A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection

PLoS Neglected Tropical Diseases

Volumn 6, Issue 3, 2012, Pages

  Hanington, Patrick C ^a   Forys, Michelle A ^b   Loker, Eric S ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN RELATED PROTEIN 3; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; FIBRINOGEN RELATED PROTEIN 3, BIOMPHALARIA GLABRATA; FIBRINOGEN-RELATED PROTEIN 3, BIOMPHALARIA GLABRATA; IMMUNOGLOBULIN; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMPHALARIA GLABRATA; CONTROLLED STUDY; DEFENSE MECHANISM; ECHINOSTOMA; GENE EXPRESSION; HISTOLOGY; HOST RESISTANCE; INFECTION RESISTANCE; KNOCKOUT GENE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIABILITY; RADIATION ATTENUATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; WESTERN BLOTTING; ANIMAL; BIOMPHALARIA; GENE EXPRESSION PROFILING; GENE SILENCING; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOGENICITY;

ANIMALS; BIOMPHALARIA; ECHINOSTOMA; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; IMMUNOGLOBULINS; MICROARRAY ANALYSIS; RNA, SMALL INTERFERING; SCHISTOSOMA MANSONI;

EID: 84859173420     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001591     Document Type: Article

References (35)

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 6: 411-425.
2. Ward RD, Lewis FA, Yoshino TP, Dunn TS, (1988) Schistosoma mansoni: relationship between cercarial production levels and snail host susceptibility. Exp Parasitol 66: 78-85.
3. Fenwick A, Webster JP, Bosque-Oliva E, Blair L, Fleming FM, et al. (2009) The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002-2008. Parasitol 136: 1719-1730.
4. Mone Y, Ribou AC, Cosseau C, Duval D, Theron A, et al. (2011) An example of molecular co-evolution: Reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions. Int J Parasitol 41: 721-730.
5. 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.
6. 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.
7. Hanington PC, Lun CM, Adema CM, Loker ES, (2010) Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. Int J Parasitol 40: 819-831.
8. Hanington PC, Zhang SM, (2011) The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J Innate Immun 3: 17-27.
9. Adema CM, Hertel LA, Miller RD, Loker ES, (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. PNAS USA 94: 8691-8696.
10. Mone Y, Gourbal B, Duval D, Du Pasquier L, Kieffer-Jaquinod S, et al. (2010) A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS NTD 4 e813.
11. Hanington PC, Forys MA, Dragoo JW, Zhang SM, Adema CM, et al. (2010) Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. PNAS USA 107: 21087-21092.
12. Adema CM, Arguello DF 2nd, Stricker SA, Loker ES, (1994) A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa. J Parasitol 80: 719-727.
13. Lie KJ, Heyneman D, (1979) Capacity of irradiated echinostome sporocysts to protect Schistosoma mansoni in resistant Biomphalaria glabrata. Int J Parasitol 9: 539-543.
14. Lie KJ, Heyneman D, Richards CS, (1977) Schistosoma mansoni- Temporary Reduction of Natural-Resistance in Biomphalaria glabrata Induced by Irradiated Miracidia of Echinostoma paraensei. Exp Parasitol 43: 54-62.
15. Adema CM, Hanington PC, Lun CM, Rosenberg GH, Aragon AD, et al. (2010) Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 47: 849-860.
16. Adema CM, Harris RA, van Deutekom-Mulder EC, (1992) A comparative study of hemocytes from six different snails: morphology and functional aspects. J Invert Pathol 59: 24-32.
17. Lewis FA, Stirewalt MA, Souza CP, Gazzinelli G, (1986) Large-scale laboratory maintenance of Schistosoma mansoni, with observations on three schistosome/snail host combinations. J Parasitol 72: 813-829.
18. Lafferty KD, Kuris AM, (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitol 25: 564-572.
19. Zhang SM, Adema CM, Kepler TB, Loker ES, (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305: 251-254.
20. Galvan AG, Paugam M, Sullivan JT, (2000) Rescue of sporocysts of Schistosoma mansoni in nonsusceptible Biomphalaria by head-foot transplantation into susceptible snails. J Parasitol 86: 308-311.
21. Lie KJ, Jeong KH, Heyneman D, (1980) Tissue reactions induced by Schistosoma mansoni in Biomphalaria glabrata. Annal Trop Med Parasitol 74: 157-166.
22. Noda S, Loker ES, (1989) Effects of infection with Echinostoma paraensei on the circulating haemocyte population of the host snail Biomphalaria glabrata. Parasitol 98 (Pt 1): 35-41.
23. Noda S, Loker ES, (1989) Phagocytic-Activity of Hemocytes of M-Line Biomphalaria glabrata Snails- Effect of Exposure to the Trematode Echinostoma paraensei. J Parasitol 75: 261-269.
24. DeGaffe G, Loker ES, (1998) Susceptibility of Biomphalaria glabrata to infection with Echinostoma paraensei: correlation with the effect of parasite secretory-excretory products on host hemocyte spreading. J Invert Pathol 71: 64-72.
25. Humbert E, Coustau C, (2001) Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata-Echinostoma caproni system. Parasitol 122: 651-660.
26. Adema CM, van Deutekom-Mulder EC, van der Knaap WP, Sminia T, (1994) Schistosomicidal activities of Lymnaea stagnalis haemocytes: the role of oxygen radicals. Parasitol 109 (Pt 4): 479-485.
27. Baeza Garcia A, Pierce RJ, Gourbal B, Werkmeister E, Colinet D, et al. (2010) Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathogen 6.
28. 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.
29. Yigzaw Y, Gielens C, Preaux G, (2001) Isolation and characterization of an alpha-macroglobulin from the gastropod mollusc Helix pomatia with tetrameric structure and preserved activity after methylamine treatment. Biochim Biophys Acta 1545: 104-113.
30. Amancha PK, Dissous C, Nadimpalli SK, (2009) Characterization of the mannose 6-phosphate receptor (Mr 300 kDa) protein dependent pathway of lysosomal enzyme targeting in Biomphalaria glabrata mollusc cells. Biochimie 91: 982-988.
31. Knight M, Raghavan N, Goodall C, Cousin C, Ittiprasert W, et al. (2009) Biomphalaria glabrata peroxiredoxin: effect of Schistosoma mansoni infection on differential gene regulation. Mol Biochem Parasitol 167: 20-31.
32. 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.
33. Brant SV, Loker ES, (2005) Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathogen 1: 167-169.
34. Southgate VR, Brown DS, Warlow A, Knowles RJ, Jones A, (1989) The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitol Research 75: 381-391.
35. Walker JC, (1979) Austrobilharzia terrigalensis- Schistosome Dominant in Interspecific Interactions in the Molluscan Host. Int J Parasitol 9: 137-140.