Circulating Biomphalaria glabrata hemocyte subpopulations possess shared schistosome glycans and receptors capable of binding larval glycoconjugates

Experimental Parasitology

Volumn 133, Issue 1, 2013, Pages 28-36

  Yoshino, Timothy P ^a   Wu, Xiao Jun ^a   Gonzalez, Laura A ^a   Hokke, Cornelis H ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Biomphalaria glabrata; Glycoconjugate; Glycotope sharing; Hemocyte; Larval transformation products (LTPs); Molecular mimicry; Schistosoma mansoni; Sporocyst

Indexed keywords

GLYCAN; GLYCOCONJUGATE; MONOCLONAL ANTIBODY; SIALYL LEWIS X ANTIGEN;

ANIMAL CELL; ARTICLE; BIOMPHALARIA GLABRATA; BLOOD CELL; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HOST PARASITE INTERACTION; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; LARVA; MOLECULAR MIMICRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR BINDING; SCHISTOSOMA MANSONI; STRAIN DIFFERENCE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOMPHALARIA; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPITOPES; GLYCOCONJUGATES; HEMOCYTES; HOST-PARASITE INTERACTIONS; IMMUNOHISTOCHEMISTRY; LARVA; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR MIMICRY; POLYSACCHARIDES; RECEPTORS, PATTERN RECOGNITION; SCHISTOSOMA MANSONI;

BIOMPHALARIA GLABRATA; GASTROPODA; SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 84870524874     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2012.10.002     Document Type: Article

References (52)

1. Adema C.M., Hertel L.A., Miller R.D., Loker E.S. A family of fibrinogen-related proteins that precipitate parasite-derived molecules is produced by an invertebrate after infection. Proc. Natl. Acad. Sci. (USA) 1997, 94:8691-8696.
2. 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.
3. Bayne C.J., Buckley P.M., DeWan P.C. Schistosoma mansoni: cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata. Exp. Parasitol. 1980, 50:409-416.
4. Cavalcanti M.G.S., Filho F.C., Mendonca A.M., Duarte G.R., Barbosa C.C., De Castro C.M., Alves L.C., Brayner F.A. Morphological characterization of hemocytes from Biomphalaria glabrata and Biomphalaria straminea. Micron 2012, 43:285-291.
5. Cheng T.C., Auld K.R. Hemocytes of the pulmonate gastropod Biomphalaria glabrata. J. Invertebr. Pathol. 1977, 30:119-122.
6. Chernin E. Observations on hearts explanted in vitro from the snail Australorbis glabratus. J. Parasitol. 1963, 49:353-364.
7. Connors V.A., Yoshino T.P. In vitro effect of larval Schistosoma mansoni excretory-secretory products on phagocytosis-stimulated superoxide production in hemocytes from Biomphalaria glabrata. J. Parasitol. 1990, 76:895-902.
8. Damian R.T. Molecular mimicry: antigen sharing by parasite and host and its consequences. Am. Nat. 1964, 98:129-149.
9. Edmondson, D.G., Dent, S.Y.R., 2001. Identification of protein interactions by far-Western analysis. Curr. Protocols Prot. Sci., 19.7.1-19.7.10. Online publication, Wiley and Sons, Inc. doi:10.1002/0471140864.ps1907s25.
10. Guillou F., Roger E., Mone Y., Rognon A., Grunau C., Theron A., Mitta G., Coustau C., Gourbal B.E. Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol. Biochem. Parasitol. 2007, 155:45-56.
11. Hall R.A. Protein-protein interactions: methods and applications. Methods Mol. Biol. 2004, 261:167-174.
12. Hanington P.C., Forys M.A., Dragoo J.W., Zhang S.M., Adema C.M., Loker E.S. Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc. Natl. Acad. Sci. USA 2010, 107:21087-21092.
13. 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.
14. Hanington P.C., Zhang S.M. The primary role of fibrinogen-related proteins is invertebrate defense, not coagulation. J. Innate Immun. 2011, 3:17-27.
15. Jeong K.H., Heyneman D. Leukocytes of Biomphalaria glabrata: morphology and behavior of granulocytic cells in vitro. J. Invertebr. Pathol. 1976, 28:357-362.
16. 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.
17. Lehr T., Geyer H., Maass K., Doenhoff M.J., Geyer R. Structural characterization of N-glycans from the freshwater snail Biomphalaria glabrata cross-reacting with Schistosoma mansoni glycoconjugates. Glycobiology 2007, 17:82-103.
18. Lehr T., Beuerlein K., Doenhoff M.J., Grevelding C.G., Geyer R. Localization of carbohydrates common to Biomphalaria glabrata as well as to sporocysts and miracidia of Schistosoma mansoni. Parasitology 2008, 135:931-942.
19. Lehr T., Frank S., Natsuka S., Geyer H., Beuerlein K., Doenhoff M.J., Hase S., Geyer R. N-Glycosylation patterns of hemolymph glycoproteins from Biomphalaria glabrata strains expressing different susceptibility to Schistosoma mansoni infection. Exp. Parasitol. 2010, 126:592-602.
20. Lie K.J. Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata. A discussion of the interference theory. Trop. Geogr. Med. 1982, 34:111-122.
21. Lodes M.J., Connors V.A., Yoshino T.P. Isolation and functional characterization of snail hemocyte-modulating polypeptide from primary sporocysts of Schistosoma mansoni. Mol. Biochem. Parasitol. 1991, 49:1-10.
22. Loker E.S. Gastropod immunobiology. Adv. Exp. Med. Biol. 2010, 708:17-43.
23. Loker E.S., Adema C.M., Zhang S.M., Kepler T.B. Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol. Rev. 2004, 198:10-24.
24. Loker E.S., Bayne C.J., Buckley P.M., Kruse K.T. Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by hemocytes of juveniles of the 10-R2 strain of Biomphalaria glabrata. J. Parasitol. 1982, 68:84-94.
25. Loker E.S., Cimino D.F., Hertel L.A. Excretory-secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria glabrata hemocyte functions. J. Parasitol. 1992, 78:104-115.
26. Matricon-Gondran M., Letocart M. Internal defenses of the snail Biomphalaria glabrata. I. Characterization of hemocytes and fixed phagocytes. J. Invertebr. Pathol. 1999, 74:224-234.
27. Martins-Souza R.L., Pereira C.A.J., Martins Filho O.A., Coelho P.M.Z., Correa A., Negrao-Correa D. Differential lectin labeling of circulating hemocytes from Biomphalaria glabrata and Biomphalaria tenagophila resistant or susceptible to Schistosoma mansoni. Mem. Inst. Oswaldo Cruz 2006, 101(Suppl. 1):185-192.
28. Mitta G., Adema C.M., Gourbal B., Loker E.S., Theron A. Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev. Comp. Immunol. 2012, 37:1-8.
29. Mone Y., Gourbal B., Duval 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):e813.
30. Nyame A.K., Yoshino T.P., Cummings R.D. Differential expression of LacdiNAc, fucosylated LacdiNAc, and Lewis x glycan antigens in intramolluscan stages of Schistosoma mansoni. J. Parasitol. 2002, 88:890-897.
31. Peterson N.A., Hokke C.H., Deelder A.M., Yoshino T.P. Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: differential expression during the miracidium-to-sporocyst transformation. Int. J. Parasitol. 2009, 39:1331-1344.
32. Robijn M.L., Wuhrer M., Kornelis D., Deelder A.M., Geyer R., Hokke C.H. Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms, and eggs. Parasitology 2005, 130:67-77.
33. Roger E., Mitta G., Mone Y., Bouchut A., Rognon A., Grunau C., Boissier J., Theron A., Gourbal B.E.F. Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/Schistosoma mansoni model: new candidates identified by a global comparative proteomics approach. Mol. Biochem. Parasitol. 2008, 157:205-216.
34. 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 intermediate host Biomphalaria glabrata. PLoS Negl. Trop. Dis. 2008, 211:e330.
35. Sullivan J.T., Richards C.S. Schistosoma mansoni, NIH-SM-PR-2 strain, in susceptible and nonsusceptible stocks of Biomphalaria glabrata: comparative histology. J. Parasitol. 1981, 67:702-708.
36. Schoenberg D.A., Cheng T.C. Lectin-binding specificities of hemocytes from two strains of Biomphalaria glabrata as determined by microhemadsorption assays. Dev. Comp. Immunol. 1980, 4:617-628.
37. Sminia T., Barendsen L. A comparative morphological and enzyme histochemical study on blood cells of the fresh water snails Lymnaea stagnalis, Biomphalaria glabrata and Bulinus truncates. J. Morphol. 1980, 165:31-39.
38. Stout B.A., Adema C.M., Zhang S.M., Loker E.S. Biology of FREPs: diversified lectins with fibrinogen-related domains from freshwater snail Biomphalaria glabrata. Animal Lectins: a Functional View 2009, 471-491. CRC Press, Taylor & Francis, Boca Raton. G. Vasta, H. Ahmed (Eds.).
39. van Remoortere A., Hokke C.H., van Dam G.J., van Die I., Deelder A.M., van den Eijnden D.H. Various stages of Schistosoma express LewisX, LacdiNAc, GalNAcβ1-4 (Fucα1-3)GlcNAc and GalNAcβ1-4(Fucα1-2Fucα1-3)GlcNAc carbohydrate epitopes: detection with monoclonal antibodies that are characterized by enzymatically synthesized neoglycoproteins. Glycobiology 2000, 10:601-609.
40. van Roon A.M.M., Aguilera B., Cuenca F., van Remoortere A., van der Marel G.A., Deelder A.M., Overkleeft H.S., Hokke C.H. Synthesis and antibody binding of a series of parasite fuco-oligosaccharides. Bioorg. Med. Chem. 2005, 13:3553-3564.
41. Vermeire J.J., Yoshino T.P. Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection. Parasitology 2007, 134:1369-1378.
42. Wu X.J., Sabat G., Brown J.F., Zhang M., Taft A., Peterson N.A., Harms A., Yoshino T.P. Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol. Biochem. Parasitol. 2009, 164:32-44.
43. Yoshino T.P., Boswell C.A. Antigen sharing between larval trematodes and their snail hosts: how real a phenomenon in immune evasion?. Immune Mechanisms in Invertebrate Vectors 1986, 221-238. Clarendon Press, Oxford, UK. A.M. Lackie (Ed.).
44. Yoshino T.P., Coustau C. Immunobiology of Biomphalaria-trematode interactions. Biomphalaria Snails and Larval Trematodes 2011, 159-189. Springer, New York. R. Toledo, B. Fried (Eds.).
45. Yoshino T.P., Granath W.O. Surface antigens of Biomphalaria glabrata (Gastropoda) hemocytes: functional heterogeneity in cell subpopulations recognized by a monoclonal antibody. J. Invertebr. Pathol. 1985, 45:174-186.
46. Yoshino T.P., Laursen J.R. Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic Bge cells. J. Parasitol. 1995, 81:714-722.
47. Yoshino T.P., Lodes M.J. Secretory protein biosynthesis in snail hemocytes: in vitro modulation by larval schistosome excretory-secretory products. J. Parasitol. 1988, 74:538-547.
48. Yoshino T.P., Wu X.J., Liu H.D., Gonzalez L.A., Deelder A.M., Hokke C.H. Glycotope shareing between snail hemolymph and larval schistosomes: larval transformation products alter shared glycan patterns of plasma proteins. PLoS Negl. Trop. Dis. 2012, 6(3):e1569.
49. Zahoor Z., Davies A.J., Kirk R.S., Rollinson D., Walker A.J. Disruption of ERK signalling in Biomphalaria glabrata defence cells by Schistosoma mansoni: implications for parasite survival in the snail host. Dev. Comp. Immunol. 2008, 32:1561-1571.
50. Zahoor Z., Davies A.J., Kirk R.S., Rollinson D., Walker A.J. Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway. Parasit. Vectors 2009, 2:18.
51. Zahoor Z., Davies A.J., Kirk R.S., Rollinson D., Walker A.J. Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata. Cell Stress Chaperones 2010, 15:639-650.
52. Zhang S.M., Zeng Y., Loker E.S. Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun. 2008, 14:175-189.