Recent advances in Schistosoma genomics

Parasite Immunology

Volumn 34, Issue 2-3, 2012, Pages 151-162

  Mourao M M ^a   Grunau, C ^b   Loverde, P T ^c   Jones, M K ^d   Oliveira, G ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSITÉ DE PERPIGNAN   (France)

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

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Disease; Epigenetics; Functional genomics; Genomics; Parasite; Schistosoma spp; Schistosomiasis

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 7; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE;

CHROMOSOME; DNA METHYLATION; EPIGENETICS; FUNCTIONAL GENOMICS; GENE MAPPING; GENE SEQUENCE; GENETIC LINKAGE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHISTOSOMA; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI;

ANIMALS; CHROMOSOME MAPPING; EPIGENOMICS; GENOME, HELMINTH; GENOMICS; HELMINTH PROTEINS; HUMANS; SCHISTOSOMA; SCHISTOSOMIASIS;

SCHISTOSOMA; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI;

EID: 84857019208     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2011.01349.x     Document Type: Review

References (113)

1. Oliveira G, Franco G & Verjovski-Almeida S. The Brazilian contribution to the study of the Schistosoma mansoni transcriptome. Acta Trop 2008; 108: 179-182.
2. Berriman M, Haas BJ, LoVerde PT, et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009; 460: 352-358.
3. The Schistosoma japonicum Genome and Functional Analysis Consortium. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009; 7253: 345-351.
4. Simpson AJ, Sher A & McCutchan TF. The genome of Schistosoma mansoni: isolation of DNA, its size, bases and repetitive sequences. Mol Biochem Parasitol 1982; 6: 125-137.
5. LoVerde PT, Hirai H, Merrick JM, Lee NH & El-Sayed N. Schistosoma mansoni genome project: an update. Parasitol Int 2004; 53: 183-192.
6. Hu W, Yan Q, Shen DK, et al. Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 2003; 35: 139-147.
7. Verjovski-Almeida S, DeMarco R, Martins EA, et al. Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nat Genet 2003; 35: 148-157.
8. Almeida GT, Amaral MS, Beckedorff FC, Kitajima JP, DeMarco R & Verjovski-Almeida S. Exploring the Schistosoma mansoni adult male transcriptome using RNA-seq. Exp Parasitol 2011; doi: (in press).
9. Piao X, Cai P, Liu S, et al. Global expression analysis revealed novel gender-specific gene expression features in the blood fluke parasite Schistosoma japonicum. PLoS ONE 2011; 6: e18267.
10. Portela J, Grunau C, Cosseau C, et al. 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 2010; 11: 387.
11. Franco GR, Valadão AF, Azevedo V & Rabelo EM. The Schistosoma gene discovery program: state of the art. Int J Parasitol 2000; 30: 453-463.
12. Fitzpatrick JM & Hoffmann KF. Dioecious Schistosoma mansoni express divergent gene repertoires regulated by pairing. Int J Parasitol 2006; 36: 1081-1089.
13. Waisberg M, Lobo FP, Cerqueira GC, et al. Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni. BMC Genomics 2007; 8: 181.
14. DeMarco R, Oliveira KC, Venancio TM & Verjovski-Almeida S. Gender biased differential alternative splicing patterns of the transcriptional cofactor CA150 gene in Schistosoma mansoni. Mol Biochem Parasitol 2006; 150: 123-131.
15. DeMarco R, Mathieson W, Manuel SJ, et al. Protein variation in blood-dwelling schistosome worms generated by differential splicing of micro-exon gene transcripts. Genome Res 2010; 20: 1112-1121.
16. Ojopi EP, Oliveira PS, Nunes DN, et al. A quantitative view of the transcriptome of Schistosoma mansoni adult-worms using SAGE. BMC Genomics 2007; 8: 186.
17. Williams DL, Sayed AA, Bernier J, et al. Profiling Schistosoma mansoni development using serial analysis of gene expression (SAGE). Exp Parasitol 2007; 117: 246-258.
18. Nawaratna SS, McManus DP, Moertel L, Gobert GN & Jones MK. Gene atlasing of digestive and reproductive tissues in Schistosoma mansoni. PLoS Negl Trop Dis 2011; 5: e1043.
19. Fitzpatrick JM, Peak E, Perally S, et al. Anti-schistosomal intervention targets identified by lifecycle transcriptomic analyses. PLoS Negl Trop Dis 2009; 3: e543.
20. Liu F, Lu J, Hu W, et al. New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2006; 2: e29.
21. Oliveira G. The Schistosoma mansoni transcriptome: an update. Exp Parasitol 2007; 117: 229-235.
22. Zerlotini A & Oliveira G. The contributions of the genome project to the study of schistosomiasis. Mem Inst Oswaldo Cruz 2010; 105: 367-369.
23. Zerlotini A, Heiges M, Wang H, et al. SchistoDB: a Schistosoma mansoni genome resource. Nucleic Acids Res 2009; 37: D579-D582.
24. Chen F, Mackey AJ, Stoeckert CJ Jr & Roos DS. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 2006; 34: D363-D368.
25. Karp PD, Paley S & Romero P. The pathway tools software. Bioinformatics 2002; 18(Suppl. 1): S225-S232.
26. Kanehisa M, Araki M, Goto S, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008; 36: D480-D484.
27. Criscione CD, Valentim CL, Hirai H, LoVerde PT & Anderson TJ. Genomic linkage map of the human blood fluke Schistosoma mansoni. Genome Biol 2009; 10: R71.
28. Gasser RB, Morahan G & Mitchell GF. Sexing single larval stages of Schistosoma mansoni by polymerase chain reaction. Mol Biochem Parasitol 1991; 47: 255-258.
29. Robb SMC, Ross E & Alvarado AS. SmedGD: The Schmidtea mediterranea genome database. Nucleic Acids Res 2008; 36: D599-D606.
30. Criscione CD, Poulin R & Blouin MS. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 2005; 14: 2247-2257.
31. Jablonka E & Lamb MJ. Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. Life and Mind: Philosophical Issues in Biology and Psychology. Cambridge, The MIT Press, 2006.
32. Waddington CH. Canalization of development and genetic assimilation of acquired characters. Nature 1959; 183: 1654-1655.
33. Cavalli G & Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 1998; 93: 505-518.
34. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400-5413.
35. Bollati V & Baccarelli A. Environmental epigenetics. Heredity 2010; 105: 105-112.
36. Jablonka E & Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 2009; 84: 131-176.
37. Barry JD & McCulloch R. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv Parasitol 2001; 49: 1-70.
38. Pays E. Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol 2005; 21: 517-520.
39. Taylor JE & Rudenko G. Switching trypanosome coats: what's in the wardrobe? Trends Genet 2006; 22: 614-620.
40. Grossman AI, Short RB & Cain GD. Karyotype evolution and sex chromosome differentiation in schistosomes (Trematoda, Schistosomatidae). Chromosoma 1981; 84: 413-430.
41. Craig JM & Bickmore WA. Chromosome bands - flavours to savour. Bioessays 1993; 15: 349-354.
42. Tanaka M, Hirai H, LoVerde PT, et al. Yeast artificial chromosome (YAC)-based genome mapping of Schistosoma mansoni. Mol Biochem Parasitol 1995; 69: 41-51.
43. Souza PP, Santos DN, Pena SD & Franco GR. Cloning and molecular characterization of the Schistosoma mansoni genes RbAp48 and histone H4. Mem Inst Oswaldo Cruz 2002; 97(Suppl. 1): 77-84.
44. Cosseau C, Azzi A, Smith K, Freitag M, Mitta G & Grunau C. Native chromatin immunoprecipitation (N-ChIP) and ChIP-Seq of Schistosoma mansoni: critical experimental parameters. Mol Biochem Parasitol 2009; 166: 70-76.
45. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129: 823-837.
46. Caby S & Pierce RJ. Quantitative chromatin immunoprecipitation (Q-ChIP) applied to Schistosoma mansoni. Mol Biochem Parasitol 2009; 166: 77-80.
47. Grzenda A, Lomberk G, Zhang JS & Urrutia R. Sin3: master scaffold and transcriptional corepressor. Biochim Biophys Acta 2009; 1789: 443-450.
48. Hayakawa T & Nakayama J. Physiological roles of class I HDAC complex and histone demethylase. J Biomed Biotechnol 2011; 2011: 129383.
49. Oger F, Dubois F, Caby S, et al. The class I histone deacetylases of the platyhelminth parasite Schistosoma mansoni. Biochem Biophys Res Commun 2008; 377: 1079-1084.
50. Verdin E, Dequiedt F & Kasler HG. Class II histone deacetylases: versatile regulators. Trends Genet 2003; 19: 286-293.
51. Roth SY, Denu JM & Allis CD. Histone acetyltransferases. Annu Rev Biochem 2001; 70: 81-120.
52. Bertin B, Oger F, Cornette J, et al. Schistosoma mansoni CBP/p300 has a conserved domain structure and interacts functionally with the nuclear receptor SmFtz-F1. Mol Biochem Parasitol 2006; 146: 180-191.
53. de Moraes MR, de Silva Dutra DL, Rumjanek FD, Juliano L, Juliano MA & Fantappie MR. Schistosoma mansoni histone acetyltransferase GCN5: linking histone acetylation to gene activation. Mol Biochem Parasitol 2004; 133: 131-135.
54. de Moraes MR, da Costa RF, de Oliveira FM, Rumjanek FD & Fantappie MR. Protein acetylation sites mediated by Schistosoma mansoni GCN5. Biochem Biophys Res Commun 2008; 370: 53-56.
55. Fantappie MR, Bastos de Oliveira FM, de Moraes MR, Rumjanek FD, Wu W & LoVerde PT. Cloning of SmNCoA-62, a novel nuclear receptor co-activator from Schistosoma mansoni: assembly of a complex with a SmRXR1/SmNR1 heterodimer, SmGCN5 and SmCBP1. Int J Parasitol 2008; 38: 1133-1147.
56. Bannister AJ & Kouzarides T. Reversing histone methylation. Nature 2005; 436: 1103-1106.
57. Balakrishnan L & Milavetz B. Decoding the histone H4 lysine 20 methylation mark. Crit Rev Biochem Mol Biol 2010; 45: 440-452.
58. Zeng W, Ball AR Jr & Yokomori K. HP1: heterochromatin binding proteins working the genome. Epigenetics 2010; 5: 287-292.
59. Pal-Bhadra M, Leibovitch BA, Gandhi SG, et al. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 2004; 303: 669-672.
60. Borst P & Sabatini R. Base J: discovery, biosynthesis, and possible functions. Annu Rev Microbiol 2008; 62: 235-251.
61. Fantappie MR, Gimba ER & Rumjanek FD. Lack of DNA methylation in Schistosoma mansoni. Exp Parasitol 2001; 98: 162-166.
62. Schaefer M & Lyko F. Solving the Dnmt2 enigma. Chromosoma 2010; 119: 35-40.
63. Geyer KK, Rodriguez Lopez CM, Chalmers IW, et al. Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni. Nat Commun 2011; 2: 424.
64. Hendrich B & Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998; 18: 6538-6547.
65. Bogdanovic O & Veenstra GJ. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 2009; 118: 549-565.
66. DeMarco R, Kowaltowski AT, Machado AA, et al. Saci-1, -2, and -3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni. J Virol 2004; 78: 2967-2978.
67. Fitzpatrick JM, Protasio AV, McArdle AJ, Williams GA, Johnston DA & Hoffmann KF. Use of genomic DNA as an indirect reference for identifying gender-associated transcripts in morphologically identical, but chromosomally distinct, Schistosoma mansoni cercariae. PLoS Negl Trop Dis 2008; 2: e323.
68. Fukagawa T, Nogami M, Yoshikawa M, et al. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 2004; 6: 784-791.
69. Grewal SI. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 2010; 20: 134-141.
70. Kanellopoulou C, Muljo SA, Kung AL, et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 2005; 19: 489-501.
71. Batista TM & Marques JT. RNAi pathways in parasitic protists and worms. J Proteomics 2011; 74: 1504-1514.
72. Gomes MS, Cabral FJ, Jannotti-Passos LK, et al. Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int 2009; 58: 61-68.
73. Krautz-Peterson G & Skelly PJ. Schistosoma mansoni: the dicer gene and its expression. Exp Parasitol 2008; 118: 122-128.
74. 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.
75. Verdel A, Vavasseur A, Le GM & Touat-Todeschini L. Common themes in siRNA-mediated epigenetic silencing pathways. Int J Dev Biol 2009; 53: 245-257.
76. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI & Martienssen RA. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 2002; 297: 1833-1837.
77. Verdel A, Jia S, Gerber S, et al. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 2004; 303: 672-676.
78. Azzi A, Cosseau C & Grunau C. Schistosoma mansoni: developmental arrest of miracidia treated with histone deacetylase inhibitors. Exp Parasitol 2009; 121: 288-291.
79. Cousseau C, Azzi A, Rognon A, et al. Epigenetic and phenotypic variability in populations of Schistosoma mansoni-a possible kick-off for adaptive host/parasite evolution. Oikos 2010; 119: 669-978.
80. Dubois F, Caby S, Oger F, et al. Histone deacetylase inhibitors induce apoptosis, histone hyperacetylation and up-regulation of gene transcription in Schistosoma mansoni. Mol Biochem Parasitol 2009; 168: 7-15.
81. Roger E, Grunau C, Pierce RJ, et al. Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Negl Trop Dis 2008; 2: e330.
82. Hoffmann KF & Strand M. Molecular characterization of a 20.8-kDa Schistosoma mansoni antigen. Sequence similarity to tegumental associated antigens and dynein light chains. J Biol Chem 1997; 272: 14509-14515.
83. Fitzsimmons CM, McBeath R, Joseph S, et al. Factors affecting human IgE and IgG responses to allergen-like Schistosoma mansoni antigens: molecular structure and patterns of in vivo exposure. Int Arch Allergy Immunol 2007; 142: 40-50.
84. Fitzsimmons CM & Dunne DW. Survival of the fittest: allergology or parasitology? Trends Parasitol 2009; 25: 447-451.
85. Braschi S & Wilson RA. Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 2006; 5: 347-356.
86. Cardoso FC, Pacifico RN, Mortara RA & Oliveira SC. Human antibody responses of patients living in endemic areas for schistosomiasis to the tegumental protein Sm29 identified through genomic studies. Clin Exp Immunol 2006; 144: 382-391.
87. Cardoso FC, Macedo GC, Gava E, et al. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2008; 2: e308.
88. Jones MK. Structure and diversity of cestode epithelia. Int J Parasitol 1998; 28: 913-923.
89. Jones MK, Gobert GN, Zhang L, Sunderland P & McManus DP. The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions. Bioessays 2004; 26: 752-765.
90. Yoshino TP, Dinguirard N & Mourão MM. In vitro manipulation of gene expression in larval Schistosoma: a model for postgenomic approaches in Trematoda. Parasitology 2010; 137: 463-483.
91. Beckmann S, Wippersteg V, El-Bahay A, Hirzmann J, Oliveira G & Grevelding CG. Schistosoma mansoni: germ-line transformation approaches and actin-promoter analysis. Exp Parasitol 2007; 117: 292-303.
92. Dvorák J, Beckmann S, Lim KC, et al. Biolistic transformation of Schistosoma mansoni: studies with modified reporter-gene constructs containing regulatory regions of protease genes. Mol Biochem Parasitol 2010; 170: 37-40.
93. Mann VH, Morales ME, Kines KJ & Brindley PJ. Transgenesis of schistosomes: approaches employing mobile genetic elements. Parasitology 2008; 135: 141-153.
94. Yang S, Brindley PJ, Zeng Q, et al. Transduction of Schistosoma japonicum schistosomules with vesicular stomatitis virus glycoprotein pseudotyped murine leukemia retrovirus and expression of reporter human telomerase reverse transcriptase in the transgenic schistosomes. Mol Biochem Parasitol 2010; 174: 109-116.
95. Krautz-Peterson G, Bhardwaj R, Faghiri Z, Tararam CA & Skelly PJ. RNA interference in schistosomes: machinery and methodology. Parasitology 2010; 137: 485-495.
96. Mourão MM, Dinguirard N, Franco GR & Yoshino TP. Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference. PLoS Negl Trop Dis 2009; 3: e502.
97. Štefanic S, Dvorák J, Horn M, et al. RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Negl Trop Dis 2010; 4: e850.
98. Ayuk MA, Suttiprapa S, Rinaldi G, Mann VH, Lee CM & Brindley PJ. Schistosoma mansoni U6 gene promoter-driven short hairpin RNA induces RNA interference in human fibrosarcoma cells and schistosomules. Int J Parasitol 2011; 41: 783-789.
99. Mourão MM, Dinguirard N, Franco GR & Yoshino TP. Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress. PLoS Negl Trop Dis 2009; 3: e550.
100. Kuntz AN, Vioud-Charvet E, Sayed AA, et al. Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Med 2007; 4: e206.
101. Fitzpatrick JM, Johansen MV, Johnston DA, Dunne DW & Hoffmann KF. Gender-associated gene expression in two related strains of Schistosoma japonicum. Mol Biochem Parasitol 2004; 136: 191-209.
102. Fitzpatrick JM, Johnston DA, Williams GW, et al. An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Mol Biochem Parasitol 2005; 141: 1-13.
103. Gobert GN, Moertel L, Brindley PJ & McManus DP. Developmental gene expression profiles of the human pathogen Schistosoma japonicum. BMC Genomics 2009; 10: 128.
104. Gobert GN, Tran MH, Moertel L, et al. Transcriptional changes in Schistosoma mansoni during early schistosomula development and in the presence of erythrocytes. PLoS Negl Trop Dis 2010; 4: e600.
105. Gobert GN, McManus DP, Nawaratna S, Moertel L, Mulvenna J & Jones MK. Tissue specific profiling of females of Schistosoma japonicum by integrated laser microdissection microscopy and microarray analysis. PLoS Negl Trop Dis 2009; 3: e469.
106. Hokke CH, Fitzpatrick JM & Hoffmann KF. Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends Parasitol 2007; 23: 165-174.
107. Mulvenna J, Moertel L, Jones MK, et al. Exposed proteins of the Schistosoma japonicum tegument. Int J Parasitol 2010; 40: 543-554.
108. Cass CL, Johnson JR, Califf LL, et al. Proteomic analysis of Schistosoma mansoni egg secretions. Mol Biochem Parasitol 2007; 155: 84-93.
109. Mathieson W & Wilson RA. A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. Int J Parasitol 2010; 40: 617-628.
110. Tran MH, Freitas TC, Cooper L, et al. Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog 2010; 6: e1000840.
111. Castro-Borges W, Dowle A, Curwen RS, Thomas-Oates J & Wilson RA. Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Negl Trop Dis 2011; 5: e993.
112. Petschnigg J, Snider J & Stagljar I. Interactive proteomics research technologies: recent applications and advances. Curr Opin Biotechnol 2011; 22: 50-58.
113. Colley DG & Secor WE. A schistosomiasis research agenda. PLoS Negl Trop Dis 2007; 1: e32.