Skip to main content
SpringerLink
Log in
Book cover

Biomphalaria Snails and Larval Trematodes pp 191–213Cite as

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

  • Chapter
  • First Online:

  • 823 Accesses

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.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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–S177

    Article  Google Scholar 

  • Bayne CJ (2009) Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165:8–18

    Article  PubMed  CAS  Google Scholar 

  • 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 31:874–878

    Article  PubMed  CAS  Google Scholar 

  • Bergquist R, Johansen MV, Utzinger J (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25:151–156

    Article  PubMed  Google Scholar 

  • 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 460:352–358

    Article  PubMed  CAS  Google Scholar 

  • 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 36:175–184

    Article  PubMed  CAS  Google Scholar 

  • 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 100:4102–4107

    Article  PubMed  CAS  Google Scholar 

  • 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 83:19–27

    Article  PubMed  CAS  Google Scholar 

  • Chitsulo L, Loverde P, Engels D (2004) Schistosomiasis. Nat Rev Microbiol 2:12–13

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 115:237–247

    Article  PubMed  CAS  Google Scholar 

  • Davids BJ, Yoshino TP (1998) Integrin-like RGD-dependent binding mechanism involved in the spreading response of circulating molluscan phagocytes. Dev Comp Immunol 22:39–53

    Article  PubMed  CAS  Google Scholar 

  • DeJong RJ, Emery AM, Adema CM (2004) The mitochondrial genome of Biomphalaria glabrata (Gastropoda: Basommatophora), intermediate host of Schistosoma mansoni. J Parasitol 90:991–997

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Goldman MA, Loverde PT, Chrisman L, Franklin DA (1984) Chromosomal evolution in planorbid snails of the genera Bulinus and Biomphalaria. Malacologia 25:427–446

    Google Scholar 

  • 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 137:321–328

    Article  PubMed  CAS  Google Scholar 

  • 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 147:207–210

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368:1106–1118

    Article  PubMed  Google Scholar 

  • 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 31:657–671

    Article  PubMed  CAS  Google Scholar 

  • 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 155:45–56

    Article  PubMed  CAS  Google Scholar 

  • 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 87:292–299

    PubMed  CAS  Google Scholar 

  • Hanelt B, Lun CM, Adema CM (2008) Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J Invertebr Pathol 99:192–203

    Article  PubMed  CAS  Google Scholar 

  • 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. 75–97

    Article  PubMed  CAS  Google Scholar 

  • 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 29:295–303

    Article  PubMed  CAS  Google Scholar 

  • Hubendick B (1958) A possible method of schistosome-vector control by competition between resistant and susceptible strains. Bull World Health Organ 18:113–116

    Google Scholar 

  • 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):27–39

    Article  PubMed  CAS  Google Scholar 

  • 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 123:203–211

    Article  PubMed  CAS  Google Scholar 

  • 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 30:855–866

    Article  PubMed  CAS  Google Scholar 

  • 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 8:2149–2151

    Article  PubMed  CAS  Google Scholar 

  • Jung Y, Nowak TS, Zhang SM, Hertel LA, Loker ES, Adema CM (2005) Manganese superoxide dismutase from Biomphalaria glabrata. J Invertebr Pathol 90:59–63

    Article  PubMed  CAS  Google Scholar 

  • 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 63:153–156

    Article  PubMed  CAS  Google Scholar 

  • 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 46:218–224

    Article  PubMed  CAS  Google Scholar 

  • 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 73:285–294

    Article  PubMed  CAS  Google Scholar 

  • 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 96:1510–1515

    Article  PubMed  CAS  Google Scholar 

  • 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 167:20–31

    Article  PubMed  CAS  Google Scholar 

  • 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:RC227

    PubMed  Google Scholar 

  • 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 269:155–165

    Article  PubMed  CAS  Google Scholar 

  • 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 89:98–101

    Article  PubMed  Google Scholar 

  • Lewis FA, Patterson CN, Knight M, Richards CS (2001) The relationship between Schistosoma mansoni and Biomphalaria glabrata: genetic and molecular approaches. Parasitology 123:S169–S179

    Article  PubMed  Google Scholar 

  • Lie KJ, Jeong KH, Heyneman D (1980) Tissue reactions induced by Schistosoma mansoni in Biomphalaria glabrata. Ann Trop Med Parasitol 74:157–166

    PubMed  CAS  Google Scholar 

  • 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 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • 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 120:399–407

    Article  PubMed  CAS  Google Scholar 

  • 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 107:97–104

    Article  PubMed  CAS  Google Scholar 

  • 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 9:634

    Article  PubMed  Google Scholar 

  • 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 151:18–27

    Article  PubMed  CAS  Google Scholar 

  • 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 68:84–94

    Article  PubMed  CAS  Google Scholar 

  • 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 62:149–154

    Article  PubMed  CAS  Google Scholar 

  • 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 89:258–265

    Article  PubMed  CAS  Google Scholar 

  • 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 31:687–696

    Article  PubMed  CAS  Google Scholar 

  • 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 29:393–407

    Article  PubMed  CAS  Google Scholar 

  • 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 94:659–668

    PubMed  CAS  Google Scholar 

  • Newton WL (1955) The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility to infection with Schistosoma mansoni. J Parasitol 41:526–528

    Article  PubMed  CAS  Google Scholar 

  • Niemann GM, Lewis FA (1990) Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Exp Parasitol 70:286–292

    Article  PubMed  CAS  Google Scholar 

  • 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 90:1034–1040

    Article  PubMed  CAS  Google Scholar 

  • 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 39:675–681

    Article  PubMed  CAS  Google Scholar 

  • 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 5:15–22

    PubMed  CAS  Google Scholar 

  • Raghavan N, Knight M (2006) The snail (Biomphalaria glabrata) genome project. Trends Parasitol 22:148–151

    Article  PubMed  CAS  Google Scholar 

  • 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 126:181–191

    Article  PubMed  CAS  Google Scholar 

  • 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 37:1307–1318

    Article  PubMed  CAS  Google Scholar 

  • Richards CS (1973) Susceptibility of adult Biomphalaria glabrata to Schistosoma mansoni infection. Am J Trop Med Hyg 22:748–756.

    Article  PubMed  CAS  Google Scholar 

  • Richards CS (1975a) Genetics of pigmentation in Biomphalaria straminea. Am J Trop Med Hyg 24:154–156

    PubMed  CAS  Google Scholar 

  • Richards CS (1975b) Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70:231–241

    Article  PubMed  CAS  Google Scholar 

  • Richards CS (1975c) Genetic studies on variation in infectivity of Schistosoma mansoni. J Parasitol 61:233–236

    Article  PubMed  CAS  Google Scholar 

  • Richards CS, Minchella DJ (1987) Transient non-susceptibility to Schistosoma mansoni associated with atrial amoebocytic accumulations in the snail host Biomphalaria glabrata. Parasitology 95:499–505

    Article  PubMed  Google Scholar 

  • Richards CS, Shade PC (1987) The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. J Parasitol 73:1146–1151

    Article  PubMed  CAS  Google Scholar 

  • 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 157:217–227

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 93:111–116

    Article  PubMed  Google Scholar 

  • Rollinson D, Webster JP, Webster B, Nyakaana S, Jorgensen A, Stothard JR (2009) Genetic diversity of schistosomes and snails: implications for control. Parasitology 27:1–11

    Google Scholar 

  • 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 101:1083–1089

    Article  PubMed  Google Scholar 

  • Schneider O, Zelck UE (2001) Differential display analysis of hemocytes from schistosome-resistant and schistosome-susceptible intermediate hosts. Parasitol Res 87:489–491

    Article  PubMed  CAS  Google Scholar 

  • 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 61:19–29

    Article  PubMed  CAS  Google Scholar 

  • 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 96:470–475

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JT, Spence JV (1994) Transfer of resistance to Schistosoma mansoni in Biomphalaria glabrata by allografts of amoebocyte-producing organ. J Parasitol 80:449–453

    Article  PubMed  CAS  Google Scholar 

  • 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 81:829–833

    Article  PubMed  CAS  Google Scholar 

  • 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 136:469–485

    Article  PubMed  CAS  Google Scholar 

  • 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 79:187–194

    Article  PubMed  CAS  Google Scholar 

  • 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 93:103–110

    Article  PubMed  Google Scholar 

  • 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):1475–1483

    Article  PubMed  Google Scholar 

  • 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 117:246–258

    Article  PubMed  CAS  Google Scholar 

  • 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 7:27

    Article  PubMed  Google Scholar 

  • 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 411:46–58

    Article  PubMed  CAS  Google Scholar 

  • 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 210–224

    Google Scholar 

  • 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 120:57–61

    Article  PubMed  CAS  Google Scholar 

  • Zelck UE, Von Janowsky B (2004) Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128:493–501

    Article  PubMed  CAS  Google Scholar 

  • 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 53:684–694

    Article  PubMed  CAS  Google Scholar 

  • 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 341:255–266

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 32:1119–1130

    Article  PubMed  CAS  Google Scholar 

  • 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 59:883–898

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Biomedical Research Institute, 20852, Rockville, MD, USA

    Matty Knight

Authors
  1. Wannaporn Ittiprasert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jocelyn Myers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edwin C. Odoemelam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nithya Raghavan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fred Lewis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joanna M. Bridger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Matty Knight
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matty Knight .

Editor information

Editors and Affiliations

  1. , Departamento de Biología Celular y Paras, Universidad de València, Av. Vicent Andrés Estellés s/n s/n, Burjassot, 46100, Valencia, Spain

    Rafael Toledo

  2. , Department of Biology, Lafayette College, Easton, 18042, Pennsylvania, USA

    Bernard Fried

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media LLC

About this chapter

Cite this chapter

Ittiprasert, W. et al. (2011). Advances in the Genomics and Proteomics of the Freshwater Intermediate Snail Host of Schistosoma mansoni, Biomphalaria glabrata . In: Toledo, R., Fried, B. (eds) Biomphalaria Snails and Larval Trematodes. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7028-2_8

Download citation

Publish with us

Policies and ethics

Search

Navigation