Genome-wide sequencing of small RNAs reveals a tissue-specific loss of conserved microRNA families in Echinococcus granulosus

BMC Genomics

Shengyue Wang¹  Wenbao Zhang⁴  Donald P McManus³  Jun Li⁴  Baoxin Shi²  Li Zhao²  Fengshou Ma¹  Xia Li¹  Lu Zhang¹  Yongqiang Zhu¹  Hui Kang¹  Lei Jin¹  Zhuangzhi Zhang²  Yun Bai¹ 

[1] Shanghai-MOST Key Laboratory of Health and Disease Genomics, Chinese National Human Genome Center at Shanghai, 250 Bibo Road, Shanghai 201203, China;Veterinary Research Institute, Xinjiang Academy of Animal Sciences, 151 East-Kelamayi Street, Urumqi, Xinjiang 830000, China;Molecular Parasitology Laboratory, QIMR Berghofer Institute of Medical Research, Brisbane, QLD, Australia;State Key Laboratory Incubation Base of Xinjiang Major Diseases Research, Clinical Medical Research Institute, The First Affiliated Hospital of Xinjiang Medical University, No. 1 Liyushan Road, Urumqi, Xinjiang 830054, China

关键词: Life cycle stage development;    Differential expression;    Deep sequencing;    microRNA;    Echinococcus granulosus;   

Others  :  1141130
DOI  :  10.1186/1471-2164-15-736

 received in 2014-03-20, accepted in 2014-08-20,  发布年份 2014

【 摘 要 】

Background

MicroRNAs (miRNAs) are important post-transcriptional regulators which control growth and development in eukaryotes. The cestode Echinococcus granulosus has a complex life-cycle involving different development stages but the mechanisms underpinning this development, including the involvement of miRNAs, remain unknown.

Results

Using Illumina next generation sequencing technology, we sequenced at the genome-wide level three small RNA populations from the adult, protoscolex and cyst membrane of E. granulosus. A total of 94 pre-miRNA candidates (coding 91 mature miRNAs and 39 miRNA stars) were in silico predicted. Through comparison of expression profiles, we found 42 mature miRNAs and 23 miRNA stars expressed with different patterns in the three life stages examined. Furthermore, considering both the previously reported and newly predicted miRNAs, 25 conserved miRNAs families were identified in the E. granulosus genome. Comparing the presence or absence of these miRNA families with the free-living Schmidtea mediterranea, we found 13 conserved miRNAs are lost in E. granulosus, most of which are tissue-specific and involved in the development of ciliated cells, the gut and sensory organs. Finally, GO enrichment analysis of the differentially expressed miRNAs and their potential targets indicated that they may be involved in bi-directional development, nutrient metabolism and nervous system development in E. granulosus.

Conclusions

This study has, for the first time, provided a comprehensive description of the different expression patterns of miRNAs in three distinct life cycle stages of E. granulosus. The analysis supports earlier suggestions that the loss of miRNAs in the Platyhelminths might be related to morphological simplification. These results may help in the exploration of the mechanism of interaction between this parasitic worm and its definitive and intermediate hosts, providing information that can be used to develop new interventions and therapeutics for the control of cystic echinococcosis.

【 授权许可】

   
2014 Bai et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Carrington JC, Ambros V: Role of microRNAs in plant and animal development. Science 2003, 301(5631):336-338.
• [2]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297.
• [3]Ambros V: MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 2003, 113(6):673-676.
• [4]Kozomara A, Griffiths-Jones S: miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39(Database issue):D152-157.
• [5]Niwa R, Slack FJ: The evolution of animal microRNA function. Curr Opin Genet Dev 2007, 17(2):145-150.
• [6]Heimberg AM, Sempere LF, Moy VN, Donoghue PC, Peterson KJ: MicroRNAs and the advent of vertebrate morphological complexity. Proc Natl Acad Sci U S A 2008, 105(8):2946-2950.
• [7]Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D: Ancient animal microRNAs and the evolution of tissue identity. Nature 2010, 463(7284):1084-1088.
• [8]Tarver JE, Sperling EA, Nailor A, Heimberg AM, Robinson JM, King BL, Pisani D, Donoghue PC, Peterson KJ: miRNAs: small genes with big potential in metazoan phylogenetics. Mol Biol Evol 2013, 30(11):2369-2382.
• [9]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):2619-2628.
• [10]Eckert J, Deplazes P: Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 2004, 17(1):107-135.
• [11]Craig PS, Larrieu E: Control of cystic echinococcosis/hydatidosis: 1863–2002. Adv Parasitol 2006, 61:443-508.
• [12]Craig PS, McManus DP, Lightowlers MW, Chabalgoity JA, Garcia HH, Gavidia CM, Gilman RH, Gonzalez AE, Lorca M, Naquira C, Nieto A, Schantz PM: Prevention and control of cystic echinococcosis. Lancet Infect Dis 2007, 7(6):385-394.
• [13]Li T, Ito A, Pengcuo R, Sako Y, Chen X, Qiu D, Xiao N, Craig PS: Post-treatment follow-up study of abdominal cystic echinococcosis in tibetan communities of northwest Sichuan Province. China PLoS Negl Trop Dis 2011, 5(10):e1364.
• [14]Moro PL, Gilman RH, Verastegui M, Bern C, Silva B, Bonilla JJ: Human hydatidosis in the central Andes of Peru: evolution of the disease over 3 years. Clin Infect Dis 1999, 29(4):807-812.
• [15]McManus DP, Zhang W, Li J, Bartley PB: Echinococcosis. Lancet 2003, 362(9392):1295-1304.
• [16]Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, Kang H, Chen J, Wang L, Chen A, Yu S, Gao Z, Jin L, Gu W, Wang Z, Zhao L, Shi B, Wen H, Lin R, Jones MK, Brejova B, Vinar T, Zhao G, McManus DP, Chen Z, Zhou Y, et al.: The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet 2013, 45(10):1168-1175.
• [17]Cui SJ, Xu LL, Zhang T, Xu M, Yao J, Fang CY, Feng Z, Yang PY, Hu W, Liu F: Proteomic characterization of larval and adult developmental stages in Echinococcus granulosus reveals novel insight into host-parasite interactions. J Proteomics 2013, 84:158-175.
• [18]Friedlander MR, Adamidi C, Han T, Lebedeva S, Isenbarger TA, Hirst M, Marra M, Nusbaum C, Lee WL, Jenkin JC, Sánchez Alvarado A, Kim JK, Rajewsky N: High-resolution profiling and discovery of planarian small RNAs. Proc Natl Acad Sci U S A 2009, 106(28):11546-11551.
• [19]Palakodeti D, Smielewska M, Graveley BR: MicroRNAs from the Planarian Schmidtea mediterranea: a model system for stem cell biology. RNA 2006, 12(9):1640-1649.
• [20]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.
• [21]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.
• [22]Huang J, Hao P, Chen H, Hu W, Yan Q, Liu F, Han ZG: Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PLoS One 2009, 4(12):e8206.
• [23]de Souza GM, Muniyappa MK, Carvalho SG, Guerra-Sa 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.
• [24]Simoes MC, Lee J, Djikeng A, Cerqueira GC, Zerlotini A, da Silva-Pereira RA, Dalby AR, LoVerde P, El-Sayed NM, Oliveira G: Identification of Schistosoma mansoni microRNAs. BMC Genomics 2011, 12:47.
• [25]Cucher M, Prada L, Mourglia-Ettlin G, Dematteis S, Camicia F, Asurmendi S, Rosenzvit M: Identification of Echinococcus granulosus microRNAs and their expression in different life cycle stages and parasite genotypes. Int J Parasitol 2011, 41(3–4):439-448.
• [26]Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ, Jacobsen SE: Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat Genet 2006, 38(6):721-725.
• [27]Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N: miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 2012, 40(1):37-52.
• [28]Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ: Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005, 33(20):e179.
• [29]Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T: Identification of novel genes coding for small expressed RNAs. Science 2001, 294(5543):853-858.
• [30]Lewis BP, Burge CB, Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120(1):15-20.
• [31]Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB: Prediction of mammalian microRNA targets. Cell 2003, 115(7):787-798.
• [32]Meyers BC, Tej SS, Vu TH, Haudenschild CD, Agrawal V, Edberg SB, Ghazal H, Decola S: The use of MPSS for whole-genome transcriptional analysis in Arabidopsis. Genome Res 2004, 14(8):1641-1653.
• [33]Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K: Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 2000, 18(6):630-634.
• [34]Wang Z, Xue X, Sun J, Luo R, Xu X, Jiang Y, Zhang Q, Pan W: An “in-depth” description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS Negl Trop Dis 2010, 4(2):e596.
• [35]Kato M, de Lencastre A, Pincus Z, Slack F: Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 2009, 10(5):R54.
• [36]Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS: MicroRNA targets in Drosophila. Genome Biol 2003, 5(1):R1.
• [37]Sperling EA, Peterson KJ: microRNAs and metazoan phylogeny: big trees from little genes. In Animal evolution-genomes, trees and fossils. Edited by Telford MJ, Littlewood DTJ. Oxford: Oxford University Press; 2009:157-170.
• [38]Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ: The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 2011, 334(6059):1091-1097.
• [39]Aboobaker AA, Tomancak P, Patel N, Rubin GM, Lai EC: Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci U S A 2005, 102(50):18017-18022.
• [40]Shalom-Feuerstein R, Serror L, De La Forest DS, Petit I, Aberdam E, Camargo L, Damour O, Vigouroux C, Solomon A, Gaggioli C, Itskovitz-Eldor J, Ahmad S, Aberdam D: Pluripotent stem cell model reveals essential roles for miR-450b-5p and miR-184 in embryonic corneal lineage specification. Stem Cells 2012, 30(5):898-909.
• [41]Nairz K, Rottig C, Rintelen F, Zdobnov E, Moser M, Hafen E: Overgrowth caused by misexpression of a microRNA with dispensable wild-type function. Dev Biol 2006, 291(2):314-324.
• [42]Wheeler BM, Heimberg AM, Moy VN, Sperling EA, Holstein TW, Heber S, Peterson KJ: The deep evolution of metazoan microRNAs. Evol Dev 2009, 11(1):50-68.
• [43]Rigano R, Buttari B, Profumo E, Ortona E, Delunardo F, Margutti P, Mattei V, Teggi A, Sorice M, Siracusano A: Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infect Immun 2007, 75(4):1667-1678.
• [44]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):1751-1761.
• [45]Bernal D, Trelis M, Montaner S, Cantalapiedra F, Galiano A, Hackenberg M, Marcilla A: Surface analysis of Dicrocoelium dendriticum. The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics 2014, 105:232-241.
• [46]Holcman B, Heath DD: The early stages of Echinococcus granulosus development. Acta Trop 1997, 64(1–2):5-17.
• [47]Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF: MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308(5723):833-838.
• [48]Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF: Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312(5770):75-79.
• [49]Hunter SE, Finnegan EF, Zisoulis DG, Lovci MT, Melnik-Martinez KV, Yeo GW, Pasquinelli AE: Functional genomic analysis of the let-7 regulatory network in Caenorhabditis elegans. PLoS Genet 2013, 9(3):e1003353.
• [50]Smyth JD: In Vitro Cultivation Of Parasitic Helminths. Boca Raton: CRC Press; 1990.
• [51]Bethke A, Fielenbach N, Wang Z, Mangelsdorf DJ, Antebi A: Nuclear hormone receptor regulation of microRNAs controls developmental progression. Science 2009, 324(5923):95-98.
• [52]Hammell CM, Karp X, Ambros V: A feedback circuit involving let-7-family miRNAs and DAF-12 integrates environmental signals and developmental timing in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2009, 106(44):18668-18673.
• [53]Li J, Zhang CS, Lu GD, Wang JH, Wen H, Yan GQ, Wei XF, Lin RY: Molecular characterization of a signal-regulated kinase homolog from Echinococcus granulosus. Chin Med J (Engl) 2011, 124(18):2838-2844.
• [54]Zhang W, Li J, Jones MK, Zhang Z, Zhao L, Blair D, McManus DP: The Echinococcus granulosus antigen B gene family comprises at least 10 unique genes in five subclasses which are differentially expressed. PLoS Negl Trop Dis 2010, 4(8):e784.
• [55]Zhang W, Zhang Z, Shi B, Li J, You H, Tulson G, Dang X, Song Y, Yimiti T, Wang J, Jones MK, McManus DP: Vaccination of dogs against Echinococcus granulosus, the cause of cystic hydatid disease in humans. J Infect Dis 2006, 194(7):966-974.
• [56]Wang WC, Lin FM, Chang WC, Lin KY, Huang HD, Lin NS: miRExpress: analyzing high-throughput sequencing data for profiling microRNA expression. BMC Bioinformatics 2009, 10:328.
• [57]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25.
• [58]Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N: Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 2008, 26(4):407-415.
• [59]Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL: The Vienna RNA websuite. Nucleic Acids Res 2008, 36(Web Server issue):W70-74.
• [60]Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T: A uniform system for microRNA annotation. RNA 2003, 9(3):277-279.
• [61]Wang L, Feng Z, Wang X, Zhang X: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010, 26(1):136-138.
• [62]Grant GR, Liu J, Stoeckert CJ Jr: A practical false discovery rate approach to identifying patterns of differential expression in microarray data. Bioinformatics 2005, 21(11):2684-2690.
• [63]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
• [64]Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA: Identifying biological themes within lists of genes with EASE. Genome Biol 2003, 4(10):R70.
• [65]Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M: KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007, 35(Web Server issue):W182-185.