persistent increase in the level of phosphorylated P38 and a large decrease in the level of phosphorylated JNK were induced by ompR. while the level of phosphorylated ERK did not change with ompR incubation. Meanwhile, the DNA binding activity of NF-κB in hemocytes increased after ompR stimulation, but it was inhibited by addition of inhibitor for P38 MAPK.
Based on our previous studies, a novel gene, Ca-LITAF, and its function in the immune response against RLO was also investigated. The full-length cDNA consists of 750 bp with an ORF of 348 bp encoding a 12.5 kDa protein. Amino acid sequence analysis revealed that Ca-LITAF shares conserved Zn2+ binding domain and LITAF domain. A similarity ranging from 33% to 96% in the entire sequence was revealed by comparison with LITAF proteins from various animals and Cα-LITAF was highly homologous to Crassostrea gigas and Chlamys farreri. As RT-PCR indicated, Ca-LITAF was ubiquitously expressed in all examined tissues, and expression levels in gills and hemocytes were higher than that in the others. Meanwhile, obvious changes in the expression level of Ca-LITAF were found after RLO challenge, suggesting that it may be involved in immune responses.
All together, we could draw the conclusion that pathogen/MAPKs/NF-κB (CREB) pathway may exist in the immune system of C. ariakensis and play an immportant role in the immune response against RLO infection.
取类立克次体诱导刺激后的近江牡蛎血淋巴细胞,采用TRIzol法提取RNA,制备cDNA模板。根据CREB蛋白的保守结构特征设计了兼并寡聚核苷酸引物,采用RT-PCR和RACE PCR技术首次在双壳贝类中获得了Ca-CREB的全长cDNA序列。该cDNA序列含有一个1068 bp的读码框,编码一个39.3 kDa的蛋白,该蛋白具有转录因子CREB的特征性结构,与无脊椎动物海兔和蜗牛的CREB同源性较高,相似度分别为56%和58%。组织半定量RT-PCR结果表明：Ca-CREB在各组织中均有表达,但在血细胞和鳃中的表达量明显高于其它组织,预示该基因可能与免疫调节有关。通过构建重组表达质粒pET-CREB,在大肠杆菌中对Ca-CREB进行了诱导表达、蛋白纯化并制备了多克隆抗体,同时利用凝胶阻滞技术(EMSA)对重组蛋白的活性进行了研究。随后采用Real time RT-PCR、Western blotting和EMSA技术探讨了Ca-CREB在类立克次体诱导刺激条件下的激活机理及功能。结果表明：①Ca-CREB在大肠杆菌中得到了高效表达,获得的重组蛋白具有特异的DNA结合活性,制备的兔多克隆抗体的效价为1:12000。②在类立克次体诱导刺激不同时间段内,血淋巴细胞中Ca-CREB的基因表达水平没有显著差异,而Ca-CREB的DNA结合活性和磷酸化水平得到了明显提高,这表明核转录因子Ca-CREB在类立克次体诱导的宿主免疫反应中具有功能,且这种功能的激活发生在转录后水平上。接着,我们分别从表达载体、胶浓度及电泳条件等方面着手,对Ca-CREB原核表达产物比预测蛋白分子量偏大的原因进行了分析,结果表明：不同的表达载体及胶浓度对Ca-CREB融合蛋白在SDS-PAGE中表现的分子量大小没有影响,而不同SDS-PAGE体系分离融合蛋白时产生了融合分子量偏小的现象,推测不同的SDS-PAGE体系与分子量偏差的产生有关。
鉴于类立克次体在菌体细胞水平上能够诱导刺激宿主发生上述免疫反应,为深入探讨类立克次体在蛋白分子水平上是否能够诱导刺激宿主的分子免疫反应机制及信号传导途径,本实验通过基因组测序方法获得了首个贝类类立克次体病原的外膜蛋白ompR基因并研究了其免疫功能。该基因全长531bp,编码176个氨基酸,预测的蛋白分子量和等电点分别为19.76 KDa和9.76。核酸和氨基酸序列分析表明该蛋白具有细菌外膜蛋白的特征,与人Q热立克次体和潮虫立克次体外膜蛋白ompH具有20%-27%的相似性。随后以上述同样方法进行了ompR重组蛋白的表达、纯化和多克隆抗体的制备。在功能研究上,采用实时定量PCR、EMSA等技术手段分析了ompR诱导刺激后,宿主多个免疫相关因子的免疫反应机制及信号传导,结果显示：①该蛋白得到了成功地表达,制备的多克隆抗体与近江牡蛎类立克次体的总外膜蛋白产生了特异性的免疫反应,在目的蛋白位置出现了单一的免疫反应条带,表明已经获得了类立克次体外膜蛋白ompR。②ompR诱导刺激后,宿主免疫相关因子Myd88和TNF-α的表达水平发生了明显变化,而TGF-β基因的表达水平不受影响；在转录后水平上的调控表现为刺激后血淋巴细胞中P38的磷酸化水平明显地增加,JNK的磷酸化水平急剧下降,而ERK的磷酸化水平无变化；同时核转录因子NF-κB的DNA结合活性的明显增加,而P38激酶抑制剂可显著地抑制该结合活性。
在前面研究基础上,我们进一步克隆鉴定了近江牡蛎的LITAF(LPS-induced TNF-α),并对其功能进行了初步研究。Ca-LITAF全长750 bp,具有一个348 bp的读码框,编码一个分子量大小约为12.5 kDa的蛋白。该蛋白具有Zn2+结合区(CXXC和HXCXXC)和LITAF结构域等特征性结构,与其它动物的LITAF蛋白的相似度介于33%和96%之间,其中与无脊椎动物太平洋长牡蛎和扇贝的LITAF蛋白具较高同源性,同属一个亚群。实时定量PCR结果显示：Ca-LITAF在各被检组织中均有表达,在鳃和血淋巴细胞的表达量要高于其它组织,类立克次体诱导刺激后血淋巴细胞中Ca-LITAF的表达明显增强,表明Ca-LITAF与病原诱导的宿主免疫反应有关。综合上述结果,病原/MAPKs/NF-κB (CREB)信号途径可能存在于牡蛎天然免疫系统中,对抵抗外来病原的入侵起着重要作用。
Currently, interaction between pathogen and host is a key topic in the frontier of microbiology and immunology in the world. Rickettsia-like organisms (RLOs) are obligate intracellular Gram-negative bacteria and caused mass mortality of oysters. However, little is known about the molecular biology and pathogenesis of rickettsia-like organism The studies on the molecular biology of pathogen rickettsia-like organism interaction with its host, oyster Crassostrea ariakensis were carried out in this scientific dissertation including the immune function and mechanism of transcription factors CREB and LITAF of oyster responsed to RLO stimulation, and signal pathways involved in the host defense under the induction of RLO outer membrane protein ompR.
RNA was extracted from hemocytes of oyster stimulated by RLO using TRIzol method and was reverse transcribed into cDNA. Degenerate oligonucleotide primers were designed for RT-PCR and RACE-PCR. Here, we first report that a homologue of CREB, Ca-CREB, was identified and functionally characterized in bivalves. The full-length cDNA of Ca-CREB contains an ORF of 1068 bp encoding a 39.3 kDa protein. Amino acid sequence analysis revealed that Ca-CREB shares conserved signature motifs with other CREB proteins and is highly homologous to Lymnaea stagnalis (56%) and Aplysia californica (58%). The expression level of Ca-CREB in various tissues was investigated by RT-PCR. The results showed that Ca-CREB was ubiquitously expressed in all examined tissues, and expression levels in gills and hemocytes were higher than the others, suggesting that may be involved in immune responses. To investigate the biological activity and functions of Ca-CREB, the recombinant plasmids (pET-CREB) were constructed and identified by sequencing, then transformed into competent cells for expression. The recombinant fusion proteins were purified by affinity chromatography, then the antiserum against New Zealand White rabbits was prepared and the activity of recombinant protein was determined by EMSA. The results of SDS-PAGE. real time RT-PCR.Western blotting and EMSA showed that:①recombinant protein Ca-CREB was successfully expressed in E. coli and purified fusion protein had the specific DNA binding activity.②no obvious changes in the expression level of Ca-CREB in the hemocytes were found after RLO challenge while DNA binding activity and the phosphorylation level of CREB were remarkably modified. The results demonstrated that Ca-CREB was regulated at the protein level, instead of the mRNA level, after RLO stimulation, suggesting that Ca-CREB is involved in immune responses against RLO. To find out the cause of the different migration in the molecular weight of recombinant protein Ca-CREB analyzed by SDS-PAGE method, another experiment was performed from different aspects such as vectors, the concentration of gels and the conditions of electrophoresis. According to our study, different expression vectors and concentrations of gels had no effects on the different migration while different electrophoresis system did.
Condering that the host immune responses has been elicited by RLO which was confirmed as above, we decided to carry out the further experiments to investigate whether or not some proteins from RLO could be involved in the immune responses. So it was considered to start a project on studies of the protein of RLO, especially the outer membrane protein of RLO. A DNA fragment of 531 bp encoding ompR was obtained by sequencing the genomic DNA of rickettsia-like organism. It encodes 176 amino acid residues containing a signal peptide and a transmembrane region. Theoretical isoelectric point and molecular weight for this protein are 9.76 and 19.76 kDa, respectively. Comparison of ompR in overall sequence with ompH proteins of Rickettsia grylli, Coxiella burnetii and Thiomicrospira crunogena revealed a similarity ranging from 20%to 27%. Construction of the recombinant plasmid pET-ompR, purification of the recombinant protein and preparation of the antibody against recombinant ompR protein was conducted as described above. The results showed that:①the recombinant ompR was successfully expressed in E. coli cells, a specific immunoreactive band was detected when anti-ompR antibody was opposed to the total outer membrane proteins of RLO.②The expression level of TNF-a and Myd88 in hemocytes was induced by ompR, whereas TGF-(3 was not; a rapid and persistent increase in the level of phosphorylated P38 and a large decrease in the level of phosphorylated JNK were induced by ompR. while the level of phosphorylated ERK did not change with ompR incubation. Meanwhile, the DNA binding activity of NF-κB in hemocytes increased after ompR stimulation, but it was inhibited by addition of inhibitor for P38 MAPK.
Based on our previous studies, a novel gene, Ca-LITAF, and its function in the immune response against RLO was also investigated. The full-length cDNA consists of 750 bp with an ORF of 348 bp encoding a 12.5 kDa protein. Amino acid sequence analysis revealed that Ca-LITAF shares conserved Zn2+ binding domain and LITAF domain. A similarity ranging from 33% to 96% in the entire sequence was revealed by comparison with LITAF proteins from various animals and Cα-LITAF was highly homologous to Crassostrea gigas and Chlamys farreri. As RT-PCR indicated, Ca-LITAF was ubiquitously expressed in all examined tissues, and expression levels in gills and hemocytes were higher than that in the others. Meanwhile, obvious changes in the expression level of Ca-LITAF were found after RLO challenge, suggesting that it may be involved in immune responses.
All together, we could draw the conclusion that pathogen/MAPKs/NF-κB (CREB) pathway may exist in the immune system of C. ariakensis and play an immportant role in the immune response against RLO infection.
引文
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