Reversing the resistance phenotype of the biomphalaria glabrata snail host schistosoma mansoni infection by temperature modulation

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Ittiprasert, Wannaporn ^a   Knight, Matty ^a  

^a BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELDANAMYCIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; RNA DIRECTED DNA POLYMERASE;

ARTICLE; BACTERIAL SHEDDING; BIOMPHALARIA GLABRATA; CERCARIA; CONTROLLED STUDY; FEMALE; GENE; HEAT STRESS; HOST; INFECTION SENSITIVITY; MALE; MODULATION; MOUSE; NONHUMAN; PARASITE; PHENOTYPE; RETROPOSON; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TEMPERATURE; ANIMAL; BIOMPHALARIA; DISEASE PREDISPOSITION; GENETICS; HEATING; HOST PARASITE INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PARASITOLOGY; TRANSCRIPTION INITIATION;

BIOMPHALARIA GLABRATA; GASTROPODA; SCHISTOSOMA MANSONI; TREMATODA;

ANIMALS; BIOMPHALARIA; CERCARIA; DISEASE SUSCEPTIBILITY; FEMALE; HEATING; HOST-PARASITE INTERACTIONS; HSP70 HEAT-SHOCK PROTEINS; IMMUNITY, INNATE; MICE; PHENOTYPE; SCHISTOSOMA MANSONI; TRANSCRIPTIONAL ACTIVATION;

EID: 84861208362     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002677     Document Type: Article

References (63)

1. King CH, Sturrock RF, Kariuki HC, Hamburger J, (2006) Transmission control for schistosomiasis-why it matters now. Trends Parasitol 22: 575-582.
2. Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, et al. (2006) Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20: 593-600.
3. Rollinson D, Webster JP, Webster B, Nyakaana S, Jorgensen A, et al. (2009) Genetic diversity of schistosomes and snails: implications for control. Parasitology pp. 1-11.
4. Lewis FA, Patterson CN, Knight M, Richards CS, (2001) The relationship between Schistosoma mansoni and Biomphalaria glabrata: genetic and molecular approaches. Parasitology 123 (Suppl): S169-179.
5. Richards CS, Knight M, Lewis FA, (1992) Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol Today 8: 171-174.
6. Knight M, Miller AN, Patterson CN, Rowe CG, Michaels G, et al. (1999) The identification of markers segregating with resistance to Schistosoma mansoni infection in the snail Biomphalaria glabrata. Proc Natl Acad Sci U S A 96: 1510-1515.
7. Lockyer AE, Spinks J, Kane RA, Hoffmann KF, Fitzpatrick JM, et al. (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.
8. 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.
9. Ittiprasert W, Miller A, Myers J, Nene V, El-Sayed NM, et al. (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: 27-39.
10. Rollinson D, Stothard JR, Jones CS, Lockyer AE, de Souza CP, et al. (1998) Molecular characterisation of intermediate snail hosts and the search for resistance genes. Mem Inst Oswaldo Cruz 93 (Suppl 1): 111-116.
11. 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 Pathog 6: e1001115.
12. Hanington PC, Zhang SM, (2011) The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J Innate Immun 3: 17-27.
13. Bouchut A, Roger E, Gourbal B, Grunau C, Coustau C, et al. (2008) The compatibiuty polymorphism in invertebrate host/trematodes interactions: research of molecular determinants. Parasite 15: 304-309.
14. Mitta G, Adema CM, Gourbal B, Loker ES, Theron A, (2011) Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms. Dev Comp Immunol E-pub ahead of print.
15. Moné 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 Negl Trop Dis 4: pii e813.
16. Theron A, Coustau C, (2005) Are Biomphalaria snails resistant to Schistosoma mansoni? J Helminthol 79: 187-191.
17. Paraense W, Correa L, (1963) Variations in susceptibility of populations of Australorbis blabratus to a strain of Schistosoma mansoni. Revista do Instituto de Medicina Tropical de São Paulo 5: 15-22.
18. Richards CS, Shade PC, (1987) The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. J Parasitol 73: 1146-1151.
19. Richards CS, Minchella DJ, (1987) Transient non-susceptibility to Schistosoma mansoni associated with atrial amoebocytic accumulations in the snail host Biomphalaria glabrata. Parasitology 95 (Pt 3): 499-505.
20. 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.
21. 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.
22. Ittiprasert W, Nene R, Miller A, Raghavan N, Lewis F, et al. (2009) Schistosoma mansoni infection of juvenile Biomphalaria glabrata induces a differential stress response between resistant and susceptible snails. Exp Parasitol 123: 203-211.
23. Zahoor Z, Davies AJ, Kirk RS, Rollinson D, Walker AJ, (2010) Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP 70 protein expression in defence cells of its snail host, Biomphalaria glabrata. Cell Stress Chaperones 15: 639-650.
24. Stirewalt MA, (1954) Effect of snail maintenance temperatures on development of Schistosoma mansoni. Exp Parasitol 3: 504-516.
25. Lefcort H, Bayne CJ, (1991) Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni (Trematoda). Parasitology 103 Pt 3: 357-362.
26. 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.
27. 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.
28. Lewis FA, Knight M, Richards CS, (1997) A laboratory-based approach to biological control of snails. Mem Inst Oswaldo Cruz 92: 661-662.
29. 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.
30. 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.
31. 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.
32. Chomczynski P, (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15: 532-534, 536-537.
33. Raghavan N, Miller AN, Gardner M, FitzGerald PC, Kerlavage AR, et al. (2003) Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol Biochem Parasitol 126: 181-191.
34. 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.
35. 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.
36. 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.
37. Simpson AJ, Dias Neto E, Vidigal TH, Pena HB, Carvalho OS, et al. (1995) DNA polymorphism of schistosomes and their snail hosts. Mem Inst Oswaldo Cruz 90: 211-213.
38. Chang YS, Lo CW, Sun FC, Chang MD, Lai YK, (2006) Differential expression of Hsp90 isoforms in geldanamycin-treated 9L cells. Biochem Biophys Res Commun 344: 37-44.
39. Harrison EM, Sharpe E, Bellamy CO, McNally SJ, Devey L, et al. (2008) Heat shock protein 90-binding agents protect renal cells from oxidative stress and reduce kidney ischemia-reperfusion injury. Am J Physiol Renal Physiol 295: F397-405.
40. Kumar R, Musiyenko A, Barik S, (2003) The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malar J 2: 30.
41. Coustau C, Mitta G, Dissous C, Guillou F, Galinier R, et al. (2003) Schistosoma mansoni and Echinostoma caproni excretory-secretory products differentially affect gene expression in Biomphalaria glabrata embryonic cells. Parasitology 127: 533-542.
42. Humphries JE, Yoshino TP, (2006) Schistosoma mansoni excretory-secretory products stimulate a p38 signalling pathway in Biomphalaria glabrata embryonic cells. Int J Parasitol 36: 37-46.
43. Zahoor Z, Davies AJ, Kirk RS, Rollinson D, Walker AJ, (2009) Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway. Parasit Vectors 2: 18.
44. Knight M, Miller A, Liu Y, Scaria P, Woodle M, et al. (2011) Polyethyleneimine (PEI) mediated siRNA gene silencing in the Schistosoma mansoni snail host, Biomphalaria glabrata. PLoS Negl Trop Dis 5: e1212.
45. Lyupina YV, Dmitrieva SB, Timokhova AV, Beljelarskaya SN, Zatsepina OG, et al. (2010) An important role of the heat shock response in infected cells for replication of baculoviruses. Virology 406: 336-341.
46. Banumathy G, Singh V, Pavithra SR, Tatu U, (2003) Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. J Biol Chem 278: 18336-18345.
47. Pallavi R, Roy N, Nageshan RK, Talukdar P, Pavithra SR, et al. (2010) Heat shock protein 90 as a drug target against protozoan infections: biochemical characterization of HSP 90 from Plasmodium falciparum and Trypanosoma evansi and evaluation of its inhibitor as a candidate drug. J Biol Chem 285: 37964-37975.
48. Miyata Y, (2005) Hsp 90 inhibitor geldanamycin and its derivatives as novel cancer chemotherapeutic agents. Curr Pharm Des 11: 1131-1138.
49. Him NA, Gillan V, Emes RD, Maitland K, Devaney E, (2009) Hsp-90 and the biology of nematodes. BMC Evol Biol 9: 254.
50. Lindquist S, Craig EA, (1988) The heat shock proteins. Annu Rev Genet 22: 631-677.
51. Picard D, (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59: 1640-1648.
52. Kimura RH, Choudary PV, Stone KK, Schmid CW, (2001) Stress induction of Bm1 RNA in silkworm larvae: SINEs, an unusual class of stress genes. Cell Stress Chaperones 6: 263-272.
53. Beauregard A, Curcio MJ, Belfort M, (2008) The take and give between retrotransposable elements and their hosts. Annu Rev Genet 42: 587-617.
54. Perrigault M, Allam B, (2009) Cytotoxicity of quahog parasite unknown (QPX) toward hard clam (Mercenaria mercenaria) haemocytes and interactions between different pathogen isolates and host strains. Parasitology 136: 1281-1289.
55. Yue X, Liu B, Sun L, Tang B, (2011) Cloning and characterization of a hsp70 gene from Asiatic hard clam Meretrix meretrix which is involved in the immune response against bacterial infection. Fish Shellfish Immunol 30: 791-799.
56. Wang N, Whang I, Lee JS, Lee J, (2011) Molecular characterization and expression analysis of a heat shock protein 90 gene from disk abalone (Haliotis discus). Mol Biol Rep 38: 3055-3060.
57. Plytycz B, Seljelid R, (2002) Stress and immunity: minireview. Folia Biol (Krakow) 50: 181-189.
58. Moser D, Doumbo O, Klinkert MQ, (1990) The humoral response to heat shock protein 70 in human and murine Schistosomiasis mansoni. Parasite Immunol 12: 341-352.
59. Kanamura HY, Hancock K, Rodrigues V, Damian RT, (2002) Schistosoma mansoni heat shock protein 70 elicits an early humoral immune response in S. mansoni infected baboons. Mem Inst Oswaldo Cruz 97: 711-716.
60. Lie KJ, Heyneman D, (1977) Schistosoma mansoni, Echinostoma lindoense, and Paryphostomum segregatum: interference by trematode larvae with acquired resistance in snails, Biomphalaria glabrata. Exp Parasitol 42: 343-347.
61. Lie KJ, Heyneman D, Jeong KH, (1976) Studies on resistance in snails. 7. Evidence of interference with the defense reaction in Biomphalaria glabrata by trematode larvae. J Parasitol 62: 608-615.
62. Triantafilou M, Sawyer D, Nor A, Vakakis E, Triantafilou K, (2008) Cell surface molecular chaperones as endogenous modulators of the innate immune response. Novartis Found Symp 291: 74-79; discussion 79-85, 137-140.
63. Martorelli SR, Poulin R, Mouritsen KN, (2006) A new cercaria and metacercaria of Acanthoparyphium (Echinostomatidae) found in an intertidal snail Zeacumantus subcarinatus (Batillaridae) from New Zealand. Parasitol Int 55: 163-167.