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Interaction between the blood fluke, Sanguinicola inermis and humoral components of the immune response of carp, Cyprinus carpio

Published online by Cambridge University Press:  29 April 2005

M. L. ROBERTS ,
J. W. LEWIS ,
G. F. WIEGERTJES  and
D. HOOLE
M. L. ROBERTS
Affiliation:
Centre for Applied Entomology and Parasitology, Huxley Building, School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK
J. W. LEWIS
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
G. F. WIEGERTJES
Affiliation:
Cell Biology and Immunology Group, Wageningen Institute of Animal Sciences, Wageningen University, PO Box 338, 6700AH Wageningen, The Netherlands
D. HOOLE
Affiliation:
Centre for Applied Entomology and Parasitology, Huxley Building, School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK
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Abstract

The effect of Sanguinicola inermis on serum antibody and complement activity in Cyprinus carpio was assessed using an ELISA and haemolytic assays. Possible immune evasion strategies were assessed using immunodetection of host proteins on the surface of the parasite. Carp acclimatized to 20 or 25 °C were infected by exposure to 500 cercariae or injected intraperitoneally with 150 cercariae, and serum monitored over a 63-day period. In cercariae-injected carp, irrespective of time and temperature, a significant increase occurred in complement activity being greatest at 25 °C. In addition, fish exposed to the cercariae of S. inermis and maintained at 20 °C the level of complement activity was significantly higher after 5 weeks compared to controls. At 20 °C intraperitoneal injections of parasites increased serum antibody levels which peaked after 7 days. In contrast, at 25 °C, antibody levels were maintained over 63 days. Exposure of fish to infection did not appear to stimulate antibody production. Immunofluorescence studies revealed ‘host-like’ molecules on the surface of the cercarial body exposed to carp serum and adult flukes obtained directly from the fish or cultured for 24 h in L15 medium. The possible role of ‘host-like’ molecules in immune evasion is discussed and the response at different temperatures is related to infection dynamics.

Keywords

Sanguinicola inermisCyprinus carpioantibodycomplementimmune evasion
Type
Research Article
Information
Parasitology , Volume 131 , Issue 2 , August 2005 , pp. 261 - 271
Copyright
2005 Cambridge University Press

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References

REFERENCES

Aaltonen, T. M., Valtonen, E. T. & Jokinen, E. I. ( 1997). Humoral response of roach (Rutilus rutilus) to digenean Rhipidocotyle fennica infection. Parasitology 114, 285–291.CrossRefGoogle Scholar
Agu, W. E., Farrell, J. P. & Soulsby, E. J. L. ( 1981). Complement increases in experimental Leishmania donovani infection of the golden hamster. International Journal for Parasitology 11, 133–136.CrossRefGoogle Scholar
Ardelli, B. F. & Woo, P. T. K. ( 2002). Experimental Cryptobia salmositica (Kinetoplastida) infections in Atlantic salmon Salmo salar L.: cell-mediated and humoral immune responses against the pathogenic and vaccine strains of the parasite. Journal of Fish Diseases 25, 265–274.Google Scholar
Bortz, B. M., Kenny, G. E., Pauley, G. B., Garcia-Ortigiza, E. & Anderson, D. P. ( 1984). The immune response in immunized and naturally infected rainbow trout (Salmo gairdneri) to Diplostomum spathaceum as detected by the enzyme-linked immunosorbent assay (ELISA). Developmental and Comparative Immunology 8, 813–822.CrossRefGoogle Scholar
Bower, S. M. & Evelyn, T. P. T. ( 1988). Acquired and innate resistance to the haemoflagellate Crytobia salmositica in sockeye salmon Oncorhynchus nerka. Developmental and Comparative Immunology 12, 749–760.CrossRefGoogle Scholar
Bower, S. M. & Woo, P. T. K. ( 1977). Crytobia catostomi: incubation in plasma of susceptible and refractory fishes. Experimental Parasitology 43, 63–68.CrossRefGoogle Scholar
Buchmann, K. ( 1998). Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195–200.CrossRefGoogle Scholar
Buchmann, K., Lindenstrøm, T. & Sigh, J. ( 1999). Partial cross protection against Ichthyophthirius multifiliis in Gyrodactylus derjavini immunized rainbow trout. Journal of Helminthology 73, 189–195.CrossRefGoogle Scholar
Carlson, R. E., Baker, E. P. & Fuller, R. E. ( 1995). Immunological assessment of hybrid striped bass at three culture temperatures. Fish and Shellfish Immunology 5, 359–373.CrossRefGoogle Scholar
Clark, T. G. & Dickerson, H. W. ( 1997). Antibody-mediated effects on parasite behavior: evidence of a novel mechanism of immunity against a parasitic protist. Parasitology Today 13, 477–480.CrossRefGoogle Scholar
Cobb, C. S., Levy, M. G. & Noga, E. J. ( 1998). Acquired immunity to amyloodiniosis is associated with an antibody response. Diseases of Aquatic Organisms 34, 125–133.CrossRefGoogle Scholar
Coscia, M. R. & Oreste, U. ( 1998). Presence of antibodies specific for proteins of Contracaecum osculatum (Rudolphi 1908) in plasma of several Antarctic teleosts. Fish and Shellfish Immunology 8, 295–302.CrossRefGoogle Scholar
Coscia, M. R. & Oreste, U. ( 2000). Plasma and bile antibodies of the teleost Trematomus bernacchi specific for the nematode Pseudoterranova decipiens. Diseases of Aquatic Organisms 41, 37–42.CrossRefGoogle Scholar
Fishelson, Z. ( 1989). Complement and parasitic trematodes. Parasitology Today 5, 19–25.CrossRefGoogle Scholar
Grayson, T. H., John, R. J., Wadsworth, S., Greaves, K., Cox, D., Roper, J., Wrathmell, A. B., Gilpin, M. L. & Harris, J. E. ( 1995). Immunization of Atlantic salmon against the salmon louse: identification of antigens and effects on louse fecundity. Journal of Fish Biology 47, 85–94.CrossRefGoogle Scholar
Hoglund, J. & Thuvander, A. ( 1990). Indications of non-specific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 91–97.CrossRefGoogle Scholar
Hoole, D. ( 1997). The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39, 219–225.Google Scholar
Hoole, D. & Arme, C. ( 1983). Ultrastructural studies on the cellular response of fish hosts following experimental infection with the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). Parasitology 87, 139–149.CrossRefGoogle Scholar
Hoole, D. & Arme, C. ( 1986). The role of serum in leucocyte adherence to the plerocercoid of Ligula intestinalis (Cestoda: Pseudophyllidea). Parasitology 92, 413–424.CrossRefGoogle Scholar
Hoole, D., Lewis, J. W., Schuwerack, P. M. M., Chakravarthy, C., Shrive, A. K., Greenhough, T. J. & Cartwright, J. R. ( 2003). Inflammatory interactions in fish exposed to pollutants and parasites: a role for apoptosis and C-reactive protein. Parasitology 126, S71–S85.CrossRefGoogle Scholar
Jones, S. R. M. & Woo, P. T. K. ( 1987). The immune response of rainbow trout Salmo gairdneri Richardson, to the haemoflagellate, Cryptobia salmositica Katz, 1951. Journal of Fish Diseases 10, 395–402.CrossRefGoogle Scholar
Kar, S. K., Mania, J., Baldwin, C. I. & Denham, D. A. ( 1993). The sheath of the microfilaria of Wuchereria bancrofti has albumin and immunoglobulin on its surface. Parasite Immunology 15, 297–300.CrossRefGoogle Scholar
Kato, T., Nakao, M., Mutsuro, J., Zarkadis, I. K. & Yano, T. ( 2003). The complement component C5 of the common carp (Cyprinus carpio): cDNA cloning of two distinct isotypes that differ in a functional site. Immunogenetics 54, 807–815.Google Scholar
Kennedy, C. R. & Walker, P. J. ( 1969). Evidence for an immune response in dace, Leuciscus leuciscus, to infection by the cestode Caryophyllaeus laticeps. Journal of Parasitology 55, 579–582.CrossRefGoogle Scholar
Kirk, R. S. & Lewis, J. W. ( 1992). The laboratory maintenance of Sanguinicola inermis Plehn, 1905 (Digenea: Sanguinicolidae). Parasitology 104, 121–127.CrossRefGoogle Scholar
Kirk, R. S. & Lewis, J. W. ( 1993). The life-cycle and morphology of Sanguinicola inermis Plehn, 1905 (Digenea: Sanguinicolidae). Systematic Parasitology 25, 125–133.CrossRefGoogle Scholar
Koumans-Van Diepen, J. C. E., Egberts, E., Peixoto, B. R., Taverne, N. & Rombout, J. H. W. M. ( 1995). B cell and immunoglobulin heterogeneity in carp (Cyprinus carpio L.); an immuno(cyto)chemical study. Developmental and Comparative Immunology 19, 97–108.CrossRefGoogle Scholar
Lee, R. S. ( 1990). The development of Sanguinicola inermis Plehn, 1905 (Digenea: Sanguinicolidae) in the common carp Cyprinus carpio L. Ph.D. thesis, University of London.
Leid, R. W. ( 1988). Parasites and complement. Advances in Parasitology 27: 131–168.Google Scholar
Machado, A. J., Gazzinelli, G., Pellegrino, J. & Dias Da Silva, W. ( 1975). Schistosoma mansoni: The role of complement C3-activating system in the cercariacidal action of normal serum. Experimental Parasitology 38, 20–29.CrossRefGoogle Scholar
Marikovsky, M., Levi-Schaffer, F., Arnon, R. & Fishelson, Z. ( 1986). Schistosoma mansoni: killing of transformed schistosomula by the alternative pathway of human complement. Experimental Parasitology 61, 86–94.CrossRefGoogle Scholar
Matsuyama, H., Tanaka, K., Nakao, M. & Yano, T. ( 1988). Characterization of the alternative complement pathway in carp. Developmental and Comparative Immunology 12, 403–408.CrossRefGoogle Scholar
Nakao, M., Fujiki, K., Konodo, M. & Yano, T. ( 2003 a). Detection of complement receptors on head kidney phagocytes of common carp Cyprinus carpio. Fisheries Science 65, 929–935.Google Scholar
Nakao, M., Hisamatsu, S., Nakahara, M., Kato, Y., Smith, S. L. & Yano, T. ( 2003 b). Molecular cloning of the complement regulatory factor I isotypes from common carp (Cyprinus carpio). Immunogenetics 54, 801–806.Google Scholar
Nakao, M., Miura, C., Itoh, S., Nakahara, M., Okumura, K., Mutsuro, J. & Yano, T. ( 2004). A complement C3 fragment equivalent to mammalian C3d from the common carp (Cyprinus carpio): generation in serum after activation of the alternative pathway and detection of its receptor on the lymphocyte surface. Fish and Shellfish Immunology 16, 139–149.CrossRefGoogle Scholar
Nakao, M., Mutsuro, J., Nakahara, M., Kato, Y. & Yano, T. ( 2003 c). Expansion of genes encoding complement components in bony fish: biological implications of the complement diversity. Development and Comparative Immunology 27, 749–762.Google Scholar
Nakao, M., Uemura, T. & Yano, T. ( 2003). Characterisation of the soluble membrane attack complex (SMAC) of carp (Cyprinus carpio) complement. Journal of the Faculty of Agricultural Kyushu University 48, 127–134.Google Scholar
Nie, P. & Hoole, D. ( 1999). Antibody response of carp, Cyprinus carpio to the cestode, Bothriocephalus acheilognathi. Parasitology 118, 635–639.CrossRefGoogle Scholar
Premaratne, U. N., Parkhouse, R. M. E. & Denham, D. A. ( 1989). Microfilariae of Brugia pahangi in the blood of cats have variable levels of feline IgG on their sheaths. Journal of Parasitology 75, 320–322.CrossRefGoogle Scholar
Richards, D. T., Hoole, D., Lewis, J. W., Ewens, E. & Arme, C. ( 1994 a). Ultrastructural observations on the cellular response of carp, Cyprinus carpio L., to eggs of the blood fluke Sanguinicola inermis Plehn, 1905 (Trematoda: Sanguinicolidae). Journal of Fish Diseases 17, 439–446.Google Scholar
Richards, D. T., Hoole, D., Lewis, J. W., Ewens, E. & Arme, C. ( 1994 b). Changes in the cellular composition of the spleen and pronephros of carp (Cyprinus carpio L.) to eggs of the blood fluke Sanguinicola inermis (Trematoda: Sanguinicolidae). Diseases of Aquatic Organisms 19, 173–179.Google Scholar
Richards, D. T., Hoole, D., Lewis, J. W., Ewens, E. & Arme, C. ( 1996 a). Stimulation of carp Cyprinus carpio lymphocytes in vitro by the blood fluke Sanguinicola inermis (Trematoda: Sanguinicolidae). Diseases of Aquatic Organisms 25, 87–93.Google Scholar
Richards, D. T., Hoole, D., Lewis, J. W., Ewens, E. & Arme, C. ( 1996 b). In vitro polarization of carp leucocytes in response to the blood fluke Sanguinicola inermis Plehn, 1905 (Trematoda: Sanguinicolidae). Parasitology 112, 509–513.Google Scholar
Richards, D. T., Hoole, D., Lewis, J. W., Ewens, E. & Arme, C. ( 1996 c). Adherence of carp leucocytes to adults and cercariae of the blood fluke Sanguinicola inermis. Journal of Helminthology 70, 63–67.Google Scholar
Rijkers, G. T., Frederix-Wolters, E. M. H. & Van Muiswinkel, W. B. ( 1980). The immune system of cyprinid fish. Kinetics and temperature dependence of antibody-producing cells in carp (Cyprinus carpio). Immunology 41, 91–97.Google Scholar
Saeij, J. P. J., De Vries, B. J. & Wiegertjes, G. F. ( 2003). The immune response of carp to Trypanoplasma borreli: kinetics of immune gene expression and polyclonal lymphocyte activation. Developmental and Comparative Immunology 27, 859–874.CrossRefGoogle Scholar
Sakai, D. K. ( 1983). Lytic and bactericidal properties of salmonid sera. Journal of Fish Biology 23, 457–466.CrossRefGoogle Scholar
Sakai, D. K. ( 1992). Repertoire of complement in immunological defence mechanisms. Annual Review of Fish Diseases 2, 223–247.CrossRefGoogle Scholar
Santoro, F., Lachmann, P. J., Capron, A. & Capron, M. ( 1979). Activation of complement by Schistosoma mansoni- schistosomula: Killing of parasites by the alternative pathway and requirement of IgG for classical pathway activation. Journal of Immunology 123, 1551–1557.Google Scholar
Santoro, F., Prata, A., Castro, C. C. & Capron, A. ( 1980). Circulating antigens, immune complexes and C3d levels in human schistosomiasis: relationship with Schistosoma mansoni egg output. Clinical and Experimental Immunology 42, 219–225.Google Scholar
Schuwerack, P.-M. M., Lewis, J. W., Hoole, D. & Morley, N. J. ( 2001). Ammonia-induced cellular and immunological changes in juvenile Cyprinus carpio infected with the blood fluke Sanguinicola inermis. Parasitology 122, 339–345.CrossRefGoogle Scholar
Schuwerack, P.-M. M., Lewis, J. W. & Hoole, D. ( 2003). Cadmium-induced cellular and immunological responses in Cyprinus carpio infected with the blood parasite Sanguinicola inermis. Journal of Helminthology 77, 341–350.CrossRefGoogle Scholar
Secombes, C. J., Van Groningen, J. J. M. & Egberts, E. ( 1983). Separation of lymphocyte subpopulations in carp Cyprinus carpio L. by monoclonal antibodies: Immunohistochemical studies. Immunology 48, 165–175.Google Scholar
Secombes, C. J., White, A., Fletcher, T. C. & Houlihan, D. F. ( 1991). The development of an ELISPOT assay to quantify total and specific antibody-secreting cells in the dab Limanda limanda. Fish and Shellfish Immunology 1, 87–97.CrossRefGoogle Scholar
Sharp, G. J. E., Pike, A. W. & Secombes, C. J. ( 1989). The immune response of wild trout, Salmo gairdneri Richardson, to naturally acquired plerocercoid infections of Diphyllobothrium dendriticum (Nitzsch, 1824), and D. ditremum (Creplin, 1825). Journal of Fish Biology 35, 781–794.Google Scholar
Sher, A., Hall, B. F. & Vadas, M. A. ( 1978). Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. Journal of Experimental Medicine 148, 46–50.CrossRefGoogle Scholar
Sommerville, C. & Iqbal, N. A. M. ( 1991). The process of infection, migration, growth and development of Sanguinicola inermis Plehn 1905 (Digenea: Sanguincolidae) in carp, Cyprinus carpio L. Journal of Fish Diseases 14, 211–219.CrossRefGoogle Scholar
Taylor, M. J. & Hoole, D. ( 1993). Ligula intestinalis (L.) (Cestoda: Pseudophyllidea): polarization of cyprinid leucocytes as an indicator of host- and parasite-derived chemoattractants. Parasitology 107, 433–440.Google Scholar
Thomas, P. T. & Woo, P. T. K. ( 1989). Complement activity in Salmo gairdneri Richardson infected with Cryptobia salmositica (Sacromastigophora: Kinetoplastida) and its relationship to the anaemia in cryptobiosis. Journal of Fish Diseases 12, 395–397.CrossRefGoogle Scholar
Wehnert, S. D. & Woo, P. T. K. ( 1980). In vivo and in vitro studies on the host specificity of Trypanoplasma salmositica. Journal of Wildlife Diseases 16, 183–187.CrossRefGoogle Scholar
Whyte, S. K., Chappell, L. H. & Secombes, C. J. ( 1989) Cytotoxic reactions of rainbow trout, Salmo gairdneri Richardson, macrophages for larvae of eye fluke Diplostomum spathaceum (Digenea). Journal of Fish Biology 35, 333–345.CrossRefGoogle Scholar
Whyte, S. K., Chappell, L. H. & Secombes, C. J. ( 1990) Protection of rainbow trout, Oncorhynchus mykiss (Richardson), against Diplostomum spathaceum (Digenea): the role of specific antibody and activated macrophages. Journal of Fish Diseases 13, 281–291.CrossRefGoogle Scholar
Williams, M. A. & Hoole, D. ( 1995). Immunolabelling of fish host molecules on the tegumental surface of Ligula intestinalis (Cestoda: Pseudophyllidea). International Journal for Parasitology 25, 249–256.CrossRefGoogle Scholar
Xu, D. H. & Klesius, P. H. ( 2003) Protective effect of cutaneous antibody produced by channel catfish, Ictalurus punctatus (Rafinesque), immune to Ichthyophthirius multifiliis Fouquet on cohabited non-immune catfish. Journal of Fish Diseases 26, 287–291.CrossRefGoogle Scholar
Yano, T. ( 1992) Assays of haemolytic complement activity. In Techniques in Fish Immunology (ed. Stolen, J. S., Fletcher, T. C., Anderson, D. P., Kaattari, S. L. & Rowley, A. F.), pp. 131–141. SOS Publications, Fair Haven, USA.