Differential expression of microRNAs and tRNA fragments mediate the adaptation of the liver fluke Fasciola gigantica to its intermediate snail and definitive mammalian hosts

International Journal for Parasitology - Tập 51 - Trang 405-414 - 2021
Rui-Si Hu1,2, Xiao-Xuan Zhang3, Qiao-Ni Ma1, Hany M. Elsheikha4, Muhammad Ehsan1, Quan Zhao2, Bastian Fromm5, Xing-Quan Zhu1,6,7
1State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, China
2College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin Province 130118, China
3College of Veterinary Medicine, Qingdao Agricultural University, Qingdao, Shandong Province 266109, China
4Faculty of Medicine and Health Sciences, School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK
5Science for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, S-10691 Stockholm, Sweden
6College of Veterinary Medicine, Shanxi Agricultural University, Taigu, Shanxi Province 030801, China
7Key Laboratory of Veterinary Public Health of Yunnan Province, College of Veterinary Medicine, Yunnan Agricultural University, Kunming, Yunnan Province 650201, China

Tài liệu tham khảo

Aebi, 1990, Isolation of a temperature-sensitive mutant with an altered tRNA nucleotidyltransferase and cloning of the gene encoding tRNA nucleotidyltransferase in the yeast Saccharomyces cerevisiae, J. Biol. Chem., 265, 16216, 10.1016/S0021-9258(17)46210-7 Andrews, 1999, The life cycle of Fasciola hepatica, 1 Baek, 2008, The impact of microRNAs on protein output, Nature, 455, 64, 10.1038/nature07242 Bai, 2014, Genome-wide sequencing of small RNAs reveals a tissue-specific loss of conserved microRNA families in Echinococcus granulosus, BMC Genomics, 15, 736, 10.1186/1471-2164-15-736 Bartel, 2018, Metazoan microRNAs, Cell, 173, 20, 10.1016/j.cell.2018.03.006 Basika, 2016, Identification and profiling of microRNAs in two developmental stages of the model cestode parasite Mesocestoides corti, Mol. Biochem. Parasitol., 210, 37, 10.1016/j.molbiopara.2016.08.004 Betel, 2010, Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites, Genome Biol., 11, R90, 10.1186/gb-2010-11-8-r90 Cai, 2016, MicroRNAs in parasitic helminthiases: current status and future perspectives, Trends Parasitol., 32, 71, 10.1016/j.pt.2015.09.003 Chan, 2019, tRNAscan-SE: searching for tRNA genes in genomic sequences, Methods Mol. Biol., 1962, 1, 10.1007/978-1-4939-9173-0_1 Conesa, 2005, Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research, Bioinformatics, 21, 3674, 10.1093/bioinformatics/bti610 Cristodero, 2017, The multifaceted regulatory potential of tRNA-derived fragments, Non-coding RNA Invest., 1, 7, 10.21037/ncri.2017.08.07 Cwiklinski, 2016, A prospective view of animal and human Fasciolosis, Parasite Immunol., 38, 558, 10.1111/pim.12343 Drurey, 2020, Extracellular vesicles: new targets for vaccines against helminth parasites, Int. J. Parasitol., 50, 623, 10.1016/j.ijpara.2020.04.011 Fontenla, 2015, The miRnome of Fasciola hepatica juveniles endorses the existence of a reduced set of highly divergent microRNAs in parasitic flatworms, Int. J. Parasitol., 45, 901, 10.1016/j.ijpara.2015.06.007 Fricker, 2019, A tRNA half modulates translation as stress response in Trypanosoma brucei, Nature Commun., 10, 118, 10.1038/s41467-018-07949-6 Friedlander, 2012, miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades, Nucleic. Acids Res., 40, 37, 10.1093/nar/gkr688 Fromm, 2015, A uniform system for the annotation of vertebrate microRNA genes and the evolution of the human microRNAome, Annu. Rev. Genet., 49, 213, 10.1146/annurev-genet-120213-092023 Fromm, 2014, MicroRNA loci support conspecificity of Gyrodactylus salaris and Gyrodactylus thymalli (Platyhelminthes: Monogenea), Int. J. Parasitol., 44, 787, 10.1016/j.ijpara.2014.05.010 Fromm, 2020, MirGeneDB 2.0: the metazoan microRNA complement, Nucleic. Acids Res., 48, D132, 10.1093/nar/gkz885 Fromm, 2017, On the presence and immunoregulatory functions of extracellular microRNAs in the trematode Fasciola hepatica, Parasite Immunol., 39, 10.1111/pim.12399 Fromm, 2015, 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., 45, 697, 10.1016/j.ijpara.2015.06.002 Fromm, 2013, Substantial loss of conserved and gain of novel microRNA families in flatworms, Mol. Biol. Evol., 30, 2619, 10.1093/molbev/mst155 Furst, 2012, Global burden of human food-borne trematodiasis: a systematic review and meta-analysis, Lancet Infect. Dis., 12, 210, 10.1016/S1473-3099(11)70294-8 Gebert, 2018, Regulation of microRNA function in animals, Nat. Rev. Mol. Cell Biol., 20, 21, 10.1038/s41580-018-0045-7 Guo, 2019, Profiling circulating microRNAs in serum of Fasciola gigantica-infected buffalo, Mol. Biochem. Parasitol., 232, 10.1016/j.molbiopara.2019.111201 Hansen, 2019, Exploration of extracellular vesicles from provides evidence of parasite-host cross talk, J. Extracell. Vesicles, 8, 1578116, 10.1080/20013078.2019.1578116 Harrington, 2017, Human liver flukes. Lancet, Gastroenterol. Hepatol., 2, 680 He, 2020, A schistosome miRNA promotes host hepatic fibrosis by targeting transforming growth factor beta receptor III, J. Hepatol., 72, 519, 10.1016/j.jhep.2019.10.029 Huang, 2017, ExUTR: a novel pipeline for large-scale prediction of 3'-UTR sequences from NGS data, BMC Genomics, 18, 847, 10.1186/s12864-017-4241-1 Hu, 2020, Proteomic profiling of the liver, hepatic lymph nodes, and spleen of buffaloes infected with Fasciola gigantica, Pathogens, 9, 982, 10.3390/pathogens9120982 Jan, 2011, Formation, regulation and evolution of Caenorhabditis elegans 3'UTRs, Nature, 469, 97, 10.1038/nature09616 Jiang, 2008, SeqMap: mapping massive amount of oligonucleotides to the genome, Bioinformatics, 24, 2395, 10.1093/bioinformatics/btn429 Kanai, 2015, Disrupted tRNA genes and tRNA fragments: a perspective on tRNA gene evolution, Life (Basel), 5, 321 Kang, 2018, miRTrace reveals the organismal origins of microRNA sequencing data, Genome Biol., 19, 213, 10.1186/s13059-018-1588-9 Kenny, 2015, The phylogenetic utility and functional constraint of microRNA flanking sequences, Proc. Biol. Sci., 282, 20142983 King, 2015, Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world, PLoS Pathog., 11, 10.1371/journal.ppat.1005098 Liu, 2019, Schistosoma japonicum extracellular vesicle miRNA cargo regulates host macrophage functions facilitating parasitism, PLoS Pathog., 15, 10.1371/journal.ppat.1007817 Lyons, 2016, YB-1 regulates tiRNA-induced stress granule formation but not translational repression, Nucleic Acids Res., 44, 6949, 10.1093/nar/gkw418 Macchiaroli, 2015, microRNA profiling in the zoonotic parasite Echinococcus canadensis using a high-throughput approach, Parasit. Vectors, 8, 83, 10.1186/s13071-015-0686-8 Marco, 2013, Clusters of microRNAs emerge by new hairpins in existing transcripts, Nucleic Acids Res., 41, 7745, 10.1093/nar/gkt534 Mas-Coma, 2005, Epidemiology of fascioliasis in human endemic areas, J. Helminthol., 79, 207, 10.1079/JOH2005296 Mas-Coma, 2018, Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures, Parasitology, 145, 1665, 10.1017/S0031182018000914 Nowacki, 2015, Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni, J. Extracell. Vesicles, 4, 28665, 10.3402/jev.v4.28665 Ovchinnikov, 2020, EV-transported microRNAs of Schistosoma mansoni and Fasciola hepatica: Potential targets in definitive hosts, Infect. Genet. Evol., 85, 10.1016/j.meegid.2020.104528 Ovchinnikov, 2017, Extreme conservation of miRNA complement in opisthorchiids, Parasitol. Int., 66, 773, 10.1016/j.parint.2017.09.006 Pandey, 2020, Draft genome of the liver fluke Fasciola gigantica, ACS Omega, 5, 11084, 10.1021/acsomega.0c00980 Phalee, 2015, Experimental life history and biological characteristics of Fasciola gigantica (Digenea: Fasciolidae), Korean J. Parasitol., 53, 59, 10.3347/kjp.2015.53.1.59 Rehmsmeier, 2004, Fast and effective prediction of microRNA/target duplexes, RNA, 10, 1507, 10.1261/rna.5248604 Richter, 2018, RNA modification landscape of the human mitochondrial tRNA regulates protein synthesis, Nature Commun., 9, 3966, 10.1038/s41467-018-06471-z Sokol, 2005, Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth, Genes Dev., 19, 2343, 10.1101/gad.1356105 Sotillo, 2020, The protein and microRNA cargo of extracellular vesicles from parasitic helminths-current status and research priorities, Int. J. Parasitol., 50, 635, 10.1016/j.ijpara.2020.04.010 Taylor, 2020, Trichinella spiralis secretes abundant unencapsulated small RNAs with potential effects on host gene expression, Int. J. Parasitol., 50, 697, 10.1016/j.ijpara.2020.05.008 Toet, 2014, Liver fluke vaccines in ruminants: strategies, progress and future opportunities, Int. J. Parasitol., 44, 915, 10.1016/j.ijpara.2014.07.011 Torgerson, 1999, Epidemiology and control, 113 Torgerson, 2015, World health organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis, PLoS Med., 12, 10.1371/journal.pmed.1001920 Wang, 2020, A microRNA derived from Schistosoma japonicum promotes schistosomiasis hepatic fibrosis by targeting host secreted frizzled-related protein 1, Front. Cell Infect. Microbiol., 10, 101, 10.3389/fcimb.2020.00101 Xiong, 2006, A story with a good ending: tRNA 3'-end maturation by CCA-adding enzymes, Curr. Opin. Struct. Biol., 16, 12, 10.1016/j.sbi.2005.12.001 Xu, 2012, Comparative characterization of microRNAs from the liver flukes Fasciola gigantica and F. hepatica, PLoS One, 7, 10.1371/journal.pone.0053387 Yamasaki, 2009, Angiogenin cleaves tRNA and promotes stress-induced translational repression, J. Cell Biol., 185, 35, 10.1083/jcb.200811106 Young, 2011, A portrait of the transcriptome of the neglected trematode, Fasciola gigantica-biological and biotechnological implications, PLoS Negl. Trop. Dis., 5, 10.1371/journal.pntd.0001004 Yu, 2019, Comprehensive analysis of miRNA profiles reveals the role of Schistosoma japonicum miRNAs at different developmental stages, Vet. Res., 50, 23, 10.1186/s13567-019-0642-2 Zhang, 2019, Global serum proteomic changes in water buffaloes infected with Fasciola gigantica, Parasit. Vectors, 12, 281, 10.1186/s13071-019-3533-5 Zhang, 2020, Comprehensive analysis of non-coding RNA profiles of exosome-like vesicles from the protoscoleces and hydatid cyst fluid of Echinococcus granulosus, Front. Cell Infect. Microbiol., 10, 316, 10.3389/fcimb.2020.00316 Zhang, 2017, De novo transcriptome sequencing and analysis of the juvenile and adult stages of Fasciola gigantica, Infect. Genet. Evol., 51, 33, 10.1016/j.meegid.2017.03.007 Zhang, 2019, Complex and dynamic transcriptional changes allow the helminth Fasciola gigantica to adjust to its intermediate snail and definitive mammalian hosts, BMC Genomics, 20, 729, 10.1186/s12864-019-6103-5 Zhu, 2016, MicroRNAs are involved in the regulation of ovary development in the pathogenic blood fluke Schistosoma japonicum, PLoS Pathog., 12, 10.1371/journal.ppat.1005423