家蚕生殖细胞发生与胚胎发育相关功能基因的蛋白质组研究
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摘要
昆虫的生殖和胚胎发育是生命科学很重要的命题。家蚕是一种重要的经济昆虫和鳞翅目模式昆虫。了解家蚕的生殖和胚胎发育,对人类提高家蚕经济价值,利用自然界有益昆虫以及防治有害昆虫具有重要的理论意义和实用价值。随着家蚕基因组草图和精细图的完成,家蚕基因组研究进入后基因组时代,即以研究整个基因组的功能及生物学意义为目标。蛋白质组学是后基因组时代的研究热点。蛋白质作为基因表达的产物,生命过程的直接执行者,蛋白质组学成为基因功能注释很重要的方法。本研究用蛋白质组学方法研究了家蚕五龄期幼虫性腺蛋白质组表达谱与家蚕性连锁胚胎期致死突变体胚胎蛋白质组表达谱,通过生物信息学对鉴定蛋白的功能和调控路径进行了分析,挖掘其在生殖细胞发生和胚胎发育中的作用。本研究主要的内容和结果如下：
(1)用shotgun的策略研究了家蚕P50品种五龄第5天幼虫精巢和卵巢组织的蛋白质组。分别以0.35%和0.49%的假阳性率(FDR)在精巢和卵巢中鉴定了285个和205个非冗余蛋白。通过对家蚕精巢和卵巢的蛋白质组表达谱比较,在鉴定的蛋白里面,有92个是精巢和卵巢共表达的,其余194个和113个分别为精巢和卵巢特异表达的。发现核糖体蛋白(Ribosomal proteins)是精巢和卵巢中鉴定最多的蛋白家族。核糖体是合成新蛋白的场所,暗示生殖细胞正在进行活跃的增殖和生长。根据多肽片段的光谱数目,Apolipophorin是精巢和卵巢中含量都较高的蛋白,暗示脂蛋白在精子和卵子发生过程中的重要作用。细胞视黄酸结合蛋白Cellular retinoic acid binding protein (CRABP)是家蚕精巢中丰度极高的蛋白。14-3-3epsilon protein是精巢中丰度较高的蛋白,暗示这些蛋白在精子形成过程中具有重要作用。发现多种30K蛋白家族成员在精巢中表达,暗示30K蛋白在家蚕精子形成过程中的作用。在卵巢中丰度较高的是微管蛋白(Tubulins),暗示微管蛋白在家蚕卵子发生过程中具有重要功能。对果蝇卵子发生过程的研究已揭示微管蛋白是卵母细胞确定、(胚胎发育)体轴建立以及运输母性RNA和蛋白所必需的,我们推测在家蚕卵子发生过程中可能也起这些重要功能。
(2)一些在果蝇生殖细胞发育过程中很关键的基因蛋白也在家蚕中鉴定到同源蛋白。比如精巢中的减数分裂阻滞基因ALY与VISMAY,在卵巢中的胚胎发育形态素定位蛋白Exuperantia和Squid蛋白,表明家蚕和果蝇在精子分化和卵子发生等关键过程具有生物的保守性。
(3)对精巢和卵巢共表达及特异表达蛋白进行生物信息学分析,揭示了家蚕精细胞和卵细胞形成相关的功能蛋白与生物学路径。基因本体(gene ontology)注释发现精巢和卵巢蛋白功能类没有较大差异,只有较少的类比如营养储存是卵巢特异的功能类。生物学路径分析发现细胞凋亡(apoptosis)、细胞周期(cell cycle).分化(differentiation).胚胎发生(embryogenesis).成熟(maturation).形态发生(morphogenesis)和迁移(migration)都是在精巢和卵巢中较丰富的生物学过程,表明精子和卵子发生的一般过程具有相似性,而相似的过程中特异的蛋白造成了最终精子和卵子在形态和功能上的差异。通过KEGG pathway分析发现涉及能量产生路径的蛋白在精巢中最丰富,这与精子需要动力的能量需求相一致。
(4)对鉴定的精巢和卵巢部分蛋白进行了其基因在mRNA水平与蛋白水平相对表达量一致性的观察,发现一些基因在mRNA和蛋白水平的不一致。比如,fibroinase (BCP)和ALY在蛋白水平显示为精巢特异的,但它们的mRNA丰度在卵巢中比精巢中高。MLE protein (MLE)和cytochrome P4509G3(Cyp9g3),在蛋白水平显示是卵巢特异的,而在转录水平上,精巢中的表达丰度比在卵巢中要高。这些结果表明这些基因可能存在转录后调控。把我们蛋白鉴定的结果和基因芯片数据比较,发现很多蛋白基因都存在转录后调控现象,表明转录后调控在生殖细胞发生过程中是一个较普遍的现象。
(5)对鉴定的精巢和卵巢蛋白基因进行染色体定位,发现性染色体含有更多精巢特异的蛋白基因,并且这些蛋白对精子的功能是必需的。
(6)以性连锁平衡致死系自交系平2品种雌性胚胎为材料,用双向电泳蛋白质组学方法研究了致死基因l2的致死作用机理。通过对致死时期前致死胚胎和存活胚胎间的双向电泳蛋白质组表达谱比较,寻找在致死基因作用下蛋白质组表达的变化。致死时期的确定通过对致死胚胎特征性形态观察确定。致死时期前存活胚胎和致死胚胎的区分通过用与致死基因l2紧密连锁的多态性SSR标记进行鉴别区分。最终存活胚胎和致死胚胎间11个差异表达的蛋白点通过MALDI-TOF/TOF被成功鉴定。在这些鉴定的蛋白中,只有一个点在致死胚胎中总是上调表达,该蛋白点被鉴定为热激蛋白HSP20.4。推测小热激蛋白HSP20.4可能是致死基因作用下应激而上调表达,小热激蛋白主要起分子伴侣的作用,也有研究证明有些小热激蛋白与膜相关,起保护膜的作用,暗示致死胚胎中可能存在异常蛋白或者膜的损伤。对其余10个下调的蛋白进行GO功能分类注释发现它们参与胚胎发育、核苷代谢、tRNA剪切、翻译和蛋白折叠等功能。对这些下调蛋白进行生物学调控网络分析,发现这些蛋白主要参与纺锤体装配和形态发生等生物学过程。根据这些结果,我们推测l2的表达一定程度上影响了胚胎发育过程中的有丝分裂和形态发生过程。
本研究结果丰富了家蚕性腺蛋白质组及家蚕胚胎发育功能基因组的信息,为阐明一些与家蚕生殖细胞发生与分化,以及胚胎发育相关的功能基因提供了蛋白质组水平的信息。更深层次地讲,我们家蚕性腺蛋白质组的结果也为家蚕性别决定机制提供了较丰富的蛋白质组水平的背景信息。
Reproduction and embryo development is the important field of life science. Silkworm is an economically important insects and Lepidopteran model. The knowledge of reproduction and embryo development in silkworm will facilitate the human in utilizing the beneficial insects and controlling the pest. With the completion of silkworm genome sequence, the functional genomics become the focus. Proteins, the products of genes, are the real executor in life processes. Therefore, proteomics has become one of major methods for functional genomics. Here, we used proteomics to study the proteome profile of silkworm gonads and sex-linked embryo lethal mutant embryos. The function and regulation network of those proteins identified were revealed using bioinformatics analysis, their roles in silkworm gametogenesis and embryo development were discussed. The main results are as follows:
(1) Shotgun proteomics were used to profile the proteome of silkworm larval gonads at the fifth day of the fifth instar. Totally286and205non-redundant proteins were identified from silkworm testis and ovary, respectively, with false discovery rate (FDR) of0.35%and0.49%. Of those,92proteins were detected in both tissues, while194and113proteins were sex-specific. Ribosomal proteins were the most enriched are protein family both in testis and ovary, indicating active cell growth and proliferation in gametogenesis. Apolipophorin was the abundant proteins both in testis and ovary, giving a clue that lipoprotein has a role in spermatogenesis and oogenesis. According to the spectral count, cellular retinoic acid binding protein (CRABP) showed to be very high-abundant in testis and14-3-3epsilon protein is abundant in testis.30K proteins, one of the major plasma protein groups, were identified in testis specifically. Those abundant proteins in testis may be critical for spermatogenesis. Tubulins showed to be abundant in ovary. This may be consistent with the fundamental roles of tubulins in oogenesis. Tubulins have been revealed to participate in the oocyte specification, axis formation and transport of maternal mRNA and proteins in Drosophila melanogaster.
(2) Several Drosophila essential proteins for gametogenesis were also identified their homologies in silkworm, such as male meiotic arrest gene product ALY and vismay in testis, and maternal mRNA localization protein exuperantia and squid in ovary. Those identifications reveal the conservation in spermatogenesis and oogenesis between Bombyx mori and Drosophila melanogaster.
(3) The bioinformatics analysis on the common and sex-specific proteins provides system-level insights into the sexual dimorphism and gametogenesis. For example, the nutrient reservoir is the ovary-specific function category, while energy generation pathway enriched in testis.
(4) The correlation of expression between mRNA and protein level of eleven genes were explored. Those11proteins genes representing common and sex-specifically expression were selected for qRT-PCR analysis. The qRT-PCR results showed discrepancy of some genes between mRNA and protein level. For instance, fibroinase (Bcp) and ALY showed testis-specific expression at protein level (Figure2A), while their mRNA abundance were higher in ovary than testis. MLE protein (MLE) and cytochrome P4509G3(Cyp9g3), showed ovary-specific at protein level, while expressed higher abundance in testis than in ovary at transcriptional level. Those results suggest post-transcriptional regulation of those genes may occur. We also compared our identification with the microarray-based studies performed by Xia et al. The discrepancy between mRNA and protein level indicated the occurrence of post-transtriptional regulations on many genes.
(5) The chromosome contribution of our identified proteins was investigated. All the common, testis-and ovary-specific genes were mapped onto the silkworm chromosomes. The testis-specific genes were higher than the ovary-specific genes on the sex chromosome, showed that the Z chromosome contains more testis-specific genes as revealed at transcriptional level. Furthermore, those testis-specific proteins showed to have crucial roles in spermatogenesis.
(6) To gain insight into the effect of one embryo-lethal gene l2, comparative proteomic analysis was carried out between the survival embryos and lethal embryos of the sex-linked balanced lethal (SLBL) strains of silkworm before the lethal stage. The lethal stage of h was confirmed by observing the typical dead embryo morphology. The two genotype embryos before lethal stage were distinguished using polymorphic simple sequence repeats (SSR) markers closely linked to l2on the sex chromosome. Finally,11differentially expressed protein spots were successfully identified by MALDI-TOF/TOF mass spectrometry (MS). Among them, only1protein identified as heat shock protein20.4(HSP20.4) was up-regulated in the lethal embryos, while the other10were down-regulated. Small heat shock proteins act as the molecular chaperon, having a role in protein folding. They were also evidenced to have a role in association with membrane protection. The up-regulation of HSP20.4suggests that there may be abnormal polypeptides or membrane harm in the lethal embryos. The gene ontology (GO) annotation indicated those down-regulated proteins are involved in important biological processes including embryo development, nucleoside metabolism, tRNA splicing, translation and protein folding. The biological pathway analysis showed that those down-regulated proteins are mainly involved in spindle assemblage and morphogenesis. Based on our results, we suggest that the expression of l2may be has a negative effect on mitosis and morphogenesis processes.
Our data enriched the information of silkworm gonad proteomics and functional genome in silkworm embryo development. Those gonad proteome data further provide valuable background for silkworm gametogenesis and sex determination.
(1)用shotgun的策略研究了家蚕P50品种五龄第5天幼虫精巢和卵巢组织的蛋白质组。分别以0.35%和0.49%的假阳性率(FDR)在精巢和卵巢中鉴定了285个和205个非冗余蛋白。通过对家蚕精巢和卵巢的蛋白质组表达谱比较,在鉴定的蛋白里面,有92个是精巢和卵巢共表达的,其余194个和113个分别为精巢和卵巢特异表达的。发现核糖体蛋白(Ribosomal proteins)是精巢和卵巢中鉴定最多的蛋白家族。核糖体是合成新蛋白的场所,暗示生殖细胞正在进行活跃的增殖和生长。根据多肽片段的光谱数目,Apolipophorin是精巢和卵巢中含量都较高的蛋白,暗示脂蛋白在精子和卵子发生过程中的重要作用。细胞视黄酸结合蛋白Cellular retinoic acid binding protein (CRABP)是家蚕精巢中丰度极高的蛋白。14-3-3epsilon protein是精巢中丰度较高的蛋白,暗示这些蛋白在精子形成过程中具有重要作用。发现多种30K蛋白家族成员在精巢中表达,暗示30K蛋白在家蚕精子形成过程中的作用。在卵巢中丰度较高的是微管蛋白(Tubulins),暗示微管蛋白在家蚕卵子发生过程中具有重要功能。对果蝇卵子发生过程的研究已揭示微管蛋白是卵母细胞确定、(胚胎发育)体轴建立以及运输母性RNA和蛋白所必需的,我们推测在家蚕卵子发生过程中可能也起这些重要功能。
(2)一些在果蝇生殖细胞发育过程中很关键的基因蛋白也在家蚕中鉴定到同源蛋白。比如精巢中的减数分裂阻滞基因ALY与VISMAY,在卵巢中的胚胎发育形态素定位蛋白Exuperantia和Squid蛋白,表明家蚕和果蝇在精子分化和卵子发生等关键过程具有生物的保守性。
(3)对精巢和卵巢共表达及特异表达蛋白进行生物信息学分析,揭示了家蚕精细胞和卵细胞形成相关的功能蛋白与生物学路径。基因本体(gene ontology)注释发现精巢和卵巢蛋白功能类没有较大差异,只有较少的类比如营养储存是卵巢特异的功能类。生物学路径分析发现细胞凋亡(apoptosis)、细胞周期(cell cycle).分化(differentiation).胚胎发生(embryogenesis).成熟(maturation).形态发生(morphogenesis)和迁移(migration)都是在精巢和卵巢中较丰富的生物学过程,表明精子和卵子发生的一般过程具有相似性,而相似的过程中特异的蛋白造成了最终精子和卵子在形态和功能上的差异。通过KEGG pathway分析发现涉及能量产生路径的蛋白在精巢中最丰富,这与精子需要动力的能量需求相一致。
(4)对鉴定的精巢和卵巢部分蛋白进行了其基因在mRNA水平与蛋白水平相对表达量一致性的观察,发现一些基因在mRNA和蛋白水平的不一致。比如,fibroinase (BCP)和ALY在蛋白水平显示为精巢特异的,但它们的mRNA丰度在卵巢中比精巢中高。MLE protein (MLE)和cytochrome P4509G3(Cyp9g3),在蛋白水平显示是卵巢特异的,而在转录水平上,精巢中的表达丰度比在卵巢中要高。这些结果表明这些基因可能存在转录后调控。把我们蛋白鉴定的结果和基因芯片数据比较,发现很多蛋白基因都存在转录后调控现象,表明转录后调控在生殖细胞发生过程中是一个较普遍的现象。
(5)对鉴定的精巢和卵巢蛋白基因进行染色体定位,发现性染色体含有更多精巢特异的蛋白基因,并且这些蛋白对精子的功能是必需的。
(6)以性连锁平衡致死系自交系平2品种雌性胚胎为材料,用双向电泳蛋白质组学方法研究了致死基因l2的致死作用机理。通过对致死时期前致死胚胎和存活胚胎间的双向电泳蛋白质组表达谱比较,寻找在致死基因作用下蛋白质组表达的变化。致死时期的确定通过对致死胚胎特征性形态观察确定。致死时期前存活胚胎和致死胚胎的区分通过用与致死基因l2紧密连锁的多态性SSR标记进行鉴别区分。最终存活胚胎和致死胚胎间11个差异表达的蛋白点通过MALDI-TOF/TOF被成功鉴定。在这些鉴定的蛋白中,只有一个点在致死胚胎中总是上调表达,该蛋白点被鉴定为热激蛋白HSP20.4。推测小热激蛋白HSP20.4可能是致死基因作用下应激而上调表达,小热激蛋白主要起分子伴侣的作用,也有研究证明有些小热激蛋白与膜相关,起保护膜的作用,暗示致死胚胎中可能存在异常蛋白或者膜的损伤。对其余10个下调的蛋白进行GO功能分类注释发现它们参与胚胎发育、核苷代谢、tRNA剪切、翻译和蛋白折叠等功能。对这些下调蛋白进行生物学调控网络分析,发现这些蛋白主要参与纺锤体装配和形态发生等生物学过程。根据这些结果,我们推测l2的表达一定程度上影响了胚胎发育过程中的有丝分裂和形态发生过程。
本研究结果丰富了家蚕性腺蛋白质组及家蚕胚胎发育功能基因组的信息,为阐明一些与家蚕生殖细胞发生与分化,以及胚胎发育相关的功能基因提供了蛋白质组水平的信息。更深层次地讲,我们家蚕性腺蛋白质组的结果也为家蚕性别决定机制提供了较丰富的蛋白质组水平的背景信息。
Reproduction and embryo development is the important field of life science. Silkworm is an economically important insects and Lepidopteran model. The knowledge of reproduction and embryo development in silkworm will facilitate the human in utilizing the beneficial insects and controlling the pest. With the completion of silkworm genome sequence, the functional genomics become the focus. Proteins, the products of genes, are the real executor in life processes. Therefore, proteomics has become one of major methods for functional genomics. Here, we used proteomics to study the proteome profile of silkworm gonads and sex-linked embryo lethal mutant embryos. The function and regulation network of those proteins identified were revealed using bioinformatics analysis, their roles in silkworm gametogenesis and embryo development were discussed. The main results are as follows:
(1) Shotgun proteomics were used to profile the proteome of silkworm larval gonads at the fifth day of the fifth instar. Totally286and205non-redundant proteins were identified from silkworm testis and ovary, respectively, with false discovery rate (FDR) of0.35%and0.49%. Of those,92proteins were detected in both tissues, while194and113proteins were sex-specific. Ribosomal proteins were the most enriched are protein family both in testis and ovary, indicating active cell growth and proliferation in gametogenesis. Apolipophorin was the abundant proteins both in testis and ovary, giving a clue that lipoprotein has a role in spermatogenesis and oogenesis. According to the spectral count, cellular retinoic acid binding protein (CRABP) showed to be very high-abundant in testis and14-3-3epsilon protein is abundant in testis.30K proteins, one of the major plasma protein groups, were identified in testis specifically. Those abundant proteins in testis may be critical for spermatogenesis. Tubulins showed to be abundant in ovary. This may be consistent with the fundamental roles of tubulins in oogenesis. Tubulins have been revealed to participate in the oocyte specification, axis formation and transport of maternal mRNA and proteins in Drosophila melanogaster.
(2) Several Drosophila essential proteins for gametogenesis were also identified their homologies in silkworm, such as male meiotic arrest gene product ALY and vismay in testis, and maternal mRNA localization protein exuperantia and squid in ovary. Those identifications reveal the conservation in spermatogenesis and oogenesis between Bombyx mori and Drosophila melanogaster.
(3) The bioinformatics analysis on the common and sex-specific proteins provides system-level insights into the sexual dimorphism and gametogenesis. For example, the nutrient reservoir is the ovary-specific function category, while energy generation pathway enriched in testis.
(4) The correlation of expression between mRNA and protein level of eleven genes were explored. Those11proteins genes representing common and sex-specifically expression were selected for qRT-PCR analysis. The qRT-PCR results showed discrepancy of some genes between mRNA and protein level. For instance, fibroinase (Bcp) and ALY showed testis-specific expression at protein level (Figure2A), while their mRNA abundance were higher in ovary than testis. MLE protein (MLE) and cytochrome P4509G3(Cyp9g3), showed ovary-specific at protein level, while expressed higher abundance in testis than in ovary at transcriptional level. Those results suggest post-transcriptional regulation of those genes may occur. We also compared our identification with the microarray-based studies performed by Xia et al. The discrepancy between mRNA and protein level indicated the occurrence of post-transtriptional regulations on many genes.
(5) The chromosome contribution of our identified proteins was investigated. All the common, testis-and ovary-specific genes were mapped onto the silkworm chromosomes. The testis-specific genes were higher than the ovary-specific genes on the sex chromosome, showed that the Z chromosome contains more testis-specific genes as revealed at transcriptional level. Furthermore, those testis-specific proteins showed to have crucial roles in spermatogenesis.
(6) To gain insight into the effect of one embryo-lethal gene l2, comparative proteomic analysis was carried out between the survival embryos and lethal embryos of the sex-linked balanced lethal (SLBL) strains of silkworm before the lethal stage. The lethal stage of h was confirmed by observing the typical dead embryo morphology. The two genotype embryos before lethal stage were distinguished using polymorphic simple sequence repeats (SSR) markers closely linked to l2on the sex chromosome. Finally,11differentially expressed protein spots were successfully identified by MALDI-TOF/TOF mass spectrometry (MS). Among them, only1protein identified as heat shock protein20.4(HSP20.4) was up-regulated in the lethal embryos, while the other10were down-regulated. Small heat shock proteins act as the molecular chaperon, having a role in protein folding. They were also evidenced to have a role in association with membrane protection. The up-regulation of HSP20.4suggests that there may be abnormal polypeptides or membrane harm in the lethal embryos. The gene ontology (GO) annotation indicated those down-regulated proteins are involved in important biological processes including embryo development, nucleoside metabolism, tRNA splicing, translation and protein folding. The biological pathway analysis showed that those down-regulated proteins are mainly involved in spindle assemblage and morphogenesis. Based on our results, we suggest that the expression of l2may be has a negative effect on mitosis and morphogenesis processes.
Our data enriched the information of silkworm gonad proteomics and functional genome in silkworm embryo development. Those gonad proteome data further provide valuable background for silkworm gametogenesis and sex determination.
引文
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