Digenean-gastropod host associations inform on aspects of specific immunity in snails

Developmental and Comparative Immunology

Volumn 48, Issue 2, 2015, Pages 275-283

  Adema, C M ^a   Loker, E S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Acquired immunity; Biomphalaria glabrata; Host specificity; Host parasite interactions; Immune priming; Schistosomiasis

Indexed keywords

CARBOHYDRATE; FIBRINOGEN; GLYCAN; PARASITE ANTIGEN; PATTERN RECOGNITION RECEPTOR; REACTIVE OXYGEN METABOLITE;

ADAPTIVE IMMUNITY; ARTICLE; BIOMPHALARIA GLABRATA; CARBOHYDRATE ANALYSIS; DIGENEA; EVOLUTION; GENE EXPRESSION; HOST PARASITE INTERACTION; HOST RANGE; IMMUNOBIOLOGY; INTRASPECIFIC VARIATION; MIRACIDIUM; MOLECULAR RECOGNITION; NONHUMAN; PARASITE IMMUNITY; PROTEIN EXPRESSION; RNA INTERFERENCE; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; TREMATODE; ANIMAL; BIOMPHALARIA; IMMUNOLOGY; INNATE IMMUNITY; PARASITOLOGY; PHYSIOLOGY;

BIOMPHALARIA GLABRATA; GASTROPODA; TREMATODA;

ANIMALS; BIOMPHALARIA; HOST SPECIFICITY; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; TREMATODA;

EID: 84918504180     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2014.06.014     Document Type: Article

References (98)

1. Adema C.M., Hanington P.C., et al. 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.
2. Adema C.M., Hertel L.A., et al. Infection with Echinostoma paraensei (Digenea) induces parasite-reactive polypeptides in the hemolymph of the gastropod host Biomphalaria glabrata. Parasite Effects on Host Physiology and Behavior 1997, 77-99. Chapman Press, New York. N. Beckage (Ed.).
3. Adema C.M., Hertel L.A., et al. A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:8691-8696.
4. Adema C.M., Loker E.S. Specificity and immunobiology of larval digenean-snail interactions. Advances in Trematode Biology 1997, 229-264. CRC Press, Boca Raton. B. Fried, T.K. Graczyk (Eds.).
5. Adema C.M., van der Knaap W.P.W., et al. Molluscan hemocyte-mediated cytotoxicity: the role of reactive oxygen intermediates. Rev. Aquat. Sci. 1991, 4:201-223.
6. Barbosa F.S., Barbosa I., et al. Laboratory infections of the snail Planorbarius metidenjensis (Forbes) from French Morocco with a Brazilian strain of Schistosoma mansoni. Ann. Trop. Med. Parasitol. 1959, 53:314-315.
7. Baron O.L., van West P., et al. Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. PLoS Pathog. 2013, 9(12):e1003792.
8. Basch P.F. Intermediate host specificity in Schistosoma mansoni. Exp. Parasitol. 1976, 39:150-169.
9. Bonner K.M., Bayne C.J., et al. 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:e1701.
10. Brown D.S. Freshwater Snails of Africa and Their Medical Importance 2005, Taylor and Francis Limited. second ed.
11. Buckley K.M., Rast J.P. Dynamic evolution of toll-like receptor multigene families in echinoderms. Front. Immunol. 2012, 5(3):136.
12. Butcher A.R., Grove D.I. Description of the life-cycle stages of Brachylaima cribbi n. sp (Digenea: Brachylaimidae) derived from eggs recovered from human faeces in Australia. Syst. Parasitol. 2001, 49:211-221.
13. Caron Y., Martens K., et al. New insight in lymnaeid snails (Mollusca, Gastropoda) as intermediate hosts of Fasciola hepatica (Trematoda, Digenea) in Belgium and Luxembourg. Parasites Vectors 2014, 7:66.
14. Chernin E., Perlstein J.M. Protection of snails against miracidia of Schistosoma mansoni by various aquatic invertebrates. J. Parasitol. 1971, 57:217-219.
15. Christofi T., Apidianakis Y. Drosophila immune priming against Pseudomonas aeruginosa is short-lasting and depends on cellular and humoral immunity. F1000Res 2013, 2:76. (5).
16. Combes C., Moné H. Possible mechanisms of the decoy effect in Schistosoma mansoni transmission. Int. J. Parasitol. 1987, 17:971-975.
17. Coustau C., Yoshino T.P. Flukes without snails: advances in the in vitro cultivation of intramolluscan stages of trematodes. Exp. Parasitol. 2000, 94:62-66.
18. Damian R.T. Molecular mimicry - antigen sharing by parasite and host and its consequences. Am. Nat. 1964, 98:129-149.
19. Deleury E., Dubreuil G., et al. Specific versus non-specific immune responses in an invertebrate species evidenced by a comparative de novo sequencing study. PLoS One 2012, 7:e32512.
20. DeJong R.J., Morgan J.A.T., et al. Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni. Mol. Biol. Evol. 2001, 18:2225-2239.
21. Donald K.M., Kennedy M., et al. Host specificity and molecular phylogeny of larval digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int. J. Parasitol. 2004, 34:557-568.
22. Erwin D.H., Laflamme M., et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 2011, 334:1091-1097.
23. Esch G.W., Barger M.A., et al. The transmission of digenetic trematodes: style, elegance, complexity. Integr. Comp. Biol. 2002, 42:304-312.
24. Farag H.F., El Sayad M.H. Biomphalaria alexandrina naturally infected with Fasciola hepatica. Trans. R. Soc. Trop. Med. Hyg. 1995, 89:36.
25. Ferrandon D., Imler J.L., et al. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 2007, 7:862-874.
26. File S.K. Superinfection of Biomphalaria glabrata with Schistosoma mansoni. J. Parasitol. 1975, 61:75-78.
27. Frandsen F. Studies of the relationship between Schistosoma and their intermediate hosts. 3. Genus Biomphalaria and Schistosoma mansoni from Egypt, Kenya, Sudan, Uganda, West Indies (St Lucia) and Zaire (2 different strains - Katanga and Kinshasa). J. Helminthol. 1979, 53:321-348.
28. Galinier R., Portela J., et al. Biomphalysin, a new β pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathog. 2013, 9(3):e1003216.
29. Garcia A.B., Pierce R.J., et al. Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog. 2010, 6(9):e1001115. Sep 2010.
30. Ghosh J., Lun C.-M., et al. Invertebrate immune diversity. Dev. Comp. Immunol. 2011, 35:959-974.
31. Guillou F., Mitta G., et al. Use of individual polymorphism to validate potential functional markers: case of a candidate lectin (BgSel) differentially expressed in susceptible and resistant strains of Biomphalaria glabrata. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2004, 138:175-181.
32. Haas W. Parasitic worms: strategies of host finding, recognition and invasion. German Zool. Soc. 2003, 106:349-364.
33. Hahn U.K., Bender R.C., et al. Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J. Parasitol. 2001, 87:292-299.
34. Hanelt B., Lun C.-M., et al. Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J. Invert. Pathol. 2008, 99:192-203.
35. Hanington P.C., Lun C.-M., et al. 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. 2010, 40:819-831.
36. Hanington P.C., Forys M.A., et al. Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:21087-21092.
37. Hanington P.C., Forys M.A., et al. A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl. Dis. 2012, 6:e1591.
38. Hauton C., Smith V.J. Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. BioEssays 2007, 29:1138-1146.
39. Heyneman D. Successful infection with larval echinostomes surgically implanted into the body cavity of the normal snail host. Exp. Parasitol. 1966, 18:220-223.
40. Hoffmann J.A., Reichhart J.M. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 2002, 3:121-126.
41. Johnson P.T.J., Lund P.J., et al. Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proc. R. Soc. B Biol. Sci. 2009, 276:1657-1663.
42. Kagan I.G., Geiger S.J. The susceptibility of three strains of Australorbis glabratus to Schistosoma mansoni from Brazil and Puerto Rico. J. Parasitol. 1965, 51:622-627.
43. Kawasaki M., Delamare-Deboutteville, et al. Hemiuroid trematode sporocysts are undetected by hemocytes of their intermediate host, the ark cockle Anadara trapezia: potential role of surface carbohydrates in successful parasitism. Fish Shellfish Immunol. 2013, 35:1937-1947.
44. Klein J. Are invertebrates capable of anticipatory immune responses?. Scand. J. Immunol. 1989, 29:499-505.
45. Kechemir N., Combes C. Development of Schistosoma haematobium in Planorbarius metidjensis by means of microsurgical transplantations. C.R. Séances Acad. Sci. III 1982, 295:505-508.
46. Kraaijeveld A.R., Layen S.J., et al. Lack of phenotypic and evolutionary cross-resistance against parasitoids and pathogens in Drosophila melanogaster. PLoS One 2012, 7:e53002.
47. Lehr T., Frank S., et al. N-Glycosylation patterns of hemolymph glycoproteins from Biomphalaria glabrata strains expressing different susceptibility to Schistosoma mansoni infection. Exp. Parasitol. 2010, 126:592-602.
48. 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.
49. Lie K.J., Heyneman D. Studies on resistance in snails: a specific tissue reaction to Echinostoma lindoense in Biomphalaria glabrata snails. Int. J. Parasitol. 1975, 5:621-625.
50. Lie K.J., Heyneman D. Studies on resistance in snails. 3. Tissue reactions to Echinostoma lindoense sporocysts in sensitized and resensitized Biomphalaria glabrata. J. Parasitol. 1976, 62:51-58.
51. Lie K.J., Heyneman D. Acquired resistance to echinostomes in 4 Biomphalaria glabrata strains. Int. J. Parasitol. 1979, 9:533-537.
52. Lie K.J., Heyneman D., et al. Studies on resistance in snails. 4. Induction of ventricular capsules and changes in the amebocyte-producing organ during sensitization of Biomphalaria glabrata snails. J. Parasitol. 1976, 62:286-291.
53. Lie K.J., Heyneman D., et al. Studies on resistance in snails: specific resistance induced by irradiated miracidia of Echinostoma lindoense in Biomphalaria glabrata snails. Int. J. Parasitol. 1975, 5:627-631.
54. Lie K.J., Jeong K.H., et al. Acquired resistance in snails. Induction of resistance to Schistosoma mansoni in Biomphalaria glabrata. Int. J. Parasitol. 1983, 13:301-304.
55. Lie K.J., Jeong K.H., et al. Molluscan host reactions to helminthic infection. Soulsby, E.J.L. (Ed.), Immune responses in parasitic infections: immunology,immunopathology, and immunoprophylaxis, Volume IV: protozoa, arthropods, and invertebrates. CRC Press, Boca Raton Florida, pp. 211-270.
56. Lockyer A.E., Emery A.M., et al. Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni. PLoS One 2012, 7(12):e51102.
57. Lockyer A.E., Spinks J.N., et al. Biomphalaria glabrata transcriptome: identification of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev. Comp. Immunol. 2007, 31:763-782.
58. Lockyer A.E., Spinks J., et al. Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 2008, 9:634.
59. Loker E.S., Adema C.M., et al. Invertebrate immune systems - not homogeneous, not simple, not well understood. Immunol. Rev. 2004, 198:10-24.
60. Loker E.S., Bayne C.J. In vitro encounters between Schistosoma mansoni primary sporocysts and hemolymph components of susceptible and resistant strains of Biomphalaria glabrata. Am. J. Trop. Med. Hyg. 1982, 31:999-1005.
61. Loker E.S., Cimino D.F., et al. Excretory-secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria glabrata hemocyte functions. J. Parasitol. 1992, 78:104-115.
62. Lotfy W.M., Brant S.V., et al. Evolutionary origins, diversification and biogeography of liver flukes (Digenea, Fasciolidae). Am. J. Trop. Med. Hyg. 2008, 79:248-255.
63. Maldonado A., Vieira G.O., et al. Biological aspects of a new isolate of Echinostoma paraensei (Trematoda: Echinostomatidae): susceptibility of sympatric snails and the natural vertebrate host. Parasitol. Res. 2001, 87:853-859.
64. Manga-Gonzalez M.Y., Gonzalez-Lanza C., et al. Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. Parasitology 2001, 123:S91-S114.
65. McKindsey C.W., McLaughlin J.D. Species-specific and size-specific infection of snails by Cyclocoelum mutabile (Digenea, Cyclocoelidae). J. Parasitol. 1995, 81:513-519.
66. Minchella D.J., Sollenberger K.M., et al. Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 1995, 111:217-220.
67. Mitta G., Adema C.M., et al. Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev. Comp. Immunol. 2012, 37:1-8.
68. Mitta G., Galinier R., et al. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev. Comp. Immunol. 2005, 29:393-407.
69. Moné Y., Gourbal B., et al. 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:e813.
70. Moné Y., Ribou A.C., et al. An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions. Int. J. Parasitol. 2011, 41:721-730.
71. Nunez P.E., De Jong-Brink M. The suppressive excretory-secretory product of Trichobilharzia ocellata: a possible factor determining compatibility in parasite-host interactions. Parasitology 1997, 115:193-203.
72. Petney T.N., Andrews R.H., et al. The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini. Int. J. Parasitol. 2013, 43:1031-1046.
73. Pham L.N., Dionne M.S., et al. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 2007, 3(3):e26.
74. Portela J., Duval D., et al. Evidence for specific genotype-dependent immune priming in the lophotrochozoan Biomphalaria glabrata snail. J. Innate Immunity 2013, 5:261-276.
75. Raghavan N., Miller A.N., et al. Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol. Biochem. Parasitol. 2003, 126:181-191.
76. Renwrantz L. Lectins in molluscs and arthropods: their occurrence, origin and roles in immunity. Proc. Zool. Soc. Lond. 1986, 56:81-93.
77. Richards C.S., Knight M., et al. Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol. Today 1992, 8:171-174.
78. Rollinson D., Stothard J.R., et al. Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group. Parasitology 2001, 123:S245-S260.
79. Sapp K.K., Loker E.S. Mechanisms underlying digenean - snail specificity: role of miracidial attachment and host plasma factors. J. Parasitol. 2000, 86:1012-1019.
80. Sapp K.K., Loker E.S. A comparative study of mechanisms underlying digenean - snail specificity: in vitro interactions between hemocytes and digenean larvae. J. Parasitol. 2000, 86:1020-1029.
81. Sire C., Rognon A., Theron A. Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism?. Parasitology 1998, 117:117-122.
82. Southgate V.R., Brown D.S., et al. The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitol. Res. 1989, 75:381-391.
83. Spatz L., Gonzalez Cappa S.M., et al. Susceptibility of wild populations of Biomphalaria spp. from Neotropical South America to Schistosoma mansoni and interference of Zygocotyle lunata. J. Parasitol. 2012, 98:1291-1295.
84. Steinauer M.L., Mwangi I.N., et al. Interactions between natural populations of human and rodent schistosomes in the lake Victoria region of Kenya: a molecular epidemiological approach. PLoS Negl. Trop. Dis. 2008, 2(4):e222.
85. Steinauer M.L., Hanelt B., et al. Genetic structure of Schistosoma mansoni in western Kenya: the effects of geography and host sharing. Int. J. Parasitol. 2009, 39:1353-1362.
86. Stout B.A., Adema C.M., et al. The biology of FREPs: diversified lectins with fibrinogen-related domains from the freshwater snail Biomphalaria glabrata. Animal Lectins, A Functional View 2008, 475-491. CRC Press Taylor & Francis. G. Vasta, H. Ahmed (Eds.).
87. Sudds R.H. Observations of schistosome miracidial behavior in the presence of normal and abnormal snail hosts and subsequent tissue studies of these hosts. J. Elisha Mitchell Sci. Soc. 1960, 76:121-133.
88. Sullivan J.T., Yeung J.T. Incompatibility between miracidia of Schistosoma mansoni and Helisoma duryi occurs at two stages: penetration and intramolluscan establishment. J. Parasitol. 2011, 97:743-745.
89. Théron A., Coustau C. Are Biomphalaria snails resistant to Schistosoma mansoni?. J. Helminthol. 2005, 79:187-191.
90. Van der Knaap W.P.W., Loker E.S. Immune mechanisms in trematode-snail interactions. Parasitol. Today 1990, 6:175-182.
91. Vasquez R.E., Sullivan J.T. Further characterization of passively transferred resistance to Schistosoma mansoni in the snail intermediate host Biomphalaria glabrata. J. Parasitol. 2001, 87:1360-1365.
92. Vasta G.R., Ahmed H., et al. Galectins as self/non-self recognition receptors in innate and adaptive immunity: an unresolved paradox. Front. Immunol. 2012, 3:199.
93. Walker J.C. Austrobilharzia terrigalensis - schistosome dominant in interspecific interactions in the molluscan host. Int. J. Parasitol. 1979, 9:137-140.
94. Yoshino T.P., Dinguirard N., et al. 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 2008, 411:46-58.
95. Yoshino T.P., Wu X.-J., et al. Glycotope sharing between snail hemolymph and larval schistosomes: larval transformation products alter shared glycan patterns of plasma proteins. PLoS Negl. Trop. Dis. 2012, 6. Article Number: e1569.
96. Yoshino T.P., Wu X.-J., et al. Circulating Biomphalaria glabrata hemocyte subpopulations possess shared schistosome glycans and receptors capable of binding larval glycoconjugates. Exp. Parasitol. 2013, 133:28-36.
97. Zhang S.M., Adema C.M., et al. Diversification of Ig superfamily genes in an invertebrate. Science 2004, 305:251-254.
98. Zhang S.M., Zeng Y., et al. 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.