A Deep Analysis of the Small Non-Coding RNA Population in Schistosoma japonicum Eggs

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Cai, Pengfei ^a   Piao, Xianyu ^a   Hao, Lili ^d   Liu, Shuai ^a   Hou, Nan ^a   Wang, Heng ^c   Chen, Qijun ^a,b  

^a INSTITUTE OF PATHOGEN BIOLOGY   (China)

^b JILIN UNIVERSITY   (China)

^c INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^d SOUTHWEST UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; MICRORNA; MICRORNA 36 3P; MICRORNA 71; MICRORNA 71 5P; SMALL UNTRANSLATED RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; LIVER; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; RABBIT; RNA ANALYSIS; RNA EXTRACTION; RNA PURIFICATION; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA; SNAIL; TRANSPOSON; WORM EGG;

ANIMALS; BASE SEQUENCE; DNA, RIBOSOMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; OVUM; RNA, SMALL UNTRANSLATED; RNA, TRANSFER; SCHISTOSOMA JAPONICUM; SEQUENCE ANALYSIS, RNA;

EID: 84877783095     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064003     Document Type: Article

References (71)

1. La Flamme AC, MacDonald AS, Huxtable CR, Carroll M, Pearce EJ, (2003) Lack of C3 affects Th2 response development and the sequelae of chemotherapy in schistosomiasis. J Immunol 170: 470-476.
2. Burke ML, Jones MK, Gobert GN, Li YS, Ellis MK, et al. (2009) Immunopathogenesis of human schistosomiasis. Parasite Immunol 31: 163-176.
3. Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, et al. (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85: 148-154.
4. Zaccone P, Burton O, Miller N, Jones FM, Dunne DW, et al. (2009) Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur J Immunol 39: 1098-1107.
5. Fairfax KC, Amiel E, King IL, Freitas TC, Mohrs M, et al. (2012) IL-10R blockade during chronic schistosomiasis mansoni results in the loss of B cells from the liver and the development of severe pulmonary disease. PLoS Pathog 8: e1002490.
6. Rutitzky LI, Stadecker MJ, (2011) Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-gamma. Eur J Immunol 41: 2677-2687.
7. van der Vlugt LE, Labuda LA, Ozir-Fazalalikhan A, Lievers E, Gloudemans AK, et al. (2012) Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS One 7: e30883.
8. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
9. Moazed D, (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413-420.
10. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, et al. (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12: 735-739.
11. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP, (2002) MicroRNAs in plants. Genes Dev 16: 1616-1626.
12. Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, et al. (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38: 803-814.
13. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, et al. (2005) Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
14. Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, et al. (2007) Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21: 644-648.
15. Wang Y, Medvid R, Melton C, Jaenisch R, Blelloch R, (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 39: 380-385.
16. Dalzell JJ, Warnock ND, Stevenson MA, Mousley A, Fleming CC, et al. (2010) Short interfering RNA-mediated knockdown of drosha and pasha in undifferentiated Meloidogyne incognita eggs leads to irregular growth and embryonic lethality. Int J Parasitol 40: 1303-1310.
17. Pauli A, Rinn JL, Schier AF, (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12: 136-149.
18. Hammond SM, Bernstein E, Beach D, Hannon GJ, (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404: 293-296.
19. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, et al. (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
20. Malone CD, Hannon GJ, (2009) Small RNAs as guardians of the genome. Cell 136: 656-668.
21. Halic M, Moazed D, Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140: 504-516.
22. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, et al. (2010) Transcriptional control of gene expression by microRNAs. Cell 140: 111-122.
23. Chen J, Yang Y, Guo S, Peng J, Liu Z, et al. (2010) Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum. Parasitol Res 107: 889-899.
24. Luo R, Xue X, Wang Z, Sun J, Zou Y, et al. (2010) Analysis and characterization of the genes encoding the Dicer and Argonaute proteins of Schistosoma japonicum. Parasit Vectors 3: 90.
25. Gomes MS, Cabral FJ, Jannotti-Passos LK, Carvalho O, Rodrigues V, et al. (2009) Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int 58: 61-68.
26. Cai P, Piao X, Hou N, Liu S, Wang H, et al. (2012) Identification and characterization of argonaute protein, Ago2 and its associated small RNAs in Schistosoma japonicum. PLoS Negl Trop Dis 6: e1745.
27. Simoes MC, Lee J, Djikeng A, Cerqueira GC, Zerlotini A, et al. (2011) Identification of Schistosoma mansoni microRNAs. BMC Genomics 12: 47.
28. Copeland CS, Marz M, Rose D, Hertel J, Brindley PJ, et al. (2009) Homology-based annotation of non-coding RNAs in the genomes of Schistosoma mansoni and Schistosoma japonicum. BMC Genomics 10: 464.
29. de Souza Gomes M, Muniyappa MK, Carvalho SG, Guerra-Sa R, Spillane C, (2011) Genome-wide identification of novel microRNAs and their target genes in the human parasite Schistosoma mansoni. Genomics 98: 96-111.
30. Friedlander MR, Adamidi C, Han T, Lebedeva S, Isenbarger TA, et al. (2009) High-resolution profiling and discovery of planarian small RNAs. Proc Natl Acad Sci U S A 106: 11546-11551.
31. Cucher M, Prada L, Mourglia-Ettlin G, Dematteis S, Camicia F, et al. (2011) Identification of Echinococcus granulosus microRNAs and their expression in different life cycle stages and parasite genotypes. Int J Parasitol 41: 439-448.
32. Xue X, Sun J, Zhang Q, Wang Z, Huang Y, et al. (2008) Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS One 3: e4034.
33. Huang J, Hao P, Chen H, Hu W, Yan Q, et al. (2009) Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PLoS One 4: e8206.
34. Lu YC, Smielewska M, Palakodeti D, Lovci MT, Aigner S, et al. (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. Rna 15: 1483-1491.
35. Wang Z, Xue X, Sun J, Luo R, Xu X, et al. (2010) An "in-depth" description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS Negl Trop Dis 4: e596.
36. Hao L, Cai P, Jiang N, Wang H, Chen Q, (2010) Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genomics 11: 55.
37. Xu MJ, Liu Q, Nisbet AJ, Cai XQ, Yan C, et al. (2010) Identification and characterization of microRNAs in Clonorchis sinensis of human health significance. BMC Genomics 11: 521.
38. Cai P, Hou N, Piao X, Liu S, Liu H, et al. (2011) Profiles of small non-coding RNAs in Schistosoma japonicum during development. PLoS Negl Trop Dis 5: e1256.
39. Poole CB, Davis PJ, Jin J, McReynolds LA, (2010) Cloning and bioinformatic identification of small RNAs in the filarial nematode, Brugia malayi. Mol Biochem Parasitol 169: 87-94.
40. Chen MX, Ai L, Xu MJ, Zhang RL, Chen SH, et al. (2011) Angiostrongylus cantonensis: identification and characterization of microRNAs in male and female adults. Exp Parasitol 128: 116-120.
41. Wang J, Czech B, Crunk A, Wallace A, Mitreva M, et al. (2011) Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res 21: 1462-1477.
42. Chen MX, Ai L, Xu MJ, Chen SH, Zhang YN, et al. (2011) Identification and characterization of microRNAs in Trichinella spiralis by comparison with Brugia malayi and Caenorhabditis elegans. Parasitol Res.
43. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158.
44. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ, (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-144.
45. Liu X, Song Y, Lu H, Tang B, Piao X, et al. (2011) Transcriptome of small regulatory RNAs in the development of the zoonotic parasite Trichinella spiralis. PLoS One 6: e26448.
46. Hertel J, Lindemeyer M, Missal K, Fried C, Tanzer A, et al. (2006) The expansion of the metazoan microRNA repertoire. BMC Genomics 7: 25.
47. Alvarez-Saavedra E, Horvitz HR, (2010) Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367-373.
48. Liu M, Liu P, Zhang L, Cai Q, Gao G, et al. (2011) mir-35 is involved in intestine cell G1/S transition and germ cell proliferation in C. elegans. Cell Res 21: 1605-1618.
49. Lee YS, Shibata Y, Malhotra A, Dutta A, (2009) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23: 2639-2649.
50. Fischer S, Benz J, Spath B, Jellen-Ritter A, Heyer R, et al. (2011) Regulatory RNAs in Haloferax volcanii. Biochem Soc Trans 39: 159-162.
51. Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F, et al. (2011) Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genomics 12: 288.
52. Thompson DM, Parker R, (2009) Stressing out over tRNA cleavage. Cell 138: 215-219.
53. Li Z, Ender C, Meister G, Moore PS, Chang Y, et al. (2012) Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res 40: 6787-6799.
54. Zhou Y, Zheng HJ, Chen YY, Zhang L, Wang K, et al. (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
55. Laha T, McManus DP, Loukas A, Brindley PJ, (2000) Sjalpha elements, short interspersed element-like retroposons bearing a hammerhead ribozyme motif from the genome of the oriental blood fluke Schistosoma japonicum. Biochim Biophys Acta 1492: 477-482.
56. Laha T, Loukas A, Verity CK, McManus DP, Brindley PJ, (2001) Gulliver, a long terminal repeat retrotransposon from the genome of the oriental blood fluke Schistosoma japonicum. Gene 264: 59-68.
57. Obbard DJ, Finnegan DJ, (2008) RNA interference: endogenous siRNAs derived from transposable elements. Curr Biol 18: R561-563.
58. Dalton JP, Day SR, Drew AC, Brindley PJ, (1997) A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology 115 (Pt1): 29-32.
59. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
60. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, et al. (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33: D121-124.
61. Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, et al. (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126: 203-224.
62. Zhao QP, Jiang MS, Dong HF, Nie P, (2012) Diversification of Schistosoma japonicum in Mainland China revealed by mitochondrial DNA. PLoS Negl Trop Dis 6: e1503.
63. Zhao GH, Blair D, Li XY, Li J, Lin RQ, et al. (2011) The ribosomal intergenic spacer (IGS) region in Schistosoma japonicum: structure and comparisons with related species. Infect Genet Evol 11: 610-617.
64. Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, et al. (2012) GenBank. Nucleic Acids Res 40: D48-53.
65. Laslett D, Canback B, (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32: 11-16.
66. Dsouza M, Larsen N, Overbeek R, (1997) Searching for patterns in genomic data. Trends Genet 13: 497-498.
67. Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA, (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12: 159-162.
68. Laha T, Brindley PJ, Verity CK, McManus DP, Loukas A, (2002) pido, a non-long terminal repeat retrotransposon of the chicken repeat 1 family from the genome of the Oriental blood fluke, Schistosoma japonicum. Gene 284: 149-159.
69. Laha T, Brindley PJ, Smout MJ, Verity CK, McManus DP, et al. (2002) Reverse transcriptase activity and untranslated region sharing of a new RTE-like, non-long terminal repeat retrotransposon from the human blood fluke, Schistosoma japonicum. Int J Parasitol 32: 1163-1174.
70. Kim SW, Li Z, Moore PS, Monaghan AP, Chang Y, et al. (2010) A sensitive non-radioactive northern blot method to detect small RNAs. Nucleic Acids Res 38: e98.
71. Pall GS, Hamilton AJ, (2008) Improved northern blot method for enhanced detection of small RNA. Nat Protoc 3: 1077-1084.