miRNAs and lncRNAs in Echinococcus and Echinococcosis
Abstract
:1. Introduction
2. Widespread Expression of miRNAs in Echinococcus spp. According to Transcriptome Analysis
2.1. MiRNAs Expressed in Different Developmental Stages of E. granulosus Sensu Stricto
2.2. MiRNA Expression Profiles in E. canadensis
2.3. MiRNA Expression Patterns in E. multilocularis
2.4. Common miRNAs in Echinococcus spp.
3. Non-Coding RNAs in Intermediate Hosts during Infection with Echinococcus spp.
3.1. MiRNAs and lncRNAs in Host Responses to E. granulosus
3.2. Mouse miRNAs Dysregulated during Infection with E. multilocularis
3.3. Common miRNA Families in the Host Model during Infection with Echinococcus spp.
4. MiRNAs Mainly Associated with Immune and Pathological Processes during Host Infection with Echinococcus spp.
4.1. MiR-71 as an Innate Immune Regulator in Echinococcosis
4.2. miR-19b as an Effective Treatment Biomarker
4.3. miR-222-3p Modulates Macrophage Immunity
5. Echinococcus miRNA-Related Databases
6. Techniques and Methods Used in miRNA Studies in Echinococcus and Echinococcosis
6.1. MiRNA Identification
6.2. Verification of the Functions and Exploration of the Mechanisms
7. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Species | Tissue | Source | Genotype | Clean Reads | Identified miRNAs | Technology | Country | Ref. |
---|---|---|---|---|---|---|---|---|
E. granulosus | Protoscoleces | Porcine liver hydatid cysts and bovine lung hydatid cysts | G1 | 182 | 34 conserved and four new candidate miRNAs | Sanger | Argentina and Uruguay | [45] |
Protoscoleces | Pig | G7 | miR-125, miR-2, miR-71, miR-9, miR-10, let-7 and miR-277 | |||||
Protoscoleces | Sheep | G1 | miR-125, miR-2, miR-71, miR-9, miR-10, let-7 and miR-277 | |||||
Germinal layer of secondary cysts | Murine | G1 | miR-2, miR-71, miR-9, miR-10, let-7 and miR-277 | |||||
Pre-microcysts | Porcine liver and bovine lung | G7 | miR-125, miR-2 | |||||
Microcysts | Porcine liver and bovine lung | G7 | miR-71 | |||||
Protoscoleces | Sheep liver | __ | 21,708,040 | 109 known and 260 novel miRNAs | Illumina HiSeqTM 250 | China | [47] | |
Adult | Sheep liver hydatid cysts | __ | 10,069,724 | 46 known miRNAs, 92 novel mature miRNAs | Illumina Genome Analyzer II | China | [44] | |
Protoscoleces | Sheep liver | 11,775,532 | 45 known miRNAs, 91 novel mature miRNAs | |||||
Cyst membrane | Dog | 8,025,262 | 45 known miRNAs, 103 novel mature miRNAs | |||||
Protoscoleces | Naturally infected sheep liver | G1 | 1,642,112/1,956,161 (two biological replicates) | 36 miRNAs | Illumina Genome Analyzer II | China | [12] | |
E. canadensis | Protoscoleces | Naturally infected swine liver | G7 | 4,065,356/1,882,945 (two biological replicates) | 35 miRNAs | Illumina Genome Analyzer II | China | [12] |
Cyst walls | 2,487,372/2,117,367 (two biological replicates) | 35 miRNAs | ||||||
Cyst walls | Swine liver | 16,431,381/16,364,826 (two biological replicates) | 42 miRNAs | |||||
E. multilocularis | Metacestodes | Female CF1 mice (6–8 weeks old) | __ | 24,703,158/20,396,074 (two biological replicates) | 37 miRNAs | High-throughput small RNA sequencing | Argentina | [1] |
Metacestodes | Naturally infected crab-eating macaque (Macaca fascicularis) liver | __ | The complete E. multilocularis genome (https://www.genedb.org/#/species/Emultilocularis) | 24 miRNAs | Self-organizing map analysis | Northern Germany | [46] |
MiRNA | Description of Target Genes | Biological Function | |
---|---|---|---|
MiR-71 | Nemo-like kinase | Involved in protoscolex development and regulates host macrophage functions in Echinococcus | [52,54] |
Let-7 | Unknown | May be associated with the capability of E. granulosus for bi-directional development, can be significantly affected in the microcyst stage of E. granulosus and can exhibit different changes in expression in response to albendazole sulfoxide | [44,49] |
MiR-61 | Unknown | Significantly affected in the microcyst stage of E. granulosus and exhibits different changes in expression in response to albendazole sulfoxide | [49] |
MiR-10 | MAPKs; ECANG7_04447; ECANG7_01705; ECANG7_09658 | May be involved in regulating the MAPK and Wnt signalling pathways in Echinococcus | [23] |
MiR-124 | ECANG7_04102; ECANG7_10164; ECANG7_00514; ECANG7_02390; ECANG7_01054 | May regulate development, host-parasite interactions, and stem cell pluripotency; related to the MAPK and TGF-beta signalling pathways in Echinococcus | [23] |
MiR-184 | ECANG7_02390; ECANG7_09002 (casein kinase II); ECANG7_05735 (phosphatidylinositol phospholipase C gene); ECANG7_00867 (calcium/calmodulin-dependent protein kinase gene) | May act in a regulatory loop in miRNA biogenesis in Echinococcus | [23] |
MiR-277 | ECANG7_01278; ECANG7_02522 | May be involved in the regulation of Wnt signalling pathways regulating the pluripotency of stem cells in Echinococcus | [23] |
MiR-281 | ECANG7_04919 and ECANG7_00818 (glypicas); Nos-1 | Potentially involved in the developmental morphogenesis of Echinococcus. | [23] |
MiR-2 | ECANG7_10172; ECANG7_02390; Nos-1; ECANG7_02601; ECANG7_05326 | Potentially involved in ubiquitin-mediated proteolysis and herpes simplex infection signalling pathways, TAFH/NHR1 transcription initiation, and segmentation in Echinococcus | [23] |
MiR-307 | Ubiquitin-conjugating enzyme, E2 | May be involved in the ubiquitin-mediated proteolysis and herpes simplex infection signalling pathways in Echinococcus | [23] |
MiR-7 | ECANG7_04919 and ECANG7_00818; ECANG7_03238 | Potentially involved in the developmental morphogenesis of Echinococcus | [23] |
MiR-9 | ECANG7_02182; ECANG7_05944 | Bromodomain-containing protein is an orthologue of Caenorhabditis elegans lin-49, which is involved in nematode larval development | [23] |
MiR-96 | ECANG7_06901 | Unknown, but has a high level of expression, particularly in the Echinococcus protoscolex stage. | [23] |
MiR-125 | ECANG7_01292; ECANG7_01524 | May regulate developmental genes in Echinococcus | [23] |
MiR-36 | Unknown | May correspond with the increased regenerative capacity of E. multilocularis with respect to that of E. granulosus s.l. | [1] |
MiR-745 | G2:M phase-specific E3 ubiquitin protein ligase | Unknown | [23] |
MiR-8 | Occludin/RNA polymerase II elongation factor, ELL domain RNA polymerase II elongation factor ELL | Unknown | [23] |
MiR-87 | Zinc finger, C2H2 | Unknown | [23] |
Bantam | Ribosomal protein S2 | Unknown | [23] |
MiRNA | Expression Level | Target | Biological Function | Ref. | |||
---|---|---|---|---|---|---|---|
Sheep Gut | Mouse | ||||||
Macrophage | Liver | Serum | |||||
MiR-1247 | ↑ | - | - | ↓ | CircUBXN7 | Represses cell growth and invasion in human bladder cancer. | [71] |
MiR-145 | ↑ | - | ↓ | - | ZEB2 | Increases the apoptosis of activated hepatic stellate cells induced by TRAIL via the NF-κB signalling pathway. | [72] |
MiR-181 | ↑ | - | - | ↓ | Smad7 Hsa_circ_0007385 | Influences the differentiation of T helper cells and the activation of macrophages, controls T cell sensitivity to antigens during development | [73] |
MiR-18 | ↑ | - | - | ↑ | Unknown | As the female immunity regulator, miR-18 controls the expression of A20/Tnfaip3 and exacerbating NF-κB-driven inflammation in fibroblast-like synoviocytes of rheumatoid arthritis | [74] |
MiR-20 | ↑ | - | ↓ | - | ATG10 | Inhibits autophagy and chondrocyte proliferation by targeting ATG10 through the PI3K/AKT/mTOR signalling pathway. | [75] |
MiR-21 | ↑ | ↑ | - | ↑ | Different targets engaged in each cell type and at each time point | As the one of the master regulators of innate immunity, miR-21 plays a myriad of roles in various cellular processes via regulating genes involved in signalling pathways, such as p53, FOXO1, TGF-α, apoptosis (PDCD4),P13K/Akt/mTOR, VEGF, and NF-αB | [69] |
MiR-22 | ↑ | - | ↓ | - | CD147, YWHAZ | Inhibits hepatocellular carcinoma cell invasion, migration, and proliferation, miR-22 downregulation predicts poor survival. | [76,77] |
MiR-223 | ↑ | - | ↓ | - | Ras-related protein Rab-1 (Rab1) | May promote apoptosis and suppress cell growth through Rab1-mediated mTOR activation in hepatocellular carcinoma cells. In addition, miR-223 is a biomarker of acute and chronic liver injury | [78,79] |
MiR-27 | ↑ | - | ↓ | ↑ | GATA3, c-Rel, Smad2, Smad3, lncRNA-CIR | MiR-27 plays the important roles for safeguarding Treg-mediated immunological tolerance | [70,80] |
MiR-30 | ↑ | ↑ | ↓ | ↓ | MyD88, lncRNA n379519, lncRNA CNALPTC1 | Inhibiting cytokine expression and TLR/MyD88 activation in THP-1 cells during Mycobacterium tuberculosis H37Rv infection | [62,81] |
MiR-339 | ↑ | ↓ | - | ↑ | Skp2 | Binding to the 3′-UTR of Skp2 mRNA to inhibit the lung cancer cells proliferation | [82] |
MiR-345 | ↑ | - | ↑ | ↓ | AKT2 | Regulates the cell cycle, apoptosis, and proliferation of acute myeloid leukaemia cells by targeting AKT2 | [83] |
MiR-365 | ↑ | - | ↑ | ↑ | LncRNA MT1DP, Timp3 | The lncRNA MT1DP exacerbates cadmium-induced oxidative stress by suppressing the function of Nrf2 acting as ceRNA of miR-365. Then, miR-365 promotes diabetic retinopathy through inhibiting lncRNA Timp3 increasing oxidative stress | [63,84] |
MiR-378 | ↑ | ↑ | ↑ | - | IRG1, lncGAPLINC | Acts as a prognostic marker and inhibits epithelial-mesenchymal transition in human glioma and acts as a molecular sponge of lncGAPLINC to stimulate gastric cancer cell proliferation | [64,85] |
MiR-449 | ↑ | - | ↓ | - | LncARSR | LncARSR is competitively binding to miR-449 and thereby promoting sunitinib resistance in renal cancer | [65] |
MiR-542 | ↑ | - | - | ↓ | SMAD | After activation of SMAD2/3 phosphorylation and the promotion of mitochondrial dysfunction, upregulated miR-542-3p/5p may reduce muscle atrophy in intensive care of patients | [86] |
MiR-877 | ↑ | - | - | ↓ | Cyclin-dependent kinase 14 | Suppresses cell migration, invasion, and growth, and predicts prognosis in hepatocellular carcinoma | [66] |
MiR-99 | ↑ | ↑ | - | - | SMARCA5 | Regulates Mycoplasma gallisepticum (HS strain) infection by suppressing cell proliferation in chickens | [87] |
MiR-124 | ↑ | - | - | ↓ | LncHOTAIR, lncMALAT1, circMMP9 | LncHOTAIR sponged miRNA-124 to promote renal cell carcinoma malignancy through alpha-2,8-sialyltransferase 4. LncRNA MALAT1 acts as a ceRNA to control amadori-glycated albumin-induced MCP-1 expression in retinal microglia through a miRNA-124-dependent mechanism | [88,89,90] |
MiR-130 | ↑ | - | - | ↓ | LncMRPL39 | LncMRPL39 inhibits gastric cancer progression and proliferation by directly binding to miR-130 | [67] |
MiR-16 | ↑ | ↓ | LncDleu2 | LncDleu2 influences the invasion, migration, and proliferation of laryngeal cancer cells via miR-16 | [68] |
Name | Website | Description | Reference |
---|---|---|---|
Wellcome Sanger institute | https://www.sanger.ac.uk/resources/downloads/helminths/echinococcus-multilocularis.html | Includes E. multilocularis and E. granulosus genomes | [14] |
Sequence Read Archive | https://www.ncbi.nlm.nih.gov/sra/?term=Echinococcus%20miRNA | Includes Echinococcus miRNA raw sequencing data obtained by second-generation sequencing | [12,107,108] |
miRBase | http://www.mirbase.org | A database of Echinococcus miRNA sequences and annotations | [101] |
Rfam | http://rfam.xfam.org/search?q=Echinococcus | Includes known Echinococcus rRNAs, tRNAs, snRNAs and mRNAs | [102] |
miRDeep2 | https://www.osc.edu/book/export/html/4389 | miRNA prediction | [109] |
miRanda | http://www.microrna.org/microrna/home.do | Used to predict the target genes of all mature miRNAs | [103] |
RNA22 | https://cm.jefferson.edu/rna22/ | Used for target predictions for multiple species | [104] |
RNAhybrid | https://bibiserv.cebitec.uni-bielefeld.de/rnahybrid/ | Used to find the minimum free energy for hybridization of a long and a short RNA for predicting miRNA targets | [105] |
TarBase v6.0 | http://diana.imis.athena-innovation.gr/DianaTools/index.php?r=tarbase/index | Includes experimentally verified interactions between miRNAs and target genes | [106] |
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He, Z.; Yan, T.; Yuan, Y.; Yang, D.; Yang, G. miRNAs and lncRNAs in Echinococcus and Echinococcosis. Int. J. Mol. Sci. 2020, 21, 730. https://doi.org/10.3390/ijms21030730
He Z, Yan T, Yuan Y, Yang D, Yang G. miRNAs and lncRNAs in Echinococcus and Echinococcosis. International Journal of Molecular Sciences. 2020; 21(3):730. https://doi.org/10.3390/ijms21030730
Chicago/Turabian StyleHe, Zhi, Taiming Yan, Ya Yuan, Deying Yang, and Guangyou Yang. 2020. "miRNAs and lncRNAs in Echinococcus and Echinococcosis" International Journal of Molecular Sciences 21, no. 3: 730. https://doi.org/10.3390/ijms21030730