Excretory products of the cestode, Schistocephalus solidus, modulate invitro responses of leukocytes from its specific host, the three-spined stickleback (Gasterosteus aculeatus)

Fish and Shellfish Immunology

Volumn 35, Issue 6, 2013, Pages 1779-1787

  Scharsack, Jörn Peter ^a   Gossens, Anabel ^a   Franke, Frederik ^a   Kurtz, Joachim ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

FSC; Gasterosteus aculeatus; HKL; Invitro leukocyte responses; Parasite excretory secretory products; Parasite immune manipulation; Schistocephalus solidus; SSCM

Indexed keywords

CESTODA; GASTEROSTEUS ACULEATUS; SCHISTOCEPHALUS SOLIDUS; VERMES;

ANIMAL; ANIMAL DISEASE; ARTICLE; CESTODE; CESTODIASIS; FISH DISEASE; FLOW CYTOMETRY; FORWARD SCATTERED LIGHT; FSC; GASTEROSTEUS ACULEATUS; GEOGRAPHY; GERMANY; HEAD KIDNEY; HEAD KIDNEY LEUKOCYTES; HKL; IMMUNOLOGY; IN VITRO LEUKOCYTE RESPONSES; LEUKOCYTE; METABOLISM; NORWAY; PARASITE EXCRETORY/SECRETORY PRODUCTS; PARASITE IMMUNE MANIPULATION; PARASITOLOGY; PHYSIOLOGY; RESPIRATORY BURST; SCHISTOCEPHALUS SOLIDUS; SCHISTOCEPHALUS SOLIDUS CONDITIONED MEDIUM; SMEGMAMORPHA; SPAIN; SSCM; TIME; UPREGULATION;

FORWARD SCATTERED LIGHT; FSC; GASTEROSTEUS ACULEATUS; HEAD KIDNEY LEUKOCYTES; HKL; IN VITRO LEUKOCYTE RESPONSES; PARASITE EXCRETORY/SECRETORY PRODUCTS; PARASITE IMMUNE MANIPULATION; SCHISTOCEPHALUS SOLIDUS; SCHISTOCEPHALUS SOLIDUS CONDITIONED MEDIUM; SSCM;

ANIMALS; CESTODA; CESTODE INFECTIONS; FISH DISEASES; FLOW CYTOMETRY; GEOGRAPHY; GERMANY; HEAD KIDNEY; LEUKOCYTES; NORWAY; RESPIRATORY BURST; SMEGMAMORPHA; SPAIN; TIME FACTORS; UP-REGULATION;

EID: 84888431993     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.08.029     Document Type: Article

References (51)

1. Scholz T. Parasites in cultured and feral fish. Vet Parasitol 1999, 84:317-335.
2. Sures B. How parasitism and pollution affect the physiological homeostasis of aquatic hosts. JHelminthol 2006, 80:151-157.
3. Hoole D., Arme C. Ultrastructural studies on the cellular response of fish hosts following experimental infection with the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidae). Parasitol 1983, 87:139-149.
4. Taylor M.J., Hoole D. Ligula intestinalis (L.) (Cestoda: Pseudophyllidea): polarization of cyprinid leucocytes as an indicator of host- and parasite-derived chemoattractants. Parasitol 1993, 107:433-440.
5. Taylor M.J., Hoole D. The chemiluminescence of cyprinid leucocytes in response to zymosan and extracts of Ligula intestinalis (Cestoda). Fish Shellfish Immunol 1995, 5:191-198.
6. Nie P., Hoole D. Effects of Bothriocephalus acheilognathi on the polarization response of pronephric leucocytes of carp, Cyprinus carpio. JHelminthol 2000, 74:253-257.
7. Sharp G.J., Pike A.W., Secombes C.J. Sequential development of the immune response in rainbow trout [Oncorhynchus mykiss (Walbaum, 1792)] to experimental plerocercoid infections of Diphyllobothrium dendriticum (Nitzsch, 1824). Parasitol 1992, 104:169-178.
8. Whyte S.K., Chappell L.H., Secombes C.J. Protection of rainbow trout (Salmo gaidneri) against Diplostomum spathaceum (Digenea): the role of specific antibody and activated macrophages. JFish Dis 1990, 13:281-291.
9. Secombes C.J., Fletcher T.C. The role of phagocytes in the protective mechanisms of fish. Ann Rev Fish Dis 1992, 2:53-71.
10. Secombes C.J., Chappell L.H. Fish immune responses to experimental and natural infection with helminth parasites. Ann Rev Fish Dis 1996, 6:167-177.
11. Scharsack J.P., Kalbe M., Derner R., Kurtz J., Milinski M. Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Dis Aquat Org 2004, 59:141-150.
12. Whyte S.K., Chappell L.H., Secombes C.J. Cytotoxic reactions of rainbow trout, Salmo gaidneri Richardson, macrophages for larvae of the eye fluke Diplostomum spathaceum (Digenea). JFish Biol 1989, 35:333-345.
13. Buchman K. Fish immune responses against endoparasitic nematodes - experimental models. JFish Dis 2012, 35:623-635.
14. Takizawa F., Araki K., Kobayashi I., Moritomo T., Ototake M., Nakanishi T. Molecular cloning and expression analysis of T-bet in ginbuna crucian carp (Carassius auratus langsdorfii). Mol Immunol 2008, 45:127-136.
15. Takizawa F., Mizunaga Y., Araki K., Moritomo T., Ototake M., Nakanishi T. GATA3 mRNA in ginbuna crucian carp (Carassius auratus langsdorfii): cDNA cloning, splice variants and expression analysis. Dev Comp Immunol 2008, 32:898-907.
16. Barber I., Scharsack J.P. The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitol 2010, 137:411-424.
17. Carter V., Pierce R., Dufour S., Arme C., Hoole D. The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 2005, 130:939-945.
18. Hoole D., Arme C. Ultrastructural studies on the cellular response of roach, Rutilus rutilus L., to the plerocercoid larva of the pseudophyllidean cestode, Ligula intestinalis. JFish Dis 1982, 5:131-144.
19. Sitja-Bobadilla A. Living of a fish: a trade-off between parasites and the immune system. Fish Shellfish Immunol 2008, 25:358-372.
20. Kutyrev I.A., Pronin N.M., Dugarov Z.N. Composition of leucocytes of the head kidney of the crucian carp (Carassius auratus gibelio, Cypriniformes: Cyprinidae) as affected by invasion of cestode Digramma interrupta (Cestoda; Pseudophyllidea). Biol Bullet 2011, 38:653-657.
21. Braten T. Host specificity in Schistocephalus solidus. Parasitology 1966, 56:657-664.
22. Milinski M. Parasites determine a predators optimal feeding strategy. Behav Ecol Sociobiol 1984, 15:35-37.
23. Milinski M. Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus) under competition for food. Behav 1985, 93:203-216.
24. Godin J.J., Sproul C.D. Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Canad J Zool 1988, 66:2360-2367.
25. Barber I., Huntingford F. The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behav 1995, 132:1223-1240.
26. Orr T.S.C., Hopkins C.A., Charles G.H. Host specificity and rejection of Schistocephalus solidus. Parasitol 1969, 59:683-690.
27. Hammerschmidt K., Kurtz J. Schistocephalus solidus: establishment of tapeworms in sticklebacks - fast food or fast lane?. Exp Parasitol 2007, 116:142-149.
28. Hammerschmidt K., Kurtz J. Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. Int J Parasitol 2005, 35:1499-1507.
29. Scharsack J.P., Koch K., Hammerschmidt K. Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proc R Soc Lond B 2007, 274:3151-3158.
30. Wedekind C., Little T.J. The clearance of hidden cestode infection triggered by an independent activation of host defense in a teleost fish. JParasitol 2004, 90:1329-1331.
31. Jäger I., Schjørring S. Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evol 2006, 60:616-622.
32. Kurtz J., Kalbe M., Aeschlimann P.B., Haberli M.A., Wegner K.M., Reusch T.B.H., et al. Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond B 2004, 271:197-204.
33. Prieto M.H., Fernandez-Lopez J.C., Gonzales R.A., Salan E.S.M. Geographical and temporal FA variation in threespine stickleback populations from Galicia (NW Spain). Evol Ecol 2005, 19:517-532.
34. Lüscher A., Milinski M. Simultaneous hermaphrodites reproducing in pairs self-fertilize some of their eggs: an experimental test of predictions of mixed-mating and Hermaphrodite's Dilemma theory. JEvol Biol 2003, 16:1030-1037.
35. Wedekind C. The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitol 1997, 115:317-324.
36. Tierney J.F., Crompton D.W.T. Infectivity of plerocercoids of Schistocephalus solidus (Cestoda, Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. JParasitol 1992, 78:1049-1054.
37. Pechhold K., Pohl T., Kabelitz D. Rapid quantification of lymphocyte subsets in heterogeneous cell populations by flow-cytometry. Cytom 1994, 16:152-159.
38. Scharsack J.P., Steinhagen D., Körting W., Leibold W., Schuberth H.J. Flow cytometric analysis of proliferative responses of carp (Cyprinus carpio L.) peripheral blood leukocytes to mitogens and to the hemoflagellate Trypanoplasma borreli. Dis Aquat Org 2000, 41:203-210.
39. Hewitson J.P., Granger J.R., Maizels R.M. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009, 167:1-11.
40. Magnadottir B. Innate immunity of fish (overview). Fish Shellfish Immunol 2006, 20:137-151.
41. Jefferies J.R., Turner R.J., Barrett J. Effect of Fasciola hepatica excretory-secretory products on the metabolic burst of sheep and human neutrophils. Int J Parasitol 1997, 27:1025-1029.
42. Salzar-Calderon M., Martin-Alonso J.M., Ruiz De Eguino A.D., Casais R., Marin M.S., Parra F. Fasciola hepatica: heterologous expression and functional characterization of a thioredoxin peroxidase. Exp Parasitol 2000, 95:63-70.
43. Gourbal B.E.F., Guillou F., Mitta G., Sibille P., Theron A., Pointer J., et al. Excretory-secretory products of larval Fasciola hepatica investigated using a two-dimensional proteomic approach. Mol Biochem Parasitol 2008, 161:63-66.
44. Overli O., Pall M., Borg B., Jobling M., Winberg S. Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proc R Soc Lond B 2001, 268:1411-1415.
45. Castro R., Bernard D., Lefranc M.P., Six A., Benmansour A., Boudinot P. Tcell diversity and TcR repertoires in teleost fish. Fish Shellfish Immunol 2011, 31:644-654.
46. Toda H., Saito Y., Koike T., Takizawa F., Araki K., Yabu T., et al. Conservation of characteristics and functions of CD4 positive lymphocytes in a teleost fish. Dev Comp Immunol 2011, 35:650-660.
47. Williams M.A., Hoole D. Immunolabelling of fish host molecules on the tegumental surface of Ligula intestinalis (Cestoda: Ppseudophyllidea). Int J Parasitol 1995, 25:249-256.
48. Hoole D., Arme C. The invitro culture and tegumental dynamics of the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). Int J Parasitol 1985, 15:609-615.
49. Kaltz O., Shykoff J. Local adaptation in host-parasite systems. Hered 1998, 81:361-370.
50. Francova K., Ondrackova M. Host-parasite interactions in sympatric and allopatric populations of European bitterling. Parasitol Res 2011, 109:801-808.
51. Scharsack J.P., Kalbe M., Harrod C., Rauch G. Habitat specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proc R Soc Lond B 2007, 274:1523-1532.