The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from Biomphalaria glabrata
The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from Biomphalaria glabrata
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DOI：
10.1371/journal.pntd.0007013
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发表时间：
2019-09-01
影响因子：
3.8
通讯作者：
Loker, Eric S.
中科院分区：
文献类型：
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作者：
Buddenborg, Sarah K.;Kamel, Bishoy;Loker, Eric S.
背景血吸虫在虫体发育过程中表达的全部基因尚未被描述。了解血吸虫幼虫在其蜗牛宿主中部署的基因产物将有助于了解它们的建立、维持、无性繁殖、阉割宿主的能力以及它们大量产生人类感染性尾蚴的能力。利用Illumina平台，研究了曼氏血吸虫在感染后1天和3天以及从脱落尾蚴的蜗牛中提取的主要媒介物种菲费生物phalaria （Biomphalaria pfeifferi）野外采集的标本中曼氏血吸虫的蚓内转录组。这些曼氏梭菌样本来自于我们补充的普费费梭菌转录组学研究中使用的相同蜗牛。我们在2d、4d、8d、16d和32d对来自光斑贝的mansoni进行了微阵列分析，以补充这一观点，以突出mansoni转录的稳健特征，即使使用了不同的技术和载体物种。研究结果表明，至少7740个（66%）已知曼氏梭菌基因的转录本在软体动物发育过程中得到表达，其中在蜗牛蜕尾蚴过程中表达的数量最多。许多转录本在整个发育过程中都有组成性表达，包括膜转运蛋白，以及参与蛋白质和核酸合成和细胞分裂的代谢酶。几种蛋白酶和蛋白酶抑制剂在所有阶段均有表达，包括一些通常与尾蚴相关的蛋白酶。与g蛋白偶联受体、生殖细胞延续、应激反应和防御相关的转录本得到了很好的表达。我们注意到与涡虫抗菌因子同源的转录物，几种神经发育或神经肽转录物，包括神经肽Y，以及可能与血吸虫生发细胞维持相关的受体，这些受体也可能影响宿主生殖。在至少一种蜗牛中，另一种地根虫（一种amphistome）的幼虫的存在与mansoni转录活性的抑制有关。曼氏血吸虫是引起被忽视的热带病人肠道血吸虫病的重要血吸虫种之一。通过关注曼氏血吸虫及其广泛分布的撒哈拉以南非洲蜗牛中间宿主Biomphalaria pfeifferi，我们发现了这种宿主-寄生虫关系的新见解和基本知识，这对理解血吸虫病的传播至关重要。我们表明，在体内的研究，特别是强调现场衍生的标本，提供了一个不同的观点，从体外或离体研究中看到的转录反应的曼索尼血吸虫幼虫阶段。随着越来越多的人认为我们需要用其他控制方法来补充化疗，了解mansoni如何与它的强制性蜗牛宿主相互作用成为未来控制方案规划的一部分。本文提供的数据提供了关于血吸虫如何成功地保护自己免受宿主防御的具体分析，以及其放大无性繁殖所需的必要转录反应，从而导致人类感染性尾蚴。
Background The full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used. Principal findings Transcripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity.Author summary Schistosoma mansoni is one of the most important schistosome species causing the neglected tropical disease human intestinal schistosomiasis. By focusing on S. mansoni in vivo with its broadly distributed sub-Saharan African snail intermediate host, Biomphalaria pfeifferi, we uncover new insights and basic knowledge of this host-parasite relationship that are critical for understanding schistosomiasis transmission. We show that in vivo studies, particularly emphasizing field-derived specimens, provides a distinct view from the transcriptional responses previously seen from in vitro or ex vivo studies of S. mansoni larval stages. With the growing consensus that we need to supplement chemotherapy with other control methods, understanding how S. mansoni interacts with its obligatory snail host becomes integral for future planning of control programs. The data provided within provides specific analysis on how schistosomes successfully protect themselves from host defenses and the necessary transcriptional responses required for its amplifying asexual proliferation that result in human-infective cercariae.