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Current Molecular Medicine

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ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

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Systematic Review Article

MicroRNAs in Helminth Parasites: A Systematic Review

Author(s): Zahra Alizadeh, Mahmoud Mahami-Oskouei*, Adel Spotin, Ehsan Ahmadpour, Pengfei Cai, Siamak Sandoghchian Shotorbani, Fariba Pashazadeh, Fereshteh Ansari and Hamed Mohammadi

Volume 22, Issue 9, 2022

Published on: 11 January, 2022

Page: [779 - 808] Pages: 30

DOI: 10.2174/1566524021666211108114009

Price: $65

Abstract

Background: MicroRNAs (miRNAs) are about 22-nucleotide, small, noncoding RNAs that control gene expression post-transcriptionally. Helminth parasites usually express a unique repertoire of genes, including miRNAs, across different developmental stages with subtle regulatory mechanisms.

Objective: There is a necessity to investigate the involvement of miRNAs in the development of parasites, host-parasite interaction, immune evasion and their abilities to govern infection in hosts. MiRNAs present in helminth parasites have been summarized in the current systematic review (SR).

Methods: Electronic databases, including PubMed, Scopus, ProQuest, Embase, and Google Scholar search engine, were searched to identify helminth miRNA studies published from February 1993 till December 2019. Only the published articles in English were included in the study.

Results: A total of 1769 articles were preliminarily recorded. Following the strict inclusion and exclusion criteria, 105 studies were included in this SR. Most of these studies focused on the identification of miRNAs in helminth parasites and/or probing of differentially expressed host miRNA profiles in specific relevant tissues, while 12 studies aimed to detect parasite-derived miRNAs in host circulating system and 15 studies characterized extracellular vesicles (EV)-derived miRNAs secreted by parasites.

Conclusion: In the current SR, information regarding all miRNAs expressed in helminth parasites has been comprehensively provided and the utility of helminth parasitesderived miRNAs in diagnosis and control of parasitic infections has been discussed. Furthermore, functional studies on helminth-derived miRNAs have also been presented.

Keywords: MicroRNA, helminth, parasites, trematode, cestode, nematode.

« Previous Next »
[1]
Nakagawa J, Ehrenberg JP, Nealon J, et al. Towards effective prevention and control of helminth neglected tropical diseases in the Western Pacific Region through multi-disease and multi-sectoral interventions Acta Trop 2015; 141(Pt B): 407-18.
[http://dx.doi.org/10.1016/j.actatropica.2013.05.010] [PMID: 23792012]
[2]
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest 2008; 118(4): 1311-21.
[http://dx.doi.org/10.1172/JCI34261] [PMID: 18382743]
[3]
Molyneux DH, Savioli L, Engels D. Neglected tropical diseases: progress towards addressing the chronic pandemic. Lancet 2017; 389(10066): 312-25.
[http://dx.doi.org/10.1016/S0140-6736(16)30171-4] [PMID: 27639954]
[4]
Britton C, Winter AD, Gillan V, Devaney E. microRNAs of parasitic helminths - Identification, characterization and potential as drug targets. Int J Parasitol Drugs Drug Resist 2014; 4(2): 85-94.
[http://dx.doi.org/10.1016/j.ijpddr.2014.03.001] [PMID: 25057458]
[5]
Zheng Y, Cai X, Bradley JE. microRNAs in parasites and parasite infection. RNA Biol 2013; 10(3): 371-9.
[http://dx.doi.org/10.4161/rna.23716] [PMID: 23392243]
[6]
Cai P, Gobert GN, McManus DP. MicroRNAs in parasitic helminthiases: current status and future perspectives. Trends Parasitol 2016; 32(1): 71-86.
[http://dx.doi.org/10.1016/j.pt.2015.09.003] [PMID: 26489492]
[7]
Grimson A, Srivastava M, Fahey B, et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 2008; 455(7217): 1193-7.
[http://dx.doi.org/10.1038/nature07415] [PMID: 18830242]
[8]
Ghildiyal M, Seitz H, Horwich MD, et al. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 2008; 320(5879): 1077-81.
[http://dx.doi.org/10.1126/science.1157396] [PMID: 18403677]
[9]
Aalaei-Andabili SH, Rezaei N. MicroRNAs (MiRs) precisely regulate immune system development and function in immunosenescence process. Int Rev Immunol 2016; 35(1): 57-66.
[http://dx.doi.org/10.3109/08830185.2015.1077828] [PMID: 26327579]
[10]
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[11]
Carrington JC, Ambros V. Role of microRNAs in plant and animal development. Science 2003; 301(5631): 336-8.
[http://dx.doi.org/10.1126/science.1085242] [PMID: 12869753]
[12]
Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 2007; 8(1): 23-36.
[http://dx.doi.org/10.1038/nrm2085] [PMID: 17183358]
[13]
Britton C, Winter AD, Marks ND, et al. Application of small RNA technology for improved control of parasitic helminths. Vet Parasitol 2015; 212(1-2): 47-53.
[http://dx.doi.org/10.1016/j.vetpar.2015.06.003] [PMID: 26095949]
[14]
Ghildiyal M, Zamore PD. Small silencing RNAs: An expanding universe. Nat Rev Genet 2009; 10(2): 94-108.
[http://dx.doi.org/10.1038/nrg2504] [PMID: 19148191]
[15]
Xue X, Sun J, Zhang Q, Wang Z, Huang Y, Pan W. Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS One 2008; 3(12): e4034.
[http://dx.doi.org/10.1371/journal.pone.0004034] [PMID: 19107204]
[16]
Braconi C, Valeri N, Gasparini P, et al. Hepatitis C virus proteins modulate microRNA expression and chemosensitivity in malignant hepatocytes. Clin Cancer Res 2010; 16(3): 957-66.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2123] [PMID: 20103677]
[17]
McVeigh P. Post-genomic progress in helminth parasitology. Parasitology 2020; 147(8): 835-40.
[http://dx.doi.org/10.1017/S0031182020000591] [PMID: 32252832]
[18]
Rangel G, Teerawattanapong N, Chamnanchanunt S, Umemura T, Pinyachat A, Wanram S. Candidate microRNAs in Malaria Infection Biomarkers: A Systematic Review. Curr Mol Med 2019; 20(1): 36-43.
[http://dx.doi.org/10.2174/1566524019666190820124827] [PMID: 31429687]
[19]
Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99(24): 15524-9.
[http://dx.doi.org/10.1073/pnas.242606799] [PMID: 12434020]
[20]
Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene 2007; 26(19): 2799-803.
[http://dx.doi.org/10.1038/sj.onc.1210083] [PMID: 17072344]
[21]
Jin X, Guo X, Zhu D, Ayaz M, Zheng Y. miRNA profiling in the mice in response to Echinococcus multilocularis infection. Acta Trop 2017; 166: 39-44.
[http://dx.doi.org/10.1016/j.actatropica.2016.10.024] [PMID: 27810427]
[22]
Zeiner GM, Norman KL, Thomson JM, Hammond SM, Boothroyd JC. Toxoplasma gondii infection specifically increases the levels of key host microRNAs. PLoS One 2010; 5(1): e8742.
[http://dx.doi.org/10.1371/journal.pone.0008742] [PMID: 20090903]
[23]
Jiang S, Li X, Wang X, Ban Q, Hui W, Jia B. MicroRNA profiling of the intestinal tissue of Kazakh sheep after experimental Echinococcus granulosus infection, using a high-throughput approach. Parasite 2016; 23: 23.
[http://dx.doi.org/10.1051/parasite/2016023] [PMID: 27235195]
[24]
Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294(5543): 862-4.
[http://dx.doi.org/10.1126/science.1065329] [PMID: 11679672]
[25]
Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75(5): 843-54.
[http://dx.doi.org/10.1016/0092-8674(93)90529-Y] [PMID: 8252621]
[26]
Meningher T, Lerman G, Regev-Rudzki N, et al. Schistosomal MicroRNAs isolated from extracellular vesicles in sera of infected patients: a new tool for diagnosis and follow-up of human schistosomiasis. J Infect Dis 2017; 215(3): 378-86.
[PMID: 28362903]
[27]
Tritten L, Burkman E, Moorhead A, et al. Detection of circulating parasite-derived microRNAs in filarial infections. PLoS Negl Trop Dis 2014; 8(7): e2971.
[http://dx.doi.org/10.1371/journal.pntd.0002971] [PMID: 25033073]
[28]
Cai P, Gobert GN, You H, Duke M, McManus DP. Circulating miRNAs: potential novel biomarkers for hepatopathology progression and diagnosis of schistosomiasis japonica in two murine models. PLoS Negl Trop Dis 2015; 9(7): e0003965.
[http://dx.doi.org/10.1371/journal.pntd.0003965] [PMID: 26230095]
[29]
Cheng G, Luo R, Hu C, Cao J, Jin Y. Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 2013; 140(14): 1751-61.
[http://dx.doi.org/10.1017/S0031182013000917] [PMID: 23942009]
[30]
Guo X, Zheng Y. Expression profiling of circulating miRNAs in mouse serum in response to Echinococcus multilocularis infection. Parasitology 2017; 144(8): 1079-87.
[http://dx.doi.org/10.1017/S0031182017000300] [PMID: 28270244]
[31]
Tritten L, O’Neill M, Nutting C, et al. Loa loa and Onchocerca ochengi miRNAs detected in host circulation. Mol Biochem Parasitol 2014; 198(1): 14-7.
[http://dx.doi.org/10.1016/j.molbiopara.2014.11.001] [PMID: 25461483]
[32]
Buck AH, Coakley G, Simbari F, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun 2014; 5: 5488.
[http://dx.doi.org/10.1038/ncomms6488] [PMID: 25421927]
[33]
Hu G, Zhou R, Liu J, Gong AY, Chen XM. MicroRNA-98 and let-7 regulate expression of suppressor of cytokine signaling 4 in biliary epithelial cells in response to Cryptosporidium parvum infection. J Infect Dis 2010; 202(1): 125-35.
[http://dx.doi.org/10.1086/653212] [PMID: 20486857]
[34]
Mahami Oskouei M, Ghabouli Mehrabani N, Miahipour A, Fallah E. Molecular characterization and sequence analysis of Echinococcus granulosus from sheep isolates in East Azerbaijan province, northwest of Iran. J Parasit Dis 2016; 40(3): 785-90.
[http://dx.doi.org/10.1007/s12639-014-0579-3] [PMID: 27605785]
[35]
Ghabouli Mehrabani N, Kousha A, Khalili M, et al. Hydatid cyst surgeries in patients referred to hospitals in East Azerbaijan province during 2009-2011. Iran J Parasitol 2014; 9(2): 233-8.
[PMID: 25848390]
[36]
Agudelo Higuita NI, Brunetti E, McCloskey C. Cystic Echinococcosis. J Clin Microbiol 2016; 54(3): 518-23.
[http://dx.doi.org/10.1128/JCM.02420-15] [PMID: 26677245]
[37]
Zhang C, Wang L, Ali T, et al. Hydatid cyst fluid promotes peri-cystic fibrosis in cystic echinococcosis by suppressing miR-19 expression. Parasit Vectors 2016; 9(1): 278.
[http://dx.doi.org/10.1186/s13071-016-1562-x] [PMID: 27177776]
[38]
Bernal D, Trelis M, Montaner S, et al. Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics 2014; 105: 232-41.
[http://dx.doi.org/10.1016/j.jprot.2014.02.012] [PMID: 24561797]
[39]
Fromm B, Trelis M, Hackenberg M, Cantalapiedra F, Bernal D, Marcilla A. The revised microRNA complement of Fasciola hepatica reveals a plethora of overlooked microRNAs and evidence for enrichment of immuno-regulatory microRNAs in extracellular vesicles. Int J Parasitol 2015; 45(11): 697-702.
[http://dx.doi.org/10.1016/j.ijpara.2015.06.002] [PMID: 26183562]
[40]
Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. J Extracell Vesicles 2015; 4: 28665.
[http://dx.doi.org/10.3402/jev.v4.28665] [PMID: 26443722]
[41]
Samoil V, Dagenais M, Ganapathy V, et al. Vesicle-based secretion in schistosomes: Analysis of protein and microRNA (miRNA) content of exosome-like vesicles derived from Schistosoma mansoni. Sci Rep 2018; 8(1): 3286.
[http://dx.doi.org/10.1038/s41598-018-21587-4] [PMID: 29459722]
[42]
Zhu L, Liu J, Dao J, et al. Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions. Sci Rep 2016; 6: 25885.
[http://dx.doi.org/10.1038/srep25885] [PMID: 27172881]
[43]
Zhu S, Wang S, Lin Y, et al. Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum. Parasit Vectors 2016; 9(1): 574.
[http://dx.doi.org/10.1186/s13071-016-1845-2] [PMID: 27825390]
[44]
Ancarola ME, Marcilla A, Herz M, et al. Cestode parasites release extracellular vesicles with microRNAs and immunodiagnostic protein cargo. Int J Parasitol Parasites 2017; 47(10-11): 675-86.
[http://dx.doi.org/10.1016/j.ijpara.2017.05.003] [PMID: 28668323]
[45]
Chow FWN, Koutsovoulos G, Ovando-Vázquez C, Laetsch DR, Bermúdez-Barrientos J. An extracellular Argonaute protein mediates export of repeat-associated small RNAs into vesicles in parasitic nematodes bioRxiv 2018.
[46]
Gu HY, Marks ND, Winter AD, et al. Conservation of a microRNA cluster in parasitic nematodes and profiling of miRNAs in excretory-secretory products and microvesicles of Haemonchus contortus. PLoS Negl Trop Dis 2017; 11(11): e0006056.
[http://dx.doi.org/10.1371/journal.pntd.0006056] [PMID: 29145392]
[47]
Eichenberger RM, Ryan S, Jones L, et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front Immunol 2018; 9: 850.
[http://dx.doi.org/10.3389/fimmu.2018.00850] [PMID: 29760697]
[48]
Eichenberger RM, Talukder MH, Field MA, et al. Characterization of Trichuris muris secreted proteins and extracellular vesicles provides new insights into host-parasite communication. J Extracell Vesicles 2018; 7(1): 1428004.
[http://dx.doi.org/10.1080/20013078.2018.1428004] [PMID: 29410780]
[49]
Jex AR, Nejsum P, Schwarz EM, et al. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat Genet 2014; 46(7): 701-6.
[http://dx.doi.org/10.1038/ng.3012] [PMID: 24929829]
[50]
Marcilla A, Trelis M, Cortés A, et al. Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One 2012; 7(9): e45974.
[http://dx.doi.org/10.1371/journal.pone.0045974] [PMID: 23029346]
[51]
Cwiklinski K, de la Torre-Escudero E, Trelis M, et al. The extracellular vesicles of the helminth pathogen, Fasciola hepatica: biogenesis pathways and cargo molecules involved in parasite pathogenesis. Mol Cell Proteomics 2015; 14(12): 3258-73.
[http://dx.doi.org/10.1074/mcp.M115.053934] [PMID: 26486420]
[52]
Kozomara A, Griffiths-Jones S. miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014; 42(Database issue): D68-73.
[http://dx.doi.org/10.1093/nar/gkt1181] [PMID: 24275495]
[53]
Manzano-Román R, Siles-Lucas M. MicroRNAs in parasitic diseases: potential for diagnosis and targeting. Mol Biochem Parasitol 2012; 186(2): 81-6.
[http://dx.doi.org/10.1016/j.molbiopara.2012.10.001] [PMID: 23069113]
[54]
Hsieh YW, Chang C, Chuang CF. The microRNA mir-71 inhibits calcium signaling by targeting the TIR-1/Sarm1 adaptor protein to control stochastic L/R neuronal asymmetry in C. elegans. PLoS Genet 2012; 8(8): e1002864.
[http://dx.doi.org/10.1371/journal.pgen.1002864] [PMID: 22876200]
[55]
Zheng Y, Guo X, He W, et al. Effects of Echinococcus multilocularis miR-71 mimics on murine macrophage RAW264.7 cells. Int Immunopharmacol 2016; 34: 259-62.
[http://dx.doi.org/10.1016/j.intimp.2016.03.015] [PMID: 26995025]
[56]
Grosshans H, Johnson T, Reinert KL, Gerstein M, Slack FJ. The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev Cell 2005; 8(3): 321-30.
[http://dx.doi.org/10.1016/j.devcel.2004.12.019] [PMID: 15737928]
[57]
Bai Y, Zhang Z, Jin L, et al. Genome-wide sequencing of small RNAs reveals a tissue-specific loss of conserved microRNA families in Echinococcus granulosus. BMC Genomics 2014; 15: 736.
[http://dx.doi.org/10.1186/1471-2164-15-736] [PMID: 25168356]
[58]
Caygill EE, Johnston LA. Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 2008; 18(13): 943-50.
[http://dx.doi.org/10.1016/j.cub.2008.06.020] [PMID: 18571409]
[59]
Huang J, Hao P, Chen H, et al. Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PLoS One 2009; 4(12): e8206.
[http://dx.doi.org/10.1371/journal.pone.0008206] [PMID: 19997615]
[60]
Copeland CS, Marz M, Rose D, et al. Homology-based annotation of non-coding RNAs in the genomes of Schistosoma mansoni and Schistosoma japonicum. BMC Genomics 2009; 10: 464.
[http://dx.doi.org/10.1186/1471-2164-10-464] [PMID: 19814823]
[61]
Hao L, Cai P, Jiang N, Wang H, Chen Q. Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genomics 2010; 11: 55.
[http://dx.doi.org/10.1186/1471-2164-11-55] [PMID: 20092619]
[62]
Wang Z, Xue X, Sun J, et al. An “in-depth” description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS Negl Trop Dis 2010; 4(2): e596.
[http://dx.doi.org/10.1371/journal.pntd.0000596] [PMID: 20161724]
[63]
Luo R, Xue X, Wang Z, Sun J, Zou Y, Pan W. Analysis and characterization of the genes encoding the Dicer and Argonaute proteins of Schistosoma japonicum. Parasit Vectors 2010; 3: 90.
[http://dx.doi.org/10.1186/1756-3305-3-90] [PMID: 20849617]
[64]
Chen J, Yang Y, Guo S, et al. Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum. Parasitol Res 2010; 107(4): 889-99.
[http://dx.doi.org/10.1007/s00436-010-1946-3] [PMID: 20582438]
[65]
Cai P, Hou N, Piao X, et al. Profiles of small non-coding RNAs in Schistosoma japonicum during development. PLoS Negl Trop Dis 2011; 5(8): e1256.
[http://dx.doi.org/10.1371/journal.pntd.0001256] [PMID: 21829742]
[66]
Cai P, Piao X, Hou N, Liu S, Wang H, Chen Q. Identification and characterization of argonaute protein, Ago2 and its associated small RNAs in Schistosoma japonicum. PLoS Negl Trop Dis 2012; 6(7): e1745.
[http://dx.doi.org/10.1371/journal.pntd.0001745] [PMID: 22860145]
[67]
Cai P, Piao X, Hao L, et al. A deep analysis of the small non-coding RNA population in Schistosoma japonicum eggs. PLoS One 2013; 8(5): e64003.
[http://dx.doi.org/10.1371/journal.pone.0064003] [PMID: 23691136]
[68]
Han H, Peng J, Hong Y, et al. Comparative characterization of microRNAs in Schistosoma japonicum schistosomula from Wistar rats and BALB/c mice. Parasitol Res 2015; 114(7): 2639-47.
[http://dx.doi.org/10.1007/s00436-015-4468-1] [PMID: 25895062]
[69]
Han H, Peng J, Hong Y, et al. Comparative analysis of microRNA in schistosomula isolated from non-permissive host and susceptible host. Mol Biochem Parasitol 2015; 204(2): 81-8.
[http://dx.doi.org/10.1016/j.molbiopara.2015.11.005] [PMID: 26844643]
[70]
Zhu L, Zhao J, Wang J, et al. MicroRNAs are involved in the regulation of ovary development in the pathogenic blood fluke Schistosoma japonicum. PLoS Pathog 2016; 12(2): e1005423.
[http://dx.doi.org/10.1371/journal.ppat.1005423] [PMID: 26871705]
[71]
Kong QM, Zhu X, Tong QB, et al. Genome-wide miRNAs expression profiles of Schistosoma japonicum schistosomula in response to artesunate. Pharmacogenomics 2016; 17(18): 2025-37.
[http://dx.doi.org/10.2217/pgs.16.23] [PMID: 27918238]
[72]
Mu Y, Cai P, Olveda RM, Ross AG, Olveda DU, McManus DP. Parasite-derived circulating microRNAs as biomarkers for the detection of human Schistosoma japonicum infection. Parasitology 2020; 147(8): 889-96.
[http://dx.doi.org/10.1017/S0031182019001690] [PMID: 31840631]
[73]
Liu J, Zhu L, Wang J, et al. Schistosoma japonicum extracellular vesicle miRNA cargo regulates host macrophage functions facilitating parasitism. PLoS Pathog 2019; 15(6): e1007817.
[http://dx.doi.org/10.1371/journal.ppat.1007817] [PMID: 31163079]
[74]
Gomes MS, Cabral FJ, Jannotti-Passos LK, et al. Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int 2009; 58(1): 61-8.
[http://dx.doi.org/10.1016/j.parint.2008.10.002] [PMID: 19007911]
[75]
Simões MC, Lee J, Djikeng A, et al. Identification of Schistosoma mansoni microRNAs. BMC Genomics 2011; 12: 47.
[http://dx.doi.org/10.1186/1471-2164-12-47] [PMID: 21247453]
[76]
de Souza Gomes M, Muniyappa MK, Carvalho SG, Guerra-Sá R, Spillane C. Genome-wide identification of novel microRNAs and their target genes in the human parasite Schistosoma mansoni. Genomics 2011; 98(2): 96-111.
[http://dx.doi.org/10.1016/j.ygeno.2011.05.007] [PMID: 21640815]
[77]
Marco A, Kozomara A, Hui JH, et al. Sex-biased expression of microRNAs in Schistosoma mansoni. PLoS Negl Trop Dis 2013; 7(9): e2402.
[http://dx.doi.org/10.1371/journal.pntd.0002402] [PMID: 24069470]
[78]
Picard MA, Boissier J, Roquis D, et al. Sex-biased transcriptome of Schistosoma mansoni: host-parasite interaction, genetic determinants and epigenetic regulators are associated with sexual differentiation. PLoS Negl Trop Dis 2016; 10(9): e0004930.
[http://dx.doi.org/10.1371/journal.pntd.0004930] [PMID: 27677173]
[79]
Hoy AM, Lundie RJ, Ivens A, et al. Parasite-derived microRNAs in host serum as novel biomarkers of helminth infection. PLoS Negl Trop Dis 2014; 8(2): e2701.
[http://dx.doi.org/10.1371/journal.pntd.0002701] [PMID: 24587461]
[80]
Stroehlein AJ, Young ND, Korhonen PK, et al. The small RNA complement of adult Schistosoma haematobium. PLoS Negl Trop Dis 2018; 12(5): e0006535.
[http://dx.doi.org/10.1371/journal.pntd.0006535] [PMID: 29813122]
[81]
Xu MJ, Liu Q, Nisbet AJ, et al. Identification and characterization of microRNAs in Clonorchis sinensis of human health significance. BMC Genomics 2010; 11: 521.
[http://dx.doi.org/10.1186/1471-2164-11-521] [PMID: 20920166]
[82]
Ovchinnikov VY, Afonnikov DA, Vasiliev GV, et al. Identification of microRNA genes in three opisthorchiids. PLoS Negl Trop Dis 2015; 9(4): e0003680.
[http://dx.doi.org/10.1371/journal.pntd.0003680] [PMID: 25898350]
[83]
Xu MJ, Ai L, Fu JH, et al. Comparative characterization of microRNAs from the liver flukes Fasciola gigantica and F. hepatica. PLoS One 2012; 7(12): e53387.
[http://dx.doi.org/10.1371/journal.pone.0053387] [PMID: 23300925]
[84]
Fontenla S, Dell’Oca N, Smircich P, Tort JF, Siles-Lucas M. The miRnome of Fasciola hepatica juveniles endorses the existence of a reduced set of highly divergent micro RNAs in parasitic flatworms. Int J Parasitol Parasites 2015; 45(14): 901-13.
[http://dx.doi.org/10.1016/j.ijpara.2015.06.007] [PMID: 26432296]
[85]
Chen MX, Hu W, Li J, He JJ, Ai L, Chen JX. Identification and characterization of microRNAs in the zoonotic fluke Fasciolopsis buski. Parasitol Res 2016; 115(6): 2433-8.
[http://dx.doi.org/10.1007/s00436-016-4995-4] [PMID: 27021181]
[86]
Wang CR, Xu MJ, Fu JH, et al. Characterization of microRNAs from Orientobilharzia turkestanicum, a neglected blood fluke of human and animal health significance. PLoS One 2012; 7(10): e47001.
[http://dx.doi.org/10.1371/journal.pone.0047001] [PMID: 23071694]
[87]
Ai L, Chen M, Chen S, Zhang Y, Li H. Characterization of microRNAs in Paragonimus westermani by Solexa deep sequencing and bioinformatics analysis. J Anim Vet Adv 2012; 11: 3469-73.
[http://dx.doi.org/10.3923/javaa.2012.3469.3473]
[88]
Xu MJ, Wang CR, Huang SY, et al. Identification and characterization of microRNAs in the pancreatic fluke Eurytrema pancreaticum. Parasit Vectors 2013; 6: 25.
[http://dx.doi.org/10.1186/1756-3305-6-25] [PMID: 23351883]
[89]
Fromm B, Worren MM, Hahn C, Hovig E, Bachmann L. Substantial loss of conserved and gain of novel MicroRNA families in flatworms. Mol Biol Evol 2013; 30(12): 2619-28.
[http://dx.doi.org/10.1093/molbev/mst155] [PMID: 24025793]
[90]
Fromm B, Burow S, Hahn C, Bachmann L. MicroRNA loci support conspecificity of Gyrodactylus salaris and Gyrodactylus thymalli (Platyhelminthes: Monogenea). Int J Parasitol Parasites 2014; 44(11): 787-93.
[http://dx.doi.org/10.1016/j.ijpara.2014.05.010] [PMID: 24998346]
[91]
Young ND, Nagarajan N, Lin SJ, et al. The Opisthorchis viverrini genome provides insights into life in the bile duct. Nat Commun 2014; 5: 4378.
[http://dx.doi.org/10.1038/ncomms5378] [PMID: 25007141]
[92]
Cucher M, Prada L, Mourglia-Ettlin G, et al. Identification of Echinococcus granulosus microRNAs and their expression in different life cycle stages and parasite genotypes. Int J Parasitol Parasites 2011; 41(3-4): 439-48.
[http://dx.doi.org/10.1016/j.ijpara.2010.11.010] [PMID: 21219906]
[93]
Alizadeh Z, Mahami-Oskouei M, Spotin A, et al. Parasite-derived microRNAs in plasma as novel promising biomarkers for the early detection of hydatid cyst infection and post-surgery follow-up. Acta Trop 2020; 202: 105255.
[http://dx.doi.org/10.1016/j.actatropica.2019.105255] [PMID: 31682814]
[94]
Macchiaroli N, Cucher M, Zarowiecki M, Maldonado L, Kamenetzky L, Rosenzvit MC. microRNA profiling in the zoonotic parasite Echinococcus canadensis using a high-throughput approach. Parasit Vectors 2015; 8: 83.
[http://dx.doi.org/10.1186/s13071-015-0686-8] [PMID: 25656283]
[95]
Cucher M, Macchiaroli N, Kamenetzky L, Maldonado L, Brehm K, Rosenzvit MC. High-throughput characterization of Echinococcus spp. metacestode miRNomes. Int J Parasitol Parasites 2015; 45(4): 253-67.
[http://dx.doi.org/10.1016/j.ijpara.2014.12.003] [PMID: 25659494]
[96]
Kamenetzky L, Stegmayer G, Maldonado L, Macchiaroli N, Yones C, Milone DH. MicroRNA discovery in the human parasite Echinococcus multilocularis from genome-wide data. Genomics 2016; 107(6): 274-80.
[http://dx.doi.org/10.1016/j.ygeno.2016.04.002] [PMID: 27107656]
[97]
Ai L, Xu MJ, Chen MX, et al. Characterization of microRNAs in Taenia saginata of zoonotic significance by Solexa deep sequencing and bioinformatics analysis. Parasitol Res 2012; 110(6): 2373-8.
[http://dx.doi.org/10.1007/s00436-011-2773-x] [PMID: 22203522]
[98]
Ai L, Chen MX, Zhang YN, Chen SH, Zhou XN, Chen JX. Comparative analysis of the miRNA profiles from Taenia solium and Taenia asiatica adult. Afr J Microbiol Res 2014; 8: 895-902.
[http://dx.doi.org/10.5897/AJMR12.1218]
[99]
Wu X, Fu Y, Yang D, et al. Identification of neglected cestode Taenia multiceps microRNAs by illumina sequencing and bioinformatic analysis. BMC Vet Res 2013; 9: 162.
[http://dx.doi.org/10.1186/1746-6148-9-162] [PMID: 23941076]
[100]
Pérez MG, Macchiaroli N, Lichtenstein G, et al. microRNA analysis of Taenia crassiceps cysticerci under praziquantel treatment and genome-wide identification of Taenia solium miRNAs. Int J Parasitol Parasites 2017; 47(10-11): 643-53.
[http://dx.doi.org/10.1016/j.ijpara.2017.04.002] [PMID: 28526608]
[101]
Zheng Y. High-throughput identification of miRNAs of Taenia ovis, a cestode threatening sheep industry. Infect Genet Evol 2017; 51: 98-100.
[http://dx.doi.org/10.1016/j.meegid.2017.03.023] [PMID: 28342885]
[102]
Jin X, Lu L, Su H, et al. Comparative analysis of known miRNAs across platyhelminths. FEBS J 2013; 280(16): 3944-51.
[http://dx.doi.org/10.1111/febs.12395] [PMID: 23777576]
[103]
Basika T, Macchiaroli N, Cucher M, et al. Identification and profiling of microRNAs in two developmental stages of the model cestode parasite Mesocestoides corti. Mol Biochem Parasitol 2016; 210(1-2): 37-49.
[http://dx.doi.org/10.1016/j.molbiopara.2016.08.004] [PMID: 27544036]
[104]
Shao C-C, Xu M-J, Alasaad S, et al. Comparative analysis of microRNA profiles between adult Ascaris lumbricoides and Ascaris suum. BMC Vet Res 2014; 10: 99.
[http://dx.doi.org/10.1186/1746-6148-10-99] [PMID: 24766827]
[105]
Wang J, Czech B, Crunk A, et al. Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res 2011; 21(9): 1462-77.
[http://dx.doi.org/10.1101/gr.121426.111] [PMID: 21685128]
[106]
Xu MJ, Fu JH, Nisbet AJ, et al. Comparative profiling of microRNAs in male and female adults of Ascaris suum. Parasitol Res 2013; 112(3): 1189-95.
[http://dx.doi.org/10.1007/s00436-012-3250-x] [PMID: 23306386]
[107]
Zhao GH, Xu MJ, Zhu XQ. Identification and characterization of microRNAs in Baylisascaris schroederi of the giant panda. Parasit Vectors 2013; 6: 216.
[http://dx.doi.org/10.1186/1756-3305-6-216] [PMID: 23883822]
[108]
Ma G, Luo Y, Zhu H, et al. MicroRNAs of Toxocara canis and their predicted functional roles. Parasit Vectors 2016; 9: 229.
[http://dx.doi.org/10.1186/s13071-016-1508-3] [PMID: 27108220]
[109]
Poole CB, Davis PJ, Jin J, McReynolds LA. Cloning and bioinformatic identification of small RNAs in the filarial nematode, Brugia malayi. Mol Biochem Parasitol 2010; 169(2): 87-94.
[http://dx.doi.org/10.1016/j.molbiopara.2009.10.004] [PMID: 19874857]
[110]
Poole CB, Gu W, Kumar S, et al. Diversity and expression of microRNAs in the filarial parasite, Brugia malayi. PLoS One 2014; 9(5): e96498.
[http://dx.doi.org/10.1371/journal.pone.0096498] [PMID: 24824352]
[111]
Sarkies P, Selkirk ME, Jones JT, et al. Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol 2015; 13(2): e1002061.
[http://dx.doi.org/10.1371/journal.pbio.1002061] [PMID: 25668728]
[112]
Zamanian M, Fraser LM, Agbedanu PN, et al. Release of small RNA-containing exosome-like vesicles from the human filarial parasite Brugia malayi. PLoS Negl Trop Dis 2015; 9(9): e0004069.
[http://dx.doi.org/10.1371/journal.pntd.0004069] [PMID: 26401956]
[113]
Winter AD, Weir W, Hunt M, et al. Diversity in parasitic nematode genomes: the microRNAs of Brugia pahangi and Haemonchus contortus are largely novel. BMC Genomics 2012; 13: 4.
[http://dx.doi.org/10.1186/1471-2164-13-4] [PMID: 22216965]
[114]
Winter AD, Gillan V, Maitland K, et al. A novel member of the let-7 microRNA family is associated with developmental transitions in filarial nematode parasites. BMC Genomics 2015; 16: 331.
[http://dx.doi.org/10.1186/s12864-015-1536-y] [PMID: 25896062]
[115]
Quintana JF, Makepeace BL, Babayan SA, et al. Extracellular Onchocerca-derived small RNAs in host nodules and blood. Parasit Vectors 2015; 8: 58.
[http://dx.doi.org/10.1186/s13071-015-0656-1] [PMID: 25623184]
[116]
Lagatie O, Batsa Debrah L, Debrah A, Stuyver LJ. Plasma-derived parasitic microRNAs have insufficient concentrations to be used as diagnostic biomarker for detection of Onchocerca volvulus infection or treatment monitoring using LNA-based RT-qPCR. Parasitol Res 2017; 116(3): 1013-22.
[http://dx.doi.org/10.1007/s00436-017-5382-5] [PMID: 28111713]
[117]
Huang Q-X, Cheng X-Y, Mao Z-C, et al. MicroRNA discovery and analysis of pinewood nematode Bursaphelenchus xylophilus by deep sequencing. PLoS One 2010; 5(10): e13271.
[http://dx.doi.org/10.1371/journal.pone.0013271] [PMID: 20967259]
[118]
Ding X, Ye J, Wu X, Huang L, Zhu L, Lin S. Deep sequencing analyses of pine wood nematode Bursaphelenchus xylophilus microRNAs reveal distinct miRNA expression patterns during the pathological process of pine wilt disease. Gene 2015; 555(2): 346-56.
[http://dx.doi.org/10.1016/j.gene.2014.11.030] [PMID: 25447893]
[119]
Chen MX, Ai L, Xu MJ, et al. Identification and characterization of microRNAs in Trichinella spiralis by comparison with Brugia malayi and Caenorhabditis elegans. Parasitol Res 2011; 109(3): 553-8.
[http://dx.doi.org/10.1007/s00436-011-2283-x] [PMID: 21327987]
[120]
Liu X, Song Y, Lu H, et al. Transcriptome of small regulatory RNAs in the development of the zoonotic parasite Trichinella spiralis. PLoS One 2011; 6(11): e26448.
[http://dx.doi.org/10.1371/journal.pone.0026448] [PMID: 22096484]
[121]
Padmashree D, Ramachandraswamy N. Identification and characterization of conserved miRNAs with its targets mRNA in Trichinella Spiralis. Bioinformation 2016; 12(5): 279-84.
[http://dx.doi.org/10.6026/97320630012279] [PMID: 28246461]
[122]
Chen MX, Ai L, Xu MJ, et al. Angiostrongylus cantonensis: identification and characterization of microRNAs in male and female adults. Exp Parasitol 2011; 128(2): 116-20.
[http://dx.doi.org/10.1016/j.exppara.2011.02.019] [PMID: 21356210]
[123]
Chang SH, Tang P, Lai CH, Kuo ML, Wang LC. Identification and characterisation of microRNAs in young adults of Angiostrongylus cantonensisvia a deep-sequencing approach. Mem Inst Oswaldo Cruz 2013; 108(6): 699-706.
[http://dx.doi.org/10.1590/0074-0276108062013005] [PMID: 24037191]
[124]
Li Z, Chen X, Zen X, et al. MicroRNA expression profile in the third- and fourth-stage larvae of Angiostrongylus cantonensis. Parasitol Res 2014; 113(5): 1883-96.
[http://dx.doi.org/10.1007/s00436-014-3836-6] [PMID: 24696273]
[125]
Ma G, Wang T, Korhonen PK, et al. Molecular alterations during larval development of Haemonchus contortus in vitro are under tight post-transcriptional control. Int J Parasitol Parasites 2018; 48(9-10): 763-72.
[http://dx.doi.org/10.1016/j.ijpara.2018.03.008] [PMID: 29792880]
[126]
Fu Y, Lan J, Wu X, et al. Identification of Dirofilaria immitis miRNA using illumina deep sequencing. Vet Res 2013; 44: 3.
[http://dx.doi.org/10.1186/1297-9716-44-3] [PMID: 23331513]
[127]
Tritten L, Clarke D, Timmins S, McTier T, Geary TG. Dirofilaria immitis exhibits sex- and stage-specific differences in excretory/secretory miRNA and protein profiles. Vet Parasitol 2016; 232: 1-7.
[http://dx.doi.org/10.1016/j.vetpar.2016.11.005] [PMID: 27890076]
[128]
Holz A, Streit A. Gain and loss of small RNA classes-characterization of small RNAs in the parasitic nematode family strongyloididae. Genome Biol Evol 2017; 9(10): 2826-43.
[http://dx.doi.org/10.1093/gbe/evx197] [PMID: 29036592]
[129]
Ahmed R, Chang Z, Younis AE, et al. Conserved miRNAs are candidate post-transcriptional regulators of developmental arrest in free-living and parasitic nematodes. Genome Biol Evol 2013; 5(7): 1246-60.
[http://dx.doi.org/10.1093/gbe/evt086] [PMID: 23729632]
[130]
Tritten L, Tam M, Vargas M, et al. Excretory/secretory products from the gastrointestinal nematode Trichuris muris. Exp Parasitol 2017; 178: 30-6.
[http://dx.doi.org/10.1016/j.exppara.2017.05.003] [PMID: 28533110]
[131]
Zhang Y, Wang Y, Xie F, et al. Identification and characterization of microRNAs in the plant parasitic root-knot nematode Meloidogyne incognita using deep sequencing. Funct Integr Genomics 2016; 16(2): 127-42.
[http://dx.doi.org/10.1007/s10142-015-0472-x] [PMID: 26743520]
[132]
Subramanian P, Choi IC, Mani V, et al. Stage-wise identification and analysis of miRNA from root-knot nematode Meloidogyne incognita. Int J Mol Sci 2016; 17(10): 1758.
[http://dx.doi.org/10.3390/ijms17101758] [PMID: 27775666]
[133]
Kulkarni AP, Mittal SP. Sequence data mining in search of hookworm (Necator americanus) microRNAs. Gene 2016; 590(2): 317-23.
[http://dx.doi.org/10.1016/j.gene.2016.05.039] [PMID: 27259664]
[134]
Rougon-Cardoso A, Flores-Ponce M, Ramos-Aboites HE, et al. The genome, transcriptome, and proteome of the nematode Steinernema carpocapsae: evolutionary signatures of a pathogenic lifestyle. Sci Rep 2016; 6: 37536.
[http://dx.doi.org/10.1038/srep37536] [PMID: 27876851]

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