High-throughput sequencing of RNAs isolated by cross-linking immunoprecipitation (HITS-CLIP) reveals Argonaute-associated microRNAs and targets in Schistosoma japonicum

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Zhao, Jing ^a   Luo, Rong ^a   Xu, Xindong ^a   Zou, Ying ^a   Zhang, Qingfeng ^a   Pan, Weiqing ^a,b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Argonaute; HITS CLIP; microRNA; Schistosoma japonicum; Target sites

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; MICRORNA 1; MICRORNA 256; MICRORNA 513; UNCLASSIFIED DRUG; HELMINTH PROTEIN; HELMINTH RNA;

ADULT; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; GENE CONTROL; GENE IDENTIFICATION; GENE INTERACTION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; NONHUMAN; RNA EXTRACTION; RNA ISOLATION; RNA SEQUENCE; SCHISTOSOMA JAPONICUM; ANIMAL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS;

ANIMALS; ARGONAUTE PROTEINS; GENE EXPRESSION REGULATION; HELMINTH PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IMMUNOPRECIPITATION; MICRORNAS; MOLECULAR SEQUENCE DATA; RNA, HELMINTH; SCHISTOSOMA JAPONICUM; SEQUENCE ANALYSIS, DNA;

EID: 84947064465     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-1203-9     Document Type: Article

References (54)

1. Makaula P, Sadalaki JR, Muula AS, Kayuni S, Jemu S, Bloch P. Schistosomiasis in Malawi: a systematic review. Parasit Vectors. 2014;7:570.
2. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta trop. 2000;77:41-51.
3. King CH. Parasites and poverty: the case of schistosomiasis. Acta trop. 2010;113:95-104.
4. Liu F, Lu J, Hu W, Wang SY, Cui SJ, Chi M, et al. New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS pathog. 2006;2:268-81.
5. Han ZG, Brindley PJ, Wang SY, Chen Z. Schistosoma genomics: new perspectives on schistosome biology and host-parasite interaction. Annu Rev Genomics Hum Genet. 2009;10:211-40.
6. Cai P, Hou N, Piao X, Liu S, Liu H, Yang F, et al. Profiles of small non-coding RNAs in Schistosoma japonicum during development. PLoS Negl Trop Dis. 2011;5:e1256.
7. Sun J, Wang SW, Li C, Ren YJ, Wang JQ. Novel expression profiles of microRNAs suggest that specific miRNAs regulate gene expression for the sexual maturation of female Schistosoma japonicum after pairing. Parasit Vectors. 2014;7:177.
8. Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem cells. 2010;28(2):357-64.
9. Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP, et al. MicroRNA-1 regulates smooth muscle cell differentiation by repressing Kruppel-like factor 4. Stem Cells Dev. 2011;20:205-10.
10. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466:835-40.
11. Hagen J, Lee EF, Fairlie WD, Kalinna BH. Functional genomics approaches in parasitic helminths. Parasite Immunol. 2012;34:163-82.
12. Williams AE. Functional aspects of animal microRNAs. Cellular and molecular life sciences: CMLS. 2008;65(4):545-62.
13. Ai L, Xu MJ, Chen MX, Zhang YN, Chen SH, Guo J, et al. Characterization of microRNAs in Taenia saginata of zoonotic significance by Solexa deep sequencing and bioinformatics analysis. Parasitol Res. 2012;110:2373-8.
14. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature. 2010;465:316-21.
15. Kim VN. Small RNAs: classification, biogenesis, and function. Mol Cells. 2005;19:1-15.
16. Bartel DP. MicroRNAs: Target Recognition and Regulatory Functions. Cell. 2009;136:215-33.
17. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004;5:522-31.
18. Cheng G, Jin Y. MicroRNAs: potentially important regulators for schistosome development and therapeutic targets against schistosomiasis. Parasitology. 2012;139:669-79.
19. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116:281-97.
20. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell. 2007;131:1097-108.
21. Forstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by Dicer-1. Cell. 2007;130:287-97.
22. Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 2002;16:2733-42.
23. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460:479-86.
24. 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:e4034.
25. 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.
26. 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:e1745.
27. 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;98:96-111.
28. Wang Z, Xue X, Sun J, Luo R, Xu X, Jiang Y, et al. An "in-depth" description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS Negl Trop Dis. 2010;4:e596.
29. Cai P, Piao X, Hao L, Liu S, Hou N, Wang H, et al. A deep analysis of the small non-coding RNA population in Schistosoma japonicum eggs. PloS one. 2013;8:e64003.
30. Hock J, Meister G. The Argonaute protein family. Genome biol. 2008;9:210.
31. 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.
32. Gomez-Manzo S, Terron-Hernandez J, de la Mora-de la Mora I, Garcia-Torres I, Lopez-Velazquez G, Reyes-Vivas H, et al. Cloning, expression, purification and characterization of his-tagged human glucose-6-phosphate dehydrogenase: a simplified method for protein yield. Protein J. 2013;32:585-92.
33. Cai P, Bu L, Wang J, Wang Z, Zhong X, Wang H. Molecular characterization of Schistosoma japonicum tegument protein tetraspanin-2: sequence variation and possible implications for immune evasion. Biochem Biophys Res Commun. 2008;372:197-202.
34. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 2005;33:D121-4.
35. Dsouza M, Larsen N, Overbeek R. Searching for patterns in genomic data. Trends Genet. 1997;13:497-8.
36. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36:D154-8.
37. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006;34:D140-4.
38. Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42:D68-73.
39. Grimson A, Farh KK-H, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing. Mol Cell. 2007;27:91-105.
40. 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;40:37-52.
41. Madeira C, Ribeiro SC, Turk MZ, Cabral JM. Optimization of gene delivery to HEK293T cells by microporation using a central composite design methodology. Biotechnol Lett. 2010;32:1393-9.
42. Maniataki E, De Planell Saguer MD, Mourelatos Z. Immunoprecipitation of microRNPs and directional cloning of microRNAs. Methods Mol Biol. 2005;309:283-94.
43. Kruger J, Rehmsmeier M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 2006;34:W451-4.
44. Friedlander MR, Lizano E, Houben AJS, Bezdan D, Banez-Coronel M, Kudla G, et al. Evidence for the biogenesis of more than 1,000 novel human microRNAs. Genome Biology. 2014;15:R57.
45. Krutzfeldt J, Poy MN, Stoffel M. Strategies to determine the biological function of microRNAs. Nat Genet. 2006;38:S14-19.
46. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19:92-105.
47. Szczesniak MW, Deorowicz S, Gapski J, Kaczynski L, Makalowska I. miRNEST database: an integrative approach in microRNA search and annotation. Nucleic Acids Res. 2012;40:D198-204.
48. Gusev Y, Schmittgen TD, Lerner M, Postier R, Brackett D. Computational analysis of biological functions and pathways collectively targeted by co-expressed microRNAs in cancer. BMC Bioinformatics. 2007;8(Suppl 7):S16.
49. Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, et al. A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 2004;18:1165-78.
50. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet. 2005;37:495-500.
51. Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, et al. A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci U S A. 2007;104:19291-6.
52. Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006;38:228-33.
53. Wang D, Zhang Z, O'Loughlin E, Lee T, Houel S, O'Carroll D, et al. Quantitative functions of Argonaute proteins in mammalian development. Genes Dev. 2012;26:693-704.
54. Gomes MS, Cabral FJ, Jannotti-Passos LK, Carvalho O, Rodrigues V, Baba EH, et al. Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int. 2009;58:61-8.