A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni

PLoS Neglected Tropical Diseases

Volumn 6, Issue 1, 2012, Pages

  Protasio, Anna V ^a   Tsai, Isheng J ^a   Babbage, Anne ^a   Nichol, Sarah ^a   Hunt, Martin ^a   Aslett, Martin A ^a   de Silva, Nishadi ^a   Velarde, Giles S ^a   Anderson, Tim J C ^b   Clark, Richard C ^a   Davidson, Claire ^a   Dillon, Gary P ^a   Holroyd, Nancy E ^a   LoVerde, Philip T ^c   Lloyd, Christine ^a   McQuillan, Jacquelline ^a   Oliveira, Guilherme ^d   Otto, Thomas D ^a   Parker Manuel, Sophia J ^e   Quail, Michael A ^a   Wilson, R Alan ^e   Zerlotini, Adhemar ^d   Dunne, David W ^f   Berriman, Matthew ^a   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d INSTITUTO OSWALDO CRUZ   (Brazil)

^e UNIVERSITY OF YORK   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SCAFFOLD PROTEIN; TRANSCRIPTOME; HELMINTH DNA; HELMINTH RNA;

ARTICLE; CERCARIA; FEMALE; GENE EXPRESSION; GENETIC MODEL; GENOME; MALE; MIRACIDIUM; MITOCHONDRIAL GENOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SCHISTOSOMA MANSONI; SCHISTOSOMULUM; SEX CHROMOSOME; TRANS SPLICING; ANIMAL; CHEMISTRY; DNA SEQUENCE; GENETICS; MOLECULAR GENETICS;

ANIMALS; DNA, HELMINTH; GENOME, HELMINTH; MOLECULAR SEQUENCE DATA; RNA, HELMINTH; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84856579279     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001455     Document Type: Article

References (58)

1. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411-425.
2. Cook GC, Zumla A, Manson PSTd, (2003) Manson's tropical diseases Edinburgh Saunders [1812] p. of plates p xiii, 1847.
3. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
4. The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
5. Li R, Fan W, Tian G, Zhu H, He L, et al. (2010) The sequence and de novo assembly of the giant panda genome. Nature 463: 311-317.
6. Nowrousian M, Stajich JE, Chu M, Engh I, Espagne E, et al. (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6: e1000891.
7. Tsai IJ, Otto TD, Berriman M, (2010) Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 11: R41.
8. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
9. Hillier LW, Reinke V, Green P, Hirst M, Marra MA, et al. (2009) Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res 19: 657-666.
10. Daines B, Wang H, Wang L, Li Y, Han Y, et al. (2011) The Drosophila melanogaster transcriptome by paired-end RNA sequencing. Genome Res 21: 315-324.
11. Lu T, Lu G, Fan D, Zhu C, Li W, et al. (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20: 1238-1249.
12. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
13. Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, et al. (2010) RNA-Seq Atlas of Glycine max: A guide to the soybean transcriptome. BMC Plant Biol 10: 160.
14. Oshlack A, Robinson MD, Young MD, (2010) From RNA-seq reads to differential expression results. Genome Biol 11: 220.
15. Shendure J, (2008) The beginning of the end for microarrays? Nat Methods 5: 585-587.
16. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y, (2008) RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
17. Criscione CD, Valentim CL, Hirai H, LoVerde PT, Anderson TJ, (2009) Genomic linkage map of the human blood fluke Schistosoma mansoni. Genome Biol 10: R71.
18. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, et al. (2009) Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat Methods 6: 291-295.
19. Brink LH, McLaren DJ, Smithers SR, (1977) Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74: 73-86.
20. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, et al. (2002) ARACHNE: a whole-genome shotgun assembler. Genome Res 12: 177-189.
21. Hirai H, LoVerde PT, (1996) Identification of the telomeres on Schistosoma mansoni chromosomes by FISH. J Parasitol 82: 511-512.
22. Otto TD, Dillon GP, Degrave WS, Berriman M, (2011) RATT: Rapid Annotation Transfer Tool. Nucleic Acids Res 39: e57.
23. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
24. Allen JE, Majoros WH, Pertea M, Salzberg SL, (2006) JIGSAW, GeneZilla, and GlimmerHMM: puzzling out the features of human genes in the ENCODE regions. Genome Biol 7 (Suppl 1): S9 1-13.
25. Rajkovic A, Davis RE, Simonsen JN, Rottman FM, (1990) A spliced leader is present on a subset of mRNAs from the human parasite Schistosoma mansoni. Proc Natl Acad Sci U S A 87: 8879-8883.
26. Ning Z, Cox AJ, Mullikin JC, (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11: 1725-1729.
27. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I, (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.
28. Robinson MD, Oshlack A, (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.
29. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
30. Alexa A, Rahnenfuhrer J, Lengauer T, (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607.
31. R Development Core Team. R: A language and environment for statistical computing (2011) R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org/. Accessed 2011 Dec 14.
32. Portela J, Grunau C, Cosseau C, Beltran S, Dantec C, et al. (2010) Whole-genome in-silico subtractive hybridization (WISH)-using massive sequencing for the identification of unique and repetitive sex-specific sequences: the example of Schistosoma mansoni. BMC Genomics 11: 387.
33. Huang X, Madan A, (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868-877.
34. Le TH, Humair PF, Blair D, Agatsuma T, Littlewood DT, et al. (2001) Mitochondrial gene content, arrangement and composition compared in African and Asian schistosomes. Mol Biochem Parasitol 117: 61-71.
35. Le TH, Blair D, McManus DP, (2000) Mitochondrial DNA sequences of human schistosomes: the current status. Int J Parasitol 30: 283-290.
36. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR, et al. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76: 12-24.
37. Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, et al. (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 20: 1451-1458.
38. Haas BJ, Berriman M, Hirai H, Cerqueira GG, Loverde PT, et al. (2007) Schistosoma mansoni genome: closing in on a final gene set. Exp Parasitol 117: 225-228.
39. Allen JE, Salzberg SL, (2005) JIGSAW: integration of multiple sources of evidence for gene prediction. Bioinformatics 21: 3596-3603.
40. DeMarco R, Kowaltowski AT, Machado AA, Soares MB, Gargioni C, et al. (2004) Saci-1,-2, and-3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni. J Virol 78: 2967-2978.
41. Davis RE, Hardwick C, Tavernier P, Hodgson S, Singh H, (1995) RNA trans-splicing in flatworms. Analysis of trans-spliced mRNAs and genes in the human parasite, Schistosoma mansoni. J Biol Chem 270: 21813-21819.
42. Sutton RE, Boothroyd JC, (1986) Evidence for trans splicing in trypanosomes. Cell 47: 527-535.
43. Spieth J, Brooke G, Kuersten S, Lea K, Blumenthal T, (1993) Operons in C. elegans: polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell 73: 521-532.
44. Douris V, Telford MJ, Averof M, (2010) Evidence for multiple independent origins of trans-splicing in Metazoa. Mol Biol Evol 27: 684-693.
45. Davis RE, Hodgson S, (1997) Gene linkage and steady state RNAs suggest trans-splicing may be associated with a polycistronic transcript in Schistosoma mansoni. Mol Biochem Parasitol 89: 25-39.
46. Ram D, Grossman Z, Markovics A, Avivi A, Ziv E, et al. (1989) Rapid changes in the expression of a gene encoding a calcium-binding protein in Schistosoma mansoni. Mol Biochem Parasitol 34: 167-175.
47. Ram D, Romano B, Schechter I, (1994) Immunochemical studies on the cercarial-specific calcium binding protein of Schistosoma mansoni. Parasitology 108 (Pt 3): 289-300.
48. Hedstrom R, Culpepper J, Harrison RA, Agabian N, Newport G, (1987) A major immunogen in Schistosoma mansoni infections is homologous to the heat-shock protein Hsp70. J Exp Med 165: 1430-1435.
49. Neumann S, Ziv E, Lantner F, Schechter I, (1992) Cloning and sequencing of an hsp70 gene of Schistosoma mansoni. Mol Biochem Parasitol 56: 357-360.
50. Neumann S, Ziv E, Lantner F, Schechter I, (1993) Regulation of HSP70 gene expression during the life cycle of the parasitic helminth Schistosoma mansoni. Eur J Biochem 212: 589-596.
51. Stein LD, David JR, (1986) Cloning of a developmentally regulated tegument antigen of Schistosoma mansoni. Mol Biochem Parasitol 20: 253-264.
52. Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, et al. (1992) Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol 22: 1483-1494.
53. Parker-Manuel SJ, Ivens AC, Dillon GP, Wilson RA, (2011) Gene Expression Patterns in Larval Schistosoma mansoni Associated with Infection of the Mammalian Host. PLoS Negl Trop Dis 5: e1274.
54. Fitzpatrick JM, Peak E, Perally S, Chalmers IW, Barrett J, et al. (2009) Anti-schistosomal intervention targets identified by lifecycle transcriptomic analyses. PLoS Negl Trop Dis 3: e543.
55. Coles GC, (1973) The metabolism of schistosomes: A review. International Journal of Biochemistry 4: 319-337.
56. Stirewalt MA, (1974) Schistosoma mansoni: cercaria to schistosomule. Adv Parasitol 12: 115-182.
57. Sayed AA, Cook SK, Williams DL, (2006) Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. J Biol Chem 281: 17001-17010.
58. Chain PS, Grafham DV, Fulton RS, Fitzgerald MG, Hostetler J, et al. (2009) Genomics. Genome project standards in a new era of sequencing. Science 326: 236-237.