粪类圆线虫感染性Ⅲ期幼虫和寄生性雌虫miRNA的鉴定

doi:10.12140/j.issn.1000-7423.2023.04.003

中国寄生虫学与寄生虫病杂志 ›› 2023, Vol. 41 ›› Issue (4): 412-420.doi: 10.12140/j.issn.1000-7423.2023.04.003

粪类圆线虫感染性Ⅲ期幼虫和寄生性雌虫miRNA的鉴定

覃裴溪¹(), 周彩显¹, 鲁志刚¹^,², 张碧瀛¹, 周涛勋¹, 胡敏¹^,^*()

1 华中农业大学动物医学院农业微生物资源发掘与利用全国重点实验室，湖北武汉 430070
2 威康桑格研究所威康基因组校园，幸克斯顿，剑桥郡 CB10 1SA，英国

收稿日期:2022-10-26 修回日期:2022-12-02 出版日期:2023-08-30 发布日期:2023-09-06
通讯作者: *胡敏（1966-），女，博士，教授，从事寄生蠕虫发育调控机制、寄生线虫种群遗传和流行病学、捻转血矛线虫抗药性及疫苗开发。E-mail：mhu@mail.hzau.edu.cn
作者简介:覃裴溪（1995-），女，博士研究生，从事粪类圆线虫miRNA研究。E-mail: peixiqin@webmail.hzau.edu.cn
基金资助:
中央高校基本科研业务费专项基金(2662017PY084)

Identification of miRNAs in the infectious third stage larvae and parasitic female adult of Strongyloides stercoralis

QIN Peixi¹(), ZHOU Caixian¹, LU Zhigang¹^,², ZHANG Biying¹, ZHOU Taoxun¹, HU Min¹^,^*()

1 National Key Laboratory of Agricultural Microbiology Core Facility, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, Hubei, China
2 Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, CB10 1SA, UK

Received:2022-10-26 Revised:2022-12-02 Online:2023-08-30 Published:2023-09-06
Contact: *E-mail: mhu@mail.hzau.edu.cn
Supported by:
Fundamental Research Funds for the Central Universities(2662017PY084)

摘要/Abstract

摘要：

目的鉴定粪类圆线虫感染性Ⅲ期幼虫（iL₃）和寄生性雌虫（pF）的微小RNA（miRNA），分析差异表达miRNA及其靶基因的功能。方法从粪类圆线虫感染犬粪便中收集iL₃。取4 000~5 000条iL₃于颈后皮下注射感染健康犬，感染后21 d，从肠道中采集pF。提取iL₃和pF的总RNA并测序。测序数据与粪类圆线虫基因组和鼠类圆线虫miRNA比对筛选保守的miRNA，用miRDeep2通过颈环结构分析、成熟序列比对筛选miRNA。分析iL₃和pF的miRNA表达谱，筛选差异表达miRNA，预测差异表达miRNA的靶基因，对log₂（差异倍数）> 1和每百万转录本上的读数（TPM）> 1 000的未注释miRNA的靶基因功能进行分析。用ClusterProfiler对差异表达miRNA靶基因进行GO富集分析。选取11个未注释或保守的差异表达miRNA进行实时荧光定量PCR（qRT-PCR）验证，以粪类圆线虫甘油醛-3-磷酸脱氢酶基因（GenBank登录号：BI773092.1）为参照基因，计算差异表达miRNA的相对转录水平。结果共鉴定出265个miRNA，包括130个保守的miRNA和135个未注释的miRNA。其中，134个miRNA在iL₃和pF之间差异表达（包含77个保守的miRNA和57个未注释的miRNA），251个为iL₃和pF所共有，10个为iL₃特有，4个为pF特有。差异表达miRNA靶基因预测结果显示，57个未注释的miRNA中，有12个差异倍数 > 2且TPM > 1 000，有248个靶基因与秀丽隐杆线虫同源，其中35.08%（87/248）的靶基因与发育相关，其余与应激、运动和蜕皮等相关。大部分在pF高表达未注释的miRNA靶向SSTP_0000114700。差异表达miRNA靶基因的GO分析结果显示，共5 595个靶基因被富集，其中富集靶基因数居前5位的分别为膜组成成分（1 821个）、核酸结合（561个）、细胞核（450个）、蛋白质水解作用（365个）和信号传导（284个）。qRT-PCR验证结果显示，sst-miR-86-5p、sst-84-5p、sst-novel-104、sst-miR-92-3p、sst-miR-34a-3p、sst-miR-81a-5p、sst-miR-1-3p、sst-novel-108、sst-miR-124-5p、sst-miR-50-3p、sst-novel-51的log₂（差异倍数）分别为-2.13、6.39、4.46、-3.69、-3.69、2.34、-2.48、-2.41、-2.30、2.25、-3.32，转录组分析获得的log₂（差异倍数）分别为-3.05、4.98、4.07、-4.9、-3.66、0.98、-3.79、-2.61、-0.99、0.63、-1.55。qRT-PCR与转录组分析获得的上调、下调趋势结果一致。结论获得粪类圆线虫感染性Ⅲ期幼虫和寄生性雌虫的miRNA表达谱和差异表达miRNA，差异表达miRNA与粪类圆线虫的生长发育和繁殖功能相关。

关键词: 粪类圆线虫, 感染性Ⅲ期幼虫, 寄生性雌虫, miRNA

Abstract:

Objective To identify the microRNA (miRNA) of the Strongyloides stercoralis infective third-stage larvae (iL₃) and parasitic female adult (pF), and analyze the differential expression of miRNA and the function of their target genes. Methods The iL₃ was collected from the feces of dogs infected with S. stercoralis. Healthy dogs were subcutaneously injected with 4 000-5 000 iL₃ at the back of the neck. The pF was collected from the dog intestine 21 days post-infection. The total RNA of iL₃ and pF was extracted and sequenced. The sequencing data was aligned with the S. stercoralis genome and S. ratti miRNA to identify the conserved miRNA. The true miRNA sequences were screened out using miRDeep2 through loop structure analysis and mature sequence readings alignment. The miRNA expression profiles of iL₃ and pF were analyzed to screen the differentially expressed miRNA, and predict their target genes. Functional analysis was performed to those of unannotated miRNAs target genes with the values of log₂(Fold chang) > 1 and transcripts per million (TPM) > 1 000. GO enrichment analysis of differentially expressed miRNA target genes were analyzed using ClusterProfiler. Eleven unannotated or conserved differentially expressed miRNAs were selected for real-time fluorescent quantitative PCR (qRT-PCR) verification. The relative transcription level was calculated with the glyceraldehyde-3-phosphate dehydrogenase gene of S. stercoralis (GenBank accession number: BI773092.1) as reference gene. Results A total of 265 miRNA were identified, including 130 conserved miRNAs and 135 novel miRNAs, of them 134 were differentially expressed between iL₃ and pF (77 conserved and 57 unannotated miRNAs), 251 miRNAs were shared by iL₃ and pF, 10 were specific in iL₃ and 4 were specific in pF. The prediction results of differentially expressed miRNA target genes showed that of the 57 unannotated miRNA, 12 miRNA with fold chang > 2 and TPM > 1 000 have 248 target genes homologous with Caenorhabditis elegans. 35.08% (87/248) of the target genes were related to development, while the rest were related to stress, exercise and molting. Most of the highly expressed unannotated miRNA in pF target SSTP_0000114700. GO analysis of differentially expressed miRNA target genes showed that a total of 5 595 target genes were enriched, among which the top 5 enriched components were membrane components (1 821), nucleic acid binding (561), nucleus (450), proteolysis (365) and signal transduction (284). The qRT-PCR analysis showed that the log₂(fold change) of sst-miR-86-5p, sst-84-5p, sst-novel-104, sst-miR-92-3p, sst-miR-34a-3p, sst-miR-81a-5p, sst-miR-1-3p, sst-novel-108, sst-miR-124-5p, sst-miR-50-3p, sst-novel-51 were -2.12, 6.39, 4.46, -3.69, -3.69, 2.34, -2.48, -2.41, -2.30, 2.25, -3.32; and the log₂(fold change) obtained from transcriptome analysis were -3.05, 4.98, 4.07, -4.9, -3.66, 0.98, -3.79, -2.61, -0.99, 0.63, -1.55, respectively. The upregulation and downregulation trends obtained from qRT-PCR and transcriptome analysis are consistent. Conclusion The miRNA expression profiles and differentially expressed miRNAs of S. stercoralis infective third-stage larvae and parasitic female adult are identified. The differentially expressed miRNAs are associated with the growth, development, and reproductive function of S. stercoralis.

Key words: Strongyloides stercoralis, Infective third-stage larvae, Parasitic female adult, miRNA

中图分类号:

R383.19

覃裴溪, 周彩显, 鲁志刚, 张碧瀛, 周涛勋, 胡敏. 粪类圆线虫感染性Ⅲ期幼虫和寄生性雌虫miRNA的鉴定[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(4): 412-420.

QIN Peixi, ZHOU Caixian, LU Zhigang, ZHANG Biying, ZHOU Taoxun, HU Min. Identification of miRNAs in the infectious third stage larvae and parasitic female adult of Strongyloides stercoralis[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2023, 41(4): 412-420.

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参考文献 36

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引物名称 Primer name	引物序列（5'→3'） Primer sequence (5'→3')
sst-miR-86-5p-F	GCCGTAAGTGAATGCTTTGCCACAG
sst-miR-86-5p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-86-5p-loop	TCGCACTGGATACGACAGACTG
sst-miR-84-5p-F	CGGGCTGAGGTAGTGTTAAATATTG
sst-miR-84-5p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-84-5p-loop	TCGCACTGGATACGACAACAAT
sst-novel-104-F	CGGGCCTGAGGTAGTGTTAAATATTG
sst-novel-104-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-novel-104-loop	TCGCACTGGATACGACAACAAT
sst-miR-92-3p-F	CGTATTGCACACGTCCCG
sst-miR-92-3p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-92-3p-loop	TCGCACTGGATACGACTCAGGC
sst-miR-34a-3p-F	GCGCGACAGCTCACTCAACT
sst-miR-34a-3p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
TCGCACTGGATACGACCTTGGC
sst-miR-81a-5P-F	CGGGCATGGGTCTATATGATTCTC
sst-miR-81a-5P-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-81a-5P-loop	TCGCACTGGATACGACCATGAG
sst-miR-1-3p-F	CGCCCGTGGAATGTAAAGAAG
sst-miR-1-3p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-1-3p-loop	TCGCACTGGATACGACTGCATA
sst-novel-108-F	TTTGCGACCGAATCCAGGC
sst-novel-108-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-novel-108-loop	TCGCACTGGATACGACTGTGGC
sst-miR-124-5p-F	GCGCTTTCATCCGTGACTTTAG
sst-miR-124-5p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-124-5p-loop	TCGCACTGGATACGACCGACCT
sst-miR-50-3p-F	CGGCCCGCGAGTAATATTAGACATATCG
sst-miR-50-3p-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-miR-50-3p-loop	TCGCACTGGATACGACCTCGAT
sst-novel-51-F	TTAAGGCACGCGGTGAATG
sst-novel-51-loop	GTCGTATCCAGTGCAGGGTCCGAGGTAT-
sst-novel-51-loop	TCGCACTGGATACGACTTGGCA
sst-miRNA-R	AGTGCAGGGTCCGAGGTATT
sst-GAPDH-F	ACTGGTGCAGCTAAAGCTGTAGG
sst-GAPDH-loop	GTCGTATCCAGTGCAGGGTCCGAGG

样品名称 Sample name	原始序列 Raw sequence	总读数 Total bases	GC含量/% GC content/%	质量值大于20的碱基数占比% Q20/%	质量值大于20的碱基数占比% Q20/%	总匹配数 Total mapped	总匹配率/% Total mapped/%
iL₃-1	24 795 684	0.553 G	50.19	99.56	95.79	22 785 621	92.0
iL₃-2	24 937 291	0.550 G	48.53	99.49	95.04	22 400 131	89.8
iL₃-3	23 295 886	0.526 G	47.99	99.14	96.47	19 707 809	84.9
pF-1	23 853 139	0.533 G	49.26	99.52	95.90	13 335 379	56.2
pF-2	23 698 225	0.529 8 G	50.98	99.48	94.92	12 059 955	51.1
pF-3	23 735 746	0.544 G	49.43	99.43	94.78	12 608 177	53.7

miRNA名称miRNA name	log₂（差异倍数） log₂ (Fold change)	iL₃ TPM	pF TPM
sst-novel-108	-2.408	132 509	24 969
sst-novel-16	2.022	3 213	13 050
sst-novel-134	-1.600	21 202	6 996
sst-novel-117	-2.052	12 863	3 102
sst-novel-22	-1.799	3 548	1 020
sst-novel-18	1.983	2 330	9 209
sst-novel-9	-1.661	13 859	4 383
sst-novel-106	1.453	14 141	38 714
sst-novel-7	-2.531	18 005	3 115
sst-novel-120	1.326	2 698	6 766
sst-novel-19	-1.108	4 890	2 268
sst-novel-10	-1.202	13 289	5 774

粪类圆线虫感染性Ⅲ期幼虫和寄生性雌虫miRNA的鉴定

Identification of miRNAs in the infectious third stage larvae and parasitic female adult of Strongyloides stercoralis

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