Resistance of biomphalaria glabrata 13-16-R1 snails to schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes

International Journal for Parasitology

Volumn 44, Issue 6, 2014, Pages 343-353

  Larson, Maureen K ^a   Bender, Randal C ^a   Bayne, Christopher J ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Biomphalaria; Expression; Haematocrit; Haemocyte; Host parasite; Oxidative; Resistance; Schistosoma

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR; OXIDOREDUCTASE; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ABUNDANCE; CELL ORGANELLE; GENE EXPRESSION; HOST-PARASITE INTERACTION; INTERMEDIATE HOST; PARASITE; PHENOTYPE; SCHISTOSOMIASIS; SNAIL;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOMPHALARIA GLABRATA; BLOOD CELL; BREEDING; CELL COUNT; CELL FUNCTION; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HOMOZYGOTE; HOST PARASITE INTERACTION; INFECTION RESISTANCE; INFECTION SENSITIVITY; LEUKOCYTE ACTIVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTE; PHENOTYPE; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI; SPOROCYST; ANIMAL; BIOMPHALARIA; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; TOXICITY;

BIOMPHALARIA; BIOMPHALARIA GLABRATA; GASTROPODA; SCHISTOSOMA; SCHISTOSOMA MANSONI;

ANIMALS; BIOMPHALARIA; BREEDING; CELL COUNT; GENE EXPRESSION PROFILING; HEMOCYTES; HOST-PARASITE INTERACTIONS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; REACTIVE OXYGEN SPECIES; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS, DNA;

EID: 84899955600     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.11.004     Document Type: Article

References (70)

1. Adema C.M., Hanington P.C., Lun C.M., Rosenberg G.H., Aragon A.D., Stout B.A., Lennard Richard M.L., Gross P.S., Loker E.S. Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol. Immunol. 2010, 47:849-860. 10.1016/j.molimm.2009.10.019.
2. Baeza Garcia A., Pierce R.J., Gourbal B., Werkmeister E., Colinet D., Reichhart J.M., Dissous C., Coustau C. Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog. 2010, 6(9):e1001115. 10.1371/journal.ppat.1001115.
3. Barçante T.A., Barçante J.M., Fujiwara R.T., Lima W.S. Analysis of circulating haemocytes from Biomphalaria glabrata following Angiostrongylus vasorum infection using flow cytometry. J. Parasitol. Res. 2012, 2012:314723. 10.1155/2012/314723.
4. Basch P.F. An interpretation of snail-trematode infection rates: specificity based on concordance of compatible phenotypes. Int. J. Parasitol. 1975, 5:449-452.
5. Bayne C.J. Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol. Biochem. Parasitol. 2009, 165:8-18. 10.1016/j.molbiopara.2009.01.005.
6. Bayne C.J., Buckley P.M., DeWan P.C. Macrophage-like hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro. J. Parasitol. 1980, 66:413-419.
7. Bayne C.J., Hahn U.K., Bender R.C. Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 2001, 123(Suppl.):S159-S167.
8. Bender R.C., Goodall C.P., Blouin M.S., Bayne C.J. Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosoma mansoni. Dev. Comp. Immunol. 2007, 31:874-878.
9. Blouin M.S., Bonner K.M., Cooper B., Amarasinghe V., O'Donnell R.P., Bayne C.J. Three genes involved in the oxidative burst are closely linked in the genome of the snail, Biomphalaria glabrata. Int. J. Parasitol. 2013, 43:51-55. 10.1016/j.ijpara.2012.10.020.
10. Bonner K.M., Bayne C.J., Larson M.K., Blouin M.S. Effects of Cu/Zn superoxide dismutase (sod1) genotype and genetic background on growth, reproduction and defense in Biomphalaria glabrata. PLoS Negl. Trop. Dis. 2012, 6(6):e1701. 10.1371/journal.pntd.0001701.
11. Castillo M.G., Wu X.J., Dinguirard N., Nyame A.K., Cummings R.D., Yoshino T.P. Surface membrane proteins of Biomphalaria glabrata embryonic cells bind fucosyl determinants on the tegumental surface of Schistosoma mansoni primary sporocysts. J. Parasitol. 2007, 93:832-840.
12. Chernin E. Observations on hearts explanted in vitro from the snail Australorbis glabratus. J. Parasitol. 1963, 49:353-364.
13. Daoust S.P., Rau M.E., McCloughlin J.D. Plagiorchis elegans (Trematoda) induces immune response in an incompatible snail host Biomphalaria glabrata (Pulmonata: Planorbidae). J. Parasitol. 2012, 98:1021-1022.
14. De Zoysa M., Nikapitiya C., Kim Y., Oh C., Kang D.H., Whang I., Kim S.J., Lee J.S., Choi C.Y., Lee J. Allograft inflammatory factor-1 in disk abalone (Haliotis discus discus): molecular cloning, transcriptional regulation against immune challenge and tissue injury. Fish Shellfish Immunol. 2010, 29:319-326. 10.1016/j.fsi.2010.04.006.
15. Deininger M.H., Meyermann R., Schluesener H.J. The allograft inflammatory factor-1 family of proteins. FEBS Lett. 2002, 514:115-121. 10.1016/S0014-5793(02)02430-4.
16. Fryer S.E., Hull C.J., Bayne C.J. Phagocytosis of yeast by Biomphalaria glabrata: carbohydrate specificity of hemocyte receptors and a plasma opsonin. Dev. Comp. Immunol. 1989, 13:9-16.
17. Goodall C.P., Bender R.C., Brooks J.K., Bayne C.J. Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Mol. Biochem. Parasitol. 2006, 147:207-210.
18. Hahn U.K., Bender R.C., Bayne C.J. Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev. Comp. Immunol. 2000, 24:531-541.
19. Hahn U.K., Bender R.C., Bayne C.J. Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J. Parasitol. 2001, 87:778-785.
20. Hall A., Nelson K., Poole L., Karplus P.A. Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 2010, 15(3):795-815.
21. Hanington P.C., Forys M.A., Loker E.S. A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl. Trop. Dis. 2012, 6(3):e1591. 10.1371/journal.pntd.0001591.
22. Humphries J.E., Yoshino T.P. Regulation of hydrogen peroxide release in circulating hemocytes of the planorbid snail Biomphalaria glabrata. Dev. Comp. Immunol. 2008, 32:554-562.
23. Ittiprasert W., Miller A., Su X.-Z., Mu J., Bhusudsawang G., Ukoskit K., Knight M. Identification and characterisation of functional expressed sequence tags-derived simple sequence repeat (eSSR) markers for genetic linkage mapping of Schistosoma mansoni juvenile resistance and susceptibility loci in Biomphalaria glabrata. Int. J. Parasitol. 2013, 43:669-677. 10.1016/j.ijpara.2013.03.007.
24. Johnston L.A., Yoshino T.P. Larval Schistosoma mansoni excretory-secretory glycoproteins (ESPs) bind to hemocytes of Biomphalaria glabrata (Gastropoda) via surface carbohydrate binding receptors. J. Parasitol. 2001, 87:786-793.
25. Knight M., Raghavan N., Goodall C., Cousin C., Ittiprasert W., Sayed A., Miller A., Williams D.L., Bayne C.J. Biomphalaria glabrata peroxiredoxin: effect of Schistosoma mansoni infection on differential gene regulation. Mol. Biochem. Parasitol. 2009, 167:20-31. 10.1016/j.molbiopara.2009.04.002.
26. Lee W., Choi K.S., Riddell J., Ip C., Ghosh D., Park J.H., Park Y.M. Human peroxiredoxin 1 and 2 are not duplicate proteins: the unique presence of CYS83 in Prx1 underscores the structural and functional differences between Prx1 and Prx2.J. Biol. Chem. 2007, 282:22011-22022.
27. Lewis F.A., Patterson C.N., Grzywacz C. Parasite-susceptibility phenotypes of F1 Biomphalaria glabrata progeny derived from interbreeding Schistosoma mansoni-resistant and -susceptible snails. Parasitol. Res. 2003, 89:98-101.
28. Lockyer A.E., Emery A.M., Kane R.A., Walker A.J., Mayer C.D., Mitta G., Coustau C., Adema C.M., Hanelt B., Rollinson D., Noble L.R., Jones C.S. Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni. PLoS ONE 2012, 7(12):e51102. 10.1371/journal.pone.0051102.
29. Loker E.S. Gastropod immunobiology. Adv. Exp. Med. Biol. 2010, 708:17-43. 10.1007/978-1-4419-8059-5_2.
30. Martins-Souza R.L., Pereira C.A., Coelho P.M., Martins-Filho O.A., Negrão-Corrêa D. Flow cytometry analysis of the circulating haemocytes from Biomphalaria glabrata and Biomphalaria tenagophila following Schistosoma mansoni infection. Parasitology 2009, 136:67-76. 10.1017/S0031182008005155.
31. Martins-Souza R.L., Pereira C.A., Rodrigues L., Araújo E.S., Coelho P.M., Corrêa A., Negrão-Corrêa D. Participation of N-acetyl-d-glucosamine carbohydrate moieties in the recognition of Schistosoma mansoni sporocysts by haemocytes of Biomphalaria tenagophila. Mem. Inst. Oswaldo Cruz 2011, 106:884-891.
32. Meitzler J.L., Hinde S., Bánfi B., Nauseef W.M., Ortiz de Montellano P.R. Conserved cysteine residues provide a protein-protein interaction surface in dual oxidase (duox) proteins. J. Biol. Chem. 2013, 288:7147-7157.
33. Michelson E.H., DuBois L. Susceptibility of Bahian populations of Biomphalaria glabrata to an allopatric strain of Schistosoma mansoni. Am. J. Trop. Med. Hyg. 1978, 27:782-786.
34. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., Bouchut A., Coustau C. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev. Comp. Immunol. 2005, 29:393-407.
35. Mitta G., Adema C.M., Gourbal B., Loker E.S., Théron A. Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev. Comp. Immunol. 2012, 37:1-8. 10.1016/j.dci.2011.09.002.
36. Molina-Cruz A., Garver L.S., Alabaster A., Bangiolo L., Haile A., Winikor J., Ortega C., van Schaijk B.C., Sauerwein R.W., Taylor-Salmon E., Barillas-Mury C. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 2013, 340(6135):984-987. 10.1126/science.1235264.
37. Moné Y., Gourba L.B., Duva l.D., Du Pasquier L., Kieffer-Jaquinod S., Mitta G. 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. 2010, 4(9):pii: e813. 10.1371/journal.pntd.0000813.
38. Mourão Mde M., Dinguirard N., Franco G.R., Yoshino T.P. Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress. PLoS Negl. Trop. Dis. 2009, 3(11):e550. 10.1371/journal.pntd.0000550.
39. Negrão-Corrêa D., Mattos A.C., Pereira C.A., Martins-Souza R.L., Coelho P.M. Interaction of Schistosoma mansoni sporocysts and hemocytes of Biomphalaria. J. Parasitol. Res. 2012, 2012:743920. 10.1155/2012/743920.
40. Neumann C.A., Krause D.S., Carman C.V., Das S., Dubey D.P., Abraham J.L., Bronson R.T., Fujiwara Y., Orkin S.H., Van Etten R.A. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 2003, 424(6948):561-565. 10.1038/nature01819. PMID 12891360.
41. Newton W.L. The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus. Exp. Parasitol. 1953, 2:242-257.
42. Niemann G.M., Lewis F.A. Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Exp. Parasitol. 1990, 70:286-292.
43. Noda S., Loker E.S. Effects of infection with Echinostoma paraensei on the circulating haemocyte population of the host snail Biomphalaria glabrata. Parasitology 1989, 98:35-41.
44. Oliveira A.L., Levada P.M., Zanotti-Magalhaes E.M., Magalhães L.A., Ribeiro-Paes J.T. Differences in the number of hemocytes in the snail host Biomphalaria tenagophila, resistant and susceptible to Schistosoma mansoni infection. Genet. Mol. Res. 2010, 9:2436-2445.
45. Pawlik A., Kurzawski M., Dziedziejko V., Safranow K., Paczkowska E., Maslinski W., Drozdzik M., Gawronska-Szklarz B. Allograft inflammatory factor-1 gene polymorphisms in patients with rheumatoid arthritis. Genet. Test Mol. Biomarkers. 2011, 16:341-534. 10.1089/gtmb.2011.0201.
46. Phalen T.J., Weirather K., Deming P.B., Anathy V., Howe A.K., van der Vliet A., Jönsson T.J., Poole L.B., Heintz N.H. Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery. J. Cell Biol. 2006, 175:779-789.
47. Ramakers C., Ruijter J.M., Deprez R.H., Moorman A.F. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 2003, 339(1):62-66.
48. Renwrantz L.R., Richards E.H. Recognition of beta-glucuronidase by the calcium-independent phosphomannosyl surface receptor of haemocytes from the gastropod mollusc, Helix pomatia. Dev. Comp. Immunol. 1992, 16:251-256.
49. Richards C.S., Merritt J.W. Genetic factors in susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection. Am. J. Trop. Med. Hyg. 1972, 21:425-434.
50. Richards C.S., Knight M., Lewis F.A. Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol. Today. 1992, 8:171-174.
51. Roger E., Grunau C., Pierce R.J., Hirai H., Gourbal B., Galinier R., Emans R., Cesari I.M., Cosseau C., Mitta G. Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Negl. Trop. Dis. 2008, 2(11):e330. 10.1371/journal.pntd.0000330.
52. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132:365-386.
53. Sim S., Jupatanakul N., Ramirez J.L., Kang S., Romero-Vivas C.M., Mohammed H., Dimopoulos G. Transcriptomic profiling of diverse Aedes aegypti strains reveals increased basal-level immune activation in Dengue virus-refractory populations and identifies novel virus-vector molecular interactions. PLoS Negl. Trop. Dis. 2013, 7(7):e2295. 10.1371/journal.pntd.0002295.
54. Steinauer M.L., Bonner K.M. Host susceptibility is altered by light intensity after exposure to parasites. J. Parasitol. 2012, 98:1052-1054. 10.1645/GE-3109.1.
55. Stibbs H.H., Owczarzak A., Bayne C.J., DeWan P. Schistosome sporocyst-killing amoebae isolated from Biomphalaria glabrata. J. Invert. Pathol. 1979, 33:159-170.
56. Trotter E.W., Rand J.D., Vickerstaff J., Grant C.M. The yeast Tsa1 peroxiredoxin is a ribosome-associated antioxidant. Biochem. J. 2008, 412:73-80.
57. Ulmer M.J. Laboratory maintenance of parasites. Experiments and Techniques in Parasitology 1970, 143-144. W.H. Freeman Co., San Francisco, California. A.J. MacInnis, M. Voge (Eds.).
58. van der Knaap W.P., Loker E.S. Immune mechanisms in trematode-snail interactions. Parasitol. Today 1990, 6:175-182.
59. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
60. Veal E.A., Findlay V.J., Day A.M., Bozonet S.M., Evans J.M., Quinn J., Morgan B.A. A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol. Cell 2004, 15:129-139.
61. Vivancos A.P., Castillo E.A., Biteau B., Nicot C., Ayte J., Toledano M.B., Hidalgo E. A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8875-8880.
62. Webster J.P., Davies C.M., Ndamba J., Noble L.R., Jones C.S., Woolhouse M.E. Spatio-temporal genetic variability in the schistosome intermediate host Biomphalaria pfeifferi. Ann. Trop. Med. Parasitol. 2001, 95. 5155-27.
63. Webster J.P., Davies C.M., Hoffman J.I., Ndamba J., Noble L.R., Woolhouse M.E. Population genetics of the schistosome intermediate host Biomphalaria pfeifferi in the Zimbabwean highveld: implications for co-evolutionary theory. Ann. Trop. Med. Parasitol. 2001, 95:203-214.
64. Wood Z.A., Poole L.B., Karplus P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003, 300:650-653.
65. Woolhouse M.E., Webster J.P. In search of the red queen. Parasitol. Today 2000, 16:506-508.
66. Yamamoto A., Ashihara E., Nakagawa Y., Obayashi H., Ohta M., Hara H., Adachi T., Seno T., Kadoya M., Hamaguchi M., Ishino H., Kohno M., Maekawa T., Kawahito Y. Allograft inflammatory factor-1 is overexpressed and induces fibroblast chemotaxis in the skin of sclerodermatous GVHD in a murine model. Immunol. Lett. 2011, 30(135):144-150. 10.1016/j.imlet.2010.10.015.
67. Zakikhani M., Smith J.M., Rau M.E. Effect of Plagiorchis elegans (Digenea: Plagiorchiidae) infections of Biomphalaria glabrata (Pulmonata: Planorbidae) on a challenge infection with Schistosoma mansoni (Digenea: Schistosomatidae). J. Parasitol. 2003, 89:70-75.
68. Zhang Y., Li J., Yu F., He X., Yu Z. Allograft inflammatory factor-1 stimulates hemocyte immune activation by enhancing phagocytosis and expression of inflammatory cytokines in Crassostrea gigas. Fish Shellfish Immunol. 2013, 34:1071-1077. 10.1016/j.fsi.2013.01.014.
69. Zhang L., Zhao J., Li C., Su X., Chen A., Li T., Qin S. Cloning and characterization of allograft inflammatory factor-1 (AIF-1) from Manila clam Venerupis philippinarum. Fish Shellfish Immunol. 2011, 30:148-153. 10.1016/j.fsi.2010.09.021.
70. Zhao Y.Y., Yan D.J., Chen Z.W. Role of AIF-1 in the regulation of inflammatory activation and diverse disease processes. Cell. Immunol. 2013, 284:75-83. 10.1016/j.cellimm.2013.07.008.