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Advances in the Genomics and Proteomics of the Freshwater Intermediate Snail Host of Schistosoma mansoni, Biomphalaria glabrata

  • Wannaporn Ittiprasert
  • Jocelyn Myers
  • Edwin C. Odoemelam
  • Nithya Raghavan
  • Fred Lewis
  • Joanna M. Bridger
  • Matty Knight
Chapter

Abstract

Molecular events governing the interplay between the intermediate snail host, Biomphalaria glabrata, and its parasitic trematodes are gradually being unraveled. The last 20 years has seen an upsurge in the number of gene sequences and proteins that are expressed, differentially regulated, and diversified in this snail in relation to its role as an obligate host for an important human pathogen, Schistosoma mansoni, the causative agent of schistosomiasis in the Western Hemisphere. Although regarded as a good model organism for studying the complexities of host–pathogen interactions, B. glabrata also serves as being useful in bridging the information gap that exists between locotrophozoans and the more popular model organisms that belong to other clades (ecdyzoa and deuterostomes). By the application of a variety of molecular tools, emerging results show the significance of innate defense and stress-related genes in the snail host/parasite relationship. In this chapter, we will provide an overview of some of the recent advances that have been made in the field of genomics and proteomics of this snail, mainly in relation to schistosomes. Although information remains for the most part rudimentary, significant advances have been made in the molecular characterization of certain genes, such as FREPs and the nimbus mobile genetic element. Key enzymes participating in the snail’s ability to either support or reject the parasite infection, such as hydrolases and oxidoreductases, have also been characterized. A significant milestone, the completion of the 931-Mb genome sequence of this snail, is also anticipated soon. Collectively, all these advances, unless interest and/or funding opportunities wane, should create a favorable research environment for attracting more investigators into the field of molecular malacology.

Keywords

Bacterial Artificial Chromosome Bacterial Artificial Chromosome Clone Bacterial Artificial Chromosome Library Cytidine Deaminase Snail Host 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We wish to thank Andre Miller for his helpful suggestions with the writing of this manuscript. We also thank Pat Caspar for helping us with the irradiation experiments, and Frances Barnes for her technical support. This work was supported by NIH-NIAID grant no. R01-AI63480.

References

  1. Adema CM, Luo MZ, Hanelt B, Hertel LA, Marshall JJ, Zhang SM, DeJong RJ, Kim HR, Kudrna D, Wing RA, Soderlund C, Knight M, Lewis FA, Caldeira RL, Jannotti-Passos LK, Carvalho Odos S, Loker ES (2006) A bacterial artificial chromosome library for Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni. Mem Inst Oswaldo Cruz 101:S167–S177CrossRefGoogle Scholar
  2. Bayne CJ (2009) Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165:8–18PubMedCrossRefGoogle Scholar
  3. Bender RC, Goodall CP, Blouin MS, Bayne CJ (2007) Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosoma mansoni. Dev Comp Immunol 31:874–878PubMedCrossRefGoogle Scholar
  4. Bergquist R, Johansen MV, Utzinger J (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25:151–156PubMedCrossRefGoogle Scholar
  5. Berriman M, Haas BJ, Loverde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, Demarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D, Macedo CD, Mcveigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–358PubMedCrossRefGoogle Scholar
  6. Bouchut A, Roger E, Coustau C, Gourbal B, Mitta G (2006) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 36:175–184PubMedCrossRefGoogle Scholar
  7. Bransteitter R, Pham P, Scharff MD, Goodman MF (2003) Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc Natl Acad Sci USA 100:4102–4107PubMedCrossRefGoogle Scholar
  8. Campos YR, Carvalho OS, Goveia CO, Romanha AJ (2002) Genetic variability of the main intermediate host of the Schistosoma mansoni in Brazil, Biomphalaria glabrata (Gastropoda: Planorbidae) assessed by SSR-PCR. Acta Trop 83:19–27PubMedCrossRefGoogle Scholar
  9. Chitsulo L, Loverde P, Engels D (2004) Schistosomiasis. Nat Rev Microbiol 2:12–13PubMedCrossRefGoogle Scholar
  10. Cooper LA, Richards CS, Lewis FA, Minchella DJ (1994) Schistosoma mansoni: relationship between low fecundity and reduced susceptibility to parasite infection in the snail Biomphalaria glabrata. Exp Parasitol 79:21–28.PubMedCrossRefGoogle Scholar
  11. Darani HY, Curtis RH, McNeice C, Price HP, Sayers JR, Doenhoff MJ (1997) Schistosoma mansoni: anomalous immunogenic properties of a 27 kDa larval serine protease associated with protective immunity. Parasitology 115:237–247PubMedCrossRefGoogle Scholar
  12. Davids BJ, Yoshino TP (1998) Integrin-like RGD-dependent binding mechanism involved in the spreading response of circulating molluscan phagocytes. Dev Comp Immunol 22:39–53PubMedCrossRefGoogle Scholar
  13. DeJong RJ, Emery AM, Adema CM (2004) The mitochondrial genome of Biomphalaria glabrata (Gastropoda: Basommatophora), intermediate host of Schistosoma mansoni. J Parasitol 90:991–997PubMedCrossRefGoogle Scholar
  14. Duclermortier P, Lardans V, Serra E, Trottein F, Dissous C (1999) Biomphalaria glabrata embryonic cells express a protein with a domain homologous to the lectin domain of mammalian selectins. Parasitol Res 85:481–486.PubMedCrossRefGoogle Scholar
  15. Goldman MA, Loverde PT, Chrisman L, Franklin DA (1984) Chromosomal evolution in planorbid snails of the genera Bulinus and Biomphalaria. Malacologia 25:427–446Google Scholar
  16. Goodall CP, Bender RC, Broderick EJ, Bayne CJ (2004) Constitutive differences in Cu/Zn superoxide dismutase mRNA levels and activity in hemocytes of Biomphalaria glabrata (Mollusca) that are either susceptible or resistant to Schistosoma mansoni (Trematoda). Mol Biochem Parasitol 137:321–328PubMedCrossRefGoogle Scholar
  17. Goodall CP, Bender RC, Brooks JK, Bayne CJ (2006) Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Mol Biochem Parasitol 147:207–210PubMedCrossRefGoogle Scholar
  18. Gregory TR (2003) Genome size estimates for two important freshwater molluscs, the zebra mussel (Dreissena polymorpha) and the schistosomiasis vector snail (Biomphalaria glabrata). Genome 46:841–844.PubMedCrossRefGoogle Scholar
  19. Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368:1106–1118PubMedCrossRefGoogle Scholar
  20. Guillou F, Mitta G, Galinier R, Coustau C (2007a) Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 31:657–671PubMedCrossRefGoogle Scholar
  21. Guillou F, Roger E, Mone Y, Rognon A, Grunau C, Theron A, Mitta G, Coustau C, Gourbal BE (2007b) Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol 155:45–56PubMedCrossRefGoogle Scholar
  22. Hahn UK, Bender RC, Bayne CJ (2001) Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87:292–299PubMedGoogle Scholar
  23. Hanelt B, Lun CM, Adema CM (2008) Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J Invertebr Pathol 99:192–203PubMedCrossRefGoogle Scholar
  24. Hansen EL (1976) A cell line from embryos of Biomphalaria glabrata(Pulmonata): Establishment and characteristics. In: Maramorosch K (ed.) In Invertebrate Tissue Culture: Research Applications. New York: Academic Press; pp. 75–97PubMedCrossRefGoogle Scholar
  25. Hertel LA, Adema CM, Loker ES (2005) Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 29:295–303PubMedCrossRefGoogle Scholar
  26. Hubendick B (1958) A possible method of schistosome-vector control by competition between resistant and susceptible strains. Bull World Health Organ 18:113–116Google Scholar
  27. Ittiprasert W, Miller A, Myers J, Nene V, El-Sayed NM, Knight M (2010) Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Mol Biochem Parasitol 169(1):27–39PubMedCrossRefGoogle Scholar
  28. Ittiprasert W, Nene R, Miller A, Raghavan N, Lewis F, Hodgson J, Knight M (2009) Schistosoma mansoni infection of juvenile Biomphalaria glabrata induces a differential stress response between resistant and susceptible snails. Exp Parasitol 123:203–211PubMedCrossRefGoogle Scholar
  29. Jiang Y, Loker ES, Zhang SM (2006) In vivo and in vitro knockdown of FREP2 gene expression in the snail Biomphalaria glabrata using RNA interference. Dev Comp Immunol 30:855–866PubMedCrossRefGoogle Scholar
  30. Jones CS, Lockyer AE, Rollinson D, Piertney SB, Noble LR (1999) Isolation and characterization of microsatellite loci in the freshwater gastropod, Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Mol Ecol 8:2149–2151PubMedCrossRefGoogle Scholar
  31. Jung Y, Nowak TS, Zhang SM, Hertel LA, Loker ES, Adema CM (2005) Manganese superoxide dismutase from Biomphalaria glabrata. J Invertebr Pathol 90:59–63PubMedCrossRefGoogle Scholar
  32. Kane RA, Rollinson D (1994) Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Mol Biochem Parasitol 63:153–156PubMedCrossRefGoogle Scholar
  33. Kassim OO, Richards CS (1978) Biomphalaria glabrata: lysozyme activities in the hemolymph, digestive gland, and headfoot of the intermediate host of Schistosoma mansoni. Exp Parasitol 46:218–224PubMedCrossRefGoogle Scholar
  34. Knight M, Brindley PJ, Richards CS, Lewis FA (1991) Schistosoma mansoni: use of a cloned ribosomal RNA gene probe to detect restriction fragment length polymorphisms in the intermediate host Biomphalaria glabrata. Exp Parasitol 73:285–294PubMedCrossRefGoogle Scholar
  35. Knight M, Miller AN, Patterson CN, Rowe CG, Michaels G, Carr D, Richards CS, Lewis FA (1999) The identification of markers segregating with resistance to Schistosoma mansoni infection in the snail Biomphalaria glabrata. Proc Natl Acad Sci USA 96:1510–1515PubMedCrossRefGoogle Scholar
  36. Knight M, Raghavan N, Goodall C, Cousin C, Ittiprasert W, Sayed A, Miller A, Williams DL, Bayne CJ (2009) Biomphalaria glabrata peroxiredoxin: effect of Schistosoma mansoni infection on differential gene regulation. Mol Biochem Parasitol 167:20–31PubMedCrossRefGoogle Scholar
  37. Korneev SA, Kemenes I, Straub V, Staras K, Korneeva EI, Kemenes G, Benjamin PR, O’Shea M (2002) Suppression of nitric oxide (NO)-dependent behavior by double-stranded RNA-mediated silencing of a neuronal NO synthase gene. J Neurosci 22:RC227PubMedGoogle Scholar
  38. Leonard PM, Adema CM, Zhang SM, Loker ES (2001) Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene 269:155–165PubMedCrossRefGoogle Scholar
  39. Lewis FA, Patterson CN, Grzywacz C (2003) Parasite-susceptibility phenotypes of F1 Biomphalaria glabrata progeny derived from interbreeding Schistosoma mansoni-resistant and -susceptible snails. Parasitol Res 89:98–101PubMedCrossRefGoogle Scholar
  40. Lewis FA, Patterson CN, Knight M, Richards CS (2001) The relationship between Schistosoma mansoni and Biomphalaria glabrata: genetic and molecular approaches. Parasitology 123:S169–S179PubMedCrossRefGoogle Scholar
  41. Lie KJ, Jeong KH, Heyneman D (1980) Tissue reactions induced by Schistosoma mansoni in Biomphalaria glabrata. Ann Trop Med Parasitol 74:157–166PubMedGoogle Scholar
  42. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  43. Lockyer AE, Jones CS, Noble LR, Rollinson D (2000) Use of differential display to detect changes in gene expression in the intermediate snail host Biomphalaria glabrata upon infection with Schistosoma mansoni. Parasitology 120:399–407PubMedCrossRefGoogle Scholar
  44. Lockyer AE, Noble LR, Rollinson D, Jones CS (2004) Schistosoma mansoni: resistant specific infection-induced gene expression in Biomphalaria glabrata identified by fluorescent-based differential display. Exp Parasitol 107:97–104PubMedCrossRefGoogle Scholar
  45. Lockyer AE, Spinks J, Kane RA, Hoffmann KF, Fitzpatrick JM, Rollinson D, Noble LR, Jones CS (2008) Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 9:634PubMedCrossRefGoogle Scholar
  46. Lockyer AE, Spinks J, Noble LR, Rollinson D, Jones CS (2007) Identification of genes involved in interactions between Biomphalaria glabrata and Schistosoma mansoni by suppression subtractive hybridization. Mol Biochem Parasitol 151:18–27PubMedCrossRefGoogle Scholar
  47. Loker ES, Bayne CJ, Buckley PM, Kruse KT (1982) Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by hemocytes of juveniles of the 10-R2 strain of Biomphalaria glabrata. J Parasitol 68:84–94PubMedCrossRefGoogle Scholar
  48. Loker ES, Bayne CJ, Yui MA (1986) Echinostoma paraensei: hemocytes of Biomphalaria glabrata as targets of echinostome mediated interference with host snail resistance to Schistosoma mansoni. Exp Parasitol 62:149–154PubMedCrossRefGoogle Scholar
  49. Mavarez J, Pointier JP, David P, Delay B, Jarne P (2002) Genetic differentiation, dispersal and mating system in the schistosome-transmitting freshwater snail Biomphalaria glabrata. Heredity 89:258–265PubMedCrossRefGoogle Scholar
  50. Miller AN, Raghavan N, Fitzgerald PC, Lewis FA, Knight M (2001) Differential gene expression in haemocytes of the snail Biomphalaria glabrata: effects of Schistosoma mansoni infection. Int J Parasitol 31:687–696PubMedCrossRefGoogle Scholar
  51. Mitta G, Galinier R, Tisseyre P, Allienne JF, Girerd-Chambaz Y, Guillou F, Bouchut A, Coustau C (2005) Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev Comp Immunol 29:393–407PubMedCrossRefGoogle Scholar
  52. Myers J, Ittiprasert W, Raghavan N, Miller A, Knight M (2008) Differences in cysteine protease activity in Schistosoma mansoni-resistant and -susceptible Biomphalaria glabrata and characterization of the hepatopancreas cathepsin B Full-length cDNA. J Parasitol 94:659–668PubMedGoogle Scholar
  53. Newton WL (1955) The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility to infection with Schistosoma mansoni. J Parasitol 41:526–528PubMedCrossRefGoogle Scholar
  54. Niemann GM, Lewis FA (1990) Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Exp Parasitol 70:286–292PubMedCrossRefGoogle Scholar
  55. Nowak TS, Woodards AC, Jung Y, Adema CM, Loker ES (2004) Identification of transcripts generated during the response of resistant Biomphalaria glabrata to Schistosoma mansoni infection using suppression subtractive hybridization. J Parasitol 90:1034–1040PubMedCrossRefGoogle Scholar
  56. Odoemelam E, Raghavan N, Miller A, Bridger JM, Knight M (2009) Revised karyotyping and gene mapping of the Biomphalaria glabrata embryonic (Bge) cell line. Int J Parasitol 39:675–681PubMedCrossRefGoogle Scholar
  57. Paraense W, Correa L (1963) Variations in susceptibility of populations of Australorbis glabratus to a strain of Schistosoma mansoni. Rev Inst Med Trop Sao Paulo 5:15–22PubMedGoogle Scholar
  58. Raghavan N, Knight M (2006) The snail (Biomphalaria glabrata) genome project. Trends Parasitol 22:148–151PubMedCrossRefGoogle Scholar
  59. Raghavan N, Miller AN, Gardner M, Fitzgerald PC, Kerlavage AR, Johnston DA, Lewis FA, Knight M (2003) Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol Biochem Parasitol 126:181–191PubMedCrossRefGoogle Scholar
  60. Raghavan N, Tettelin H, Miller A, Hostetler J, Tallon L, Knight M (2007) Nimbus (BgI): an active non-LTR retrotransposon of the Schistosoma mansoni snail host Biomphalaria glabrata. Int J Parasitol 37:1307–1318PubMedCrossRefGoogle Scholar
  61. Richards CS (1973) Susceptibility of adult Biomphalaria glabrata to Schistosoma mansoni infection. Am J Trop Med Hyg 22:748–756.PubMedCrossRefGoogle Scholar
  62. Richards CS (1975a) Genetics of pigmentation in Biomphalaria straminea. Am J Trop Med Hyg 24:154–156PubMedGoogle Scholar
  63. Richards CS (1975b) Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70:231–241PubMedCrossRefGoogle Scholar
  64. Richards CS (1975c) Genetic studies on variation in infectivity of Schistosoma mansoni. J Parasitol 61:233–236PubMedCrossRefGoogle Scholar
  65. Richards CS, Minchella DJ (1987) Transient non-susceptibility to Schistosoma mansoni associated with atrial amoebocytic accumulations in the snail host Biomphalaria glabrata. Parasitology 95:499–505PubMedCrossRefGoogle Scholar
  66. Richards CS, Shade PC (1987) The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. J Parasitol 73:1146–1151PubMedCrossRefGoogle Scholar
  67. Roger E, Gourbal B, Grunau C, Pierce RJ, Galinier R, Mitta G (2008) Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Mol Biochem Parasitol 157:217–227PubMedCrossRefGoogle Scholar
  68. Roger E, Grunau C, Pierce RJ, Hirai H, Gourbal B, Galinier R, Emans R, Cesari IM, Cosseau C, Mitta G (2008a) Controlled Chaos of Polymorphic Mucins in a Metazoan Parasite (Schistosoma mansoni) Interacting with Its Invertebrate Host (Biomphalaria glabrata). PLoS Negl Trop Dis 2:e330.PubMedCrossRefGoogle Scholar
  69. Roger E, Mitta G, Mone Y, Bouchut A, Rognon A, Grunau C, Boissier J, Theron A, Gourbal BE (2008b) Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/Schistosoma mansoni model: new candidates identified by a global comparative proteomics approach. Mol Biochem Parasitol 157:205–216.PubMedCrossRefGoogle Scholar
  70. Rollinson D, Stothard JR, Jones CS, Lockyer AE, De Souza CP, Noble LR (1998) Molecular characterisation of intermediate snail hosts and the search for resistance genes. Mem Inst Oswaldo Cruz 93:111–116PubMedCrossRefGoogle Scholar
  71. Rollinson D, Webster JP, Webster B, Nyakaana S, Jorgensen A, Stothard JR (2009) Genetic diversity of schistosomes and snails: implications for control. Parasitology 27:1–11Google Scholar
  72. Sandland GJ, Foster AV, Zavodna M, Minchella DJ (2007) Interplay between host genetic variation and parasite transmission in the Biomphalaria glabrata-Schistosoma mansoni system. Parasitol Res 101:1083–1089PubMedCrossRefGoogle Scholar
  73. Schneider O, Zelck UE (2001) Differential display analysis of hemocytes from schistosome-resistant and schistosome-susceptible intermediate hosts. Parasitol Res 87:489–491PubMedCrossRefGoogle Scholar
  74. Stothard JR, Hughes S, Rollinson D (1996) Variation within the internal transcribed spacer (ITS) of ribosomal DNA genes of intermediate snail hosts within the genus Bulinus (Gastropoda: Planorbidae). Acta Trop 61:19–29PubMedCrossRefGoogle Scholar
  75. Stothard JR, Mgeni AF, Khamis S, Seto E, Ramsan M, Hubbard SJ, Kristensen TK, Rollinson D (2002) New insights into the transmission biology of urinary schistosomiasis in Zanzibar. Trans R Soc Trop Med Hyg 96:470–475PubMedCrossRefGoogle Scholar
  76. Sullivan JT, Spence JV (1994) Transfer of resistance to Schistosoma mansoni in Biomphalaria glabrata by allografts of amoebocyte-producing organ. J Parasitol 80:449–453PubMedCrossRefGoogle Scholar
  77. Sullivan JT, Spence JV, Nunez JK (1995) Killing of Schistosoma mansoni sporocysts in Biomphalaria glabrata implanted with amoebocyte-producing organ allografts from resistant snails. J Parasitol 81:829–833PubMedCrossRefGoogle Scholar
  78. Taft AS, Vermeire JJ, Bernier J, Birkeland SR, Cipriano MJ, Papa AR, McArthur AG, Yoshino TP (2009) Transcriptome analysis of Schistosoma mansoni larval development using serial analysis of gene expression (SAGE). Parasitology 136:469–485PubMedCrossRefGoogle Scholar
  79. Vidigal TH, Dias Neto E, Carvalho Odos S, Simpson AJ (1994) Biomphalaria glabrata: extensive genetic variation in Brazilian isolates revealed by random amplified polymorphic DNA analysis. Exp Parasitol 79:187–194PubMedCrossRefGoogle Scholar
  80. Vidigal TH, Dias Neto E, Spatz L, Nunes DN, Pires ER, Simpson AJ, Carvalho OS (1998) Genetic variability and identification of the intermediate snail hosts of Schistosoma mansoni. Mem Inst Oswaldo Cruz 93:103–110PubMedCrossRefGoogle Scholar
  81. Wang LD, Guo JG, Wu XH, Chen HG, Wang TP, Zhu SP, Zhang ZH, Steinmann P, Yang GJ, Wang SP, Wu ZD, Wang LY, Hao Y, Bergquist R, Utzinger J, Zhou XN (2009) China’s new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop Med Int Health 14(12):1475–1483PubMedCrossRefGoogle Scholar
  82. Williams DL, Sayed AA, Bernier J, Birkeland SR, Cipriano MJ, Papa AR, Mcarthur AG, Taft A, Vermeire JJ, Yoshino TP (2007) Profiling Schistosoma mansoni development using serial analysis of gene expression (SAGE). Exp Parasitol 117:246–258PubMedCrossRefGoogle Scholar
  83. Wu W, Niles EG, Hirai HA, LoVerde PT (2007) Evolution of a novel subfamily of nuclear receptors with members that each contain two DNA binding domains. BMC Evol Biol 7:27PubMedCrossRefGoogle Scholar
  84. Yoshino TP, Dinguirard N, Kunert J, Hokke CH (2008) Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411:46–58PubMedCrossRefGoogle Scholar
  85. Yoshino TP, Vermeire JJ, Humphreys JE (2006) Signal transduction at the host-parasite interface. In: Maule AG, Mark NJ (eds) Parasitic flatworms molecular biology, biochemistry, immunology and physiology. CAB International, Belfast, pp 210–224Google Scholar
  86. Zavodna M, Sandland GJ, Minchella DJ (2008) Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni. Exp Parasitol 120:57–61PubMedCrossRefGoogle Scholar
  87. Zelck UE, Von Janowsky B (2004) Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128:493–501PubMedCrossRefGoogle Scholar
  88. Zhang SM, Leonard PM, Adema CM, Loker ES (2001) Parasite-responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 53:684–694PubMedCrossRefGoogle Scholar
  89. Zhang SM, Loker ES (2004) Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 341:255–266PubMedCrossRefGoogle Scholar
  90. Zhang SM, Nian H, Wang B, Loker ES, Adema CM (2009) Schistosomin from the snail Biomphalaria glabrata: expression studies suggest no involvement in trematode-mediated castration. Mol Biochem Parasitol 165(1):79–86.PubMedCrossRefGoogle Scholar
  91. Zhang SM, Nian H, Zeng Y, DeJong RJ (2008) Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev Comp Immunol 32:1119–1130PubMedCrossRefGoogle Scholar
  92. Zhang SM, Zeng Y, Loker ES (2007) Characterization of immune genes from the schistosome host snail Biomphalaria glabrata that encode peptidoglycan recognition proteins and gram-negative bacteria binding protein. Immunogenetics 59:883–898PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2011

Authors and Affiliations

  • Wannaporn Ittiprasert
  • Jocelyn Myers
  • Edwin C. Odoemelam
  • Nithya Raghavan
  • Fred Lewis
  • Joanna M. Bridger
  • Matty Knight
    • 1
  1. 1.Biomedical Research InstituteRockvilleUSA

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