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Gilthead seabream (Sparus aurata L.) innate defence against the parasite Enteromyxum leei (Myxozoa)

Published online by Cambridge University Press:  21 September 2005

A. CUESTA
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain
P. MUÑOZ
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain
A. RODRÍGUEZ
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain
I. SALINAS
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain
A. SITJÀ-BOBADILLA
Affiliation:
Instituto de Acuicultura Torre de la Sal (CSIC), 12595 Ribera de Cabanes, Castellón, Spain
P. ÁLVAREZ-PELLITERO
Affiliation:
Instituto de Acuicultura Torre de la Sal (CSIC), 12595 Ribera de Cabanes, Castellón, Spain
M. A. ESTEBAN
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain
J. MESEGUER
Affiliation:
Fish Innate Immune System Group, Department of Cell Biology, Faculty of Biology, University of Murcia, 30100 Murcia, Spain

Abstract

The humoral innate immune response of gilthead seabream (Sparus aurata L.) against the myxozoan Enteromyxum leei has been studied. At 10, 22, 38, 52 and 108 days of cohabitation fish were sampled to examine gut histology and to determine serum innate immune parameters and the mRNA expression of pro-inflammatory cytokines (IL-1β and TNFα) in head-kidney. The parasite was successfully transmitted to 45% of the recipient fish and prevalence reached a maximum (62·5%) at the last sampling time (108 days). Recipient fish started to die after 74 days of cohabitation. In general, alternative complement activity was higher whereas the peroxidase level was lower in recipient fish than in controls. Moreover, IL-1β mRNA expression increased while the TNFα gene expression decreased in recipient fish. These data demonstrate the involvement of complement activity in the defence mechanisms of the gilthead seabream against the myxosporean E. leei. Within the recipient fish group, few differences were observed in the studied immune parameters between E. leei-parasitized and non-parasitized recipient fish. Parasitological and immunological implications of E. leei infections in Mediterranean fish farms are discussed.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Ardelli, B. F. and Woo, P. T. ( 1997). Protective antibodies and anamnestic response in Salvelinus fontinalis to Cryptobia salmositica and innate resistance of Salvelinus namaycush to the hemoflagellate. Journal of Parasitology 83, 943946.CrossRefGoogle Scholar
Athanassopoulou, F., Prapas, T. H. and Rodger, H. ( 1999). Diseases of Puntazzo puntazzo Cuvier in marine aquaculture systems in Greece. Journal of Fish Diseases 22, 215218.CrossRefGoogle Scholar
Bartholomew, J. L., Smith, C. E., Rohovec, J. S. and Fryer, J. L. ( 1989). Characterization of a host response to the myxosporean parasite, Ceratomyxa shasta (Noble), by histology, scanning electron microscopy and immunological techniques. Journal of Fish Diseases 12, 509522.CrossRefGoogle Scholar
Bower, S. M. and Evelyn, T. P. ( 1988). Acquired and innate resistance to the haemoflagellate Cryptobia salmositica in sockeye salmon (Oncorhynchus nerka). Developmental and Comparative Immunology 12, 749760.CrossRefGoogle Scholar
Bower, S. M. and Woo, P. T. ( 1977). Cryptobia catostomi: incubation in plasma of susceptible and refractory fishes. Experimental Parasitology 43, 6368.CrossRefGoogle Scholar
Buchmann, K. ( 1998). Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactilus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195200.CrossRefGoogle Scholar
Buchmann, K. and Nielsen, M. E. ( 1999). Chemoattraction of Ichthyophthirius multifiliis (Ciliophora) to host molecules. International Journal for Parasitology 29, 14151423.CrossRefGoogle Scholar
Buchmann, K., Sigh, J., Nielsen, C. V. and Dalgaard, M. ( 2001). Host responses against the fish parasitizing ciliate Ichthyophthirius multifiliis. Veterinary Parasitology 100, 105116.CrossRefGoogle Scholar
Diamant, A. ( 1992). A new pathogenic histozoic Myxidium (Myxosporea) in cultured gilt-head seabream Sparus aurata L. Bulletin of the European Association of Fish Pathologists 12, 6466.Google Scholar
Diamant, A. ( 1997). Fish-to-fish transmission of a marine myxosporean. Diseases of Aquatic Organisms 30, 99105.CrossRefGoogle Scholar
Diamant, A., Lom, J. and Dyková, I. ( 1994). Myxidium leei n. sp., a pathogenic myxosporean of cultured sea bream Sparus aurata. Diseases of Aquatic Organisms 20, 137141.Google Scholar
Foott, J. S. and Hedrick, R. P. ( 1990). Blood parameters and immune status of rainbow trout with proliferative kidney disease. Journal of Aquatic Animal Health 2, 141148.2.3.CO;2>CrossRefGoogle Scholar
Forward, G. M. and Woo, P. T. ( 1996). An in vitro study on the mechanism of innate immunity in Cryptobia-resistant brook charr (Salvelinus fontinalis) against Cryptobia salmositica. Parasitology Research 82, 238241.CrossRefGoogle Scholar
Furuta, T., Ogawa, K. and Wakabayashi, H. ( 1993). Humoral immune response of carp Cyprinus carpio to Myxobolus artus (Myxozoa: Myxobolidae) infection. Journal of Fish Biology 43, 441450.CrossRefGoogle Scholar
García-Castillo, J., Pelegrin, P., Mulero, V. and Meseguer, J. ( 2002). Molecular cloning and expression analysis of tumor necrosis factor alpha from a marine fish reveal its constitutive expression and ubiquitous nature. Immunogenetics 54, 200207.CrossRefGoogle Scholar
Graves, S. S., Evans, D. L. and Dawe, D. L. ( 1985). Mobilization and activation of nonspecific cytotoxic cells (NCC) in the channel catfish (Ictalurus punctatus) infected with Ichthyophthirius multifiliis. Comparative Immunology, Microbiology and Infectious Diseases 8, 4351.CrossRefGoogle Scholar
Harris, P. D., Soleng, A. and Bakke, T. A. ( 1998). Killing of Gyrodactylus salaries (Platyhelminthes, Monogenea) mediated by host complement. Parasitology 117, 137143.CrossRefGoogle Scholar
Holland, M. C. and Lambris, J. D. ( 2002). The complement system in teleosts. Fish and Shellfish Immunology 12, 399420.CrossRefGoogle Scholar
Holland, J. W., Gould, C. R., Jones, C. S., Noble, L. R. and Secombes, C. J. ( 2003). The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferativa kidney disease (PKD). Parasitology 126, S95S102.Google Scholar
Jones, S. R. M. ( 2001). The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25, 841852.CrossRefGoogle Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J., Longshaw, M., Palenzeula, O., Siddall, M. E. and Xiao, C. ( 2001). Recent advances in our knowledge of the Myxozoa. The Journal of Eukaryotic Microbiology 48, 395413.CrossRefGoogle Scholar
Klebanoff, S. J. ( 1998). Microbicidal mechanisms, oxygen-dependent. In Encyclopedia of Immunology ( ed. Delves, P. J. and Roitt, I. M.), pp. 17131718. Academic Press, London.CrossRef
Le Breton, A. and Marques, A. ( 1995). Occurrence of an histozoic Myxidium infection in two marine cultured species. Puntazzo puntazzo C. and Pagrus major. Bulletin of the European Association of Fish Pathologists 15, 210212.Google Scholar
Li, S. and Woo, P. T. ( 1995). Efficacy of live Cryptobia salmositica vaccine, and the mechanism of protection in vaccinated rainbow trout, Oncorhynchus mykiss, against cryptobiosis. Veterinary Immunology and Immunopathology 48, 343353.CrossRefGoogle Scholar
Lindestrøm, T., Buchmann, K. and Secombes, C. J. ( 2003). Gyrodactylus derjavini infection elicits IL-1beta expression in rainbow trout skin. Fish and Shellfish Immunology 15, 107115.CrossRefGoogle Scholar
Lindestrøm, T., Secombes, C. J. and Buchmann, K. ( 2004). Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Veterinary Immunology and Immunopathology 97, 137148.CrossRefGoogle Scholar
Mehta, M. and Woo, P. T. ( 2002). Acquired cell-mediated protection in rainbow trout, Oncorhynchus mykiss, against the haemoflagellate, Cryptobia salmositica. Parasitology Research 88, 956962.CrossRefGoogle Scholar
Meseguer, J., López-Ruiz, A. and Esteban, M. A. ( 1994). Cytochemical characterization of leucocytes from the seawater teleost, gilthead seabream (Sparus aurata L.). Histochemistry 102, 3744.CrossRefGoogle Scholar
Muñoz, P., Calduch-Giner, J. A., Sitjà-Bobadilla, A., Álvarez-Pellitero, P. and Pérez-Sánchez, J. ( 1998). Modulation of the respiratory burst activity of Mediterranenan sea bass (Dicentrarchus labrax L.) phagocytes by growth hormone and parasitic status. Fish and Shellfish Immunology 8, 2536.Google Scholar
Muñoz, P., Sitjà-Bobadilla, A. and Álvarez-Pellitero, P. ( 2000). Cellular and humoral immune response of European sea bass (Dicentrarchus labrax L.) (Teleostei: Serranidae) immunized with Sphaerospora dicentrarchi (Myxosporea: Bivalvulida). Parasitology 120, 465477.Google Scholar
Nakanishi, Y., Fischer, U., Dijkstra, J. M., Hasegawa, S., Somamoto, T., Okamoto, N. and Ototake, M. ( 2002). Cytotoxic T cell function in fish. Developmental and Comparative Immunology 26, 131139.CrossRefGoogle Scholar
Nielsen, C. V. and Buchmann, K. ( 2000). Prolonged in vitro cultivation of Ichthyophthirius multifiliis using an EPC line as substrate. Diseases of Aquatic Organisms 42, 215219.CrossRefGoogle Scholar
Olabuenaga, S. ( 2000). In vitro effect of rainbow trout (Oncorhynchus mykiss) serum in Tylodelphys sp. (Trematoda, Diplosromatidae) metacercariae. Boletin Chileno de Parasitologia 55, 3945.Google Scholar
Ortuño, J., Esteban, M. A., Mulero, V. and Meseguer, J. ( 1998). Methods for studying the haemolytic, chemoattractant and opsonic activities of seabream (Sparus aurata L.) serum. In Methodology in Fish Diseases Research ( ed. Barnes, A. C., Davidson, G. A., Hiney, M. P. and Mclntosh, D.), pp. 97100. Albion Press, Aberdeen, UK.
Padrós, F., Palenzuela, O., Hispano, C., Tosas, O., Zarza, C., Crespo, S. and Álvarez-Pellitero, P. ( 2001). Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Diseases of Aquatic Organisms 47, 5762.CrossRefGoogle Scholar
Pelegrín, P., García-Castillo, J., Mulero, V. and Meseguer, J. ( 2001). Interleukin-1b isolated from a marine fish reveals up-regulated expression in macrophages following activation with lipopolysaccharide and lymphokines. Cytokine 16, 6772.Google Scholar
Plouffe, D. A. and Belosevic, M. ( 2004). Enzyme treatment of Trypanoplasma danilewskyi (Laveran and Mesnil) increases its susceptibility to lysis by the alternative complement pathway of goldfish, Carassius auratus (L.). Journal of Fish Diseases 27, 277285.CrossRefGoogle Scholar
Quade, M. J. and Roth, J. A. ( 1997). A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Veterinary Immunology and Immunopathology 58, 239248.CrossRefGoogle Scholar
Redondo, M. J., Palenzuela, O., Riaza, A., Macías, A. and Álvarez-Pellitero, P. ( 2002). Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Journal of Parasitology 88, 482488.CrossRefGoogle Scholar
Redondo, M. J., Palenzuela, O. and Álvarez-Pellitero, P. ( 2003). In vitro studies on viability and proliferation of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of cultured turbot Scophthalmus maximus. Diseases of Aquatic Organisms 55, 133144.CrossRefGoogle Scholar
Rodríguez, A., Esteban, M. A. and Meseguer, J. ( 2003). Phagocytosis and peroxidase release by seabream (Sparus aurata L.) leucocytes in response to yeast cells. Anatomical Record 272A, 415423.Google Scholar
Rubio-Godoy, M., Porter, R. and Tinsley, R. C. ( 2004). Evidence of complement-mediated killing of Discocotyle sagittata (Platyhelminthes, Monogenea) oncomiracidia. Fish and Shellfish Immunology 17, 95103.CrossRefGoogle Scholar
Saeij, J. P., de Vries, B. J. and 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, 859874.CrossRefGoogle Scholar
Sakiti, P. N., Tarer, V., Jacquemin, D. and Marques, A. ( 1996). Prèsence en Méditerrané occidentale d'une Myxosporidie histozoïque pathogène dans les élevages de daurade, Sparus aurata L. Annales des Sciences Naturalles, Zoologie, Paris 17, 123127.Google Scholar
Scharsack, J. P., Steinhagen, D., Korting, W., Wagner, B., Leibold, W. and Schuberth, H. J. ( 2004). Some immune parameters in carp Cyprinus carpio susceptible and resistant to the haemoflagellate Trypanoplasma borreli. Diseases of Aquatic Organisms 60, 4148.CrossRefGoogle Scholar
Secombes, C. J., Wang, T., Hong, S., Peddie, S., Crampe, M., Laing, K. J., Cunningham, C. and Zou, J. ( 2001). Cytokines and innate immunity of fish. Developmental and Comparative Immunology 25, 713723.CrossRefGoogle Scholar
Sigh, J., Lindenstrøm, T. and Buchmann, K. ( 2004 a). The parasitic ciliate Ichthyophthirius multifiliis induces expression of immune relevant genes in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 27, 409417.Google Scholar
Sigh, J., Lindenstrøm, T. and Buchmann, K. ( 2004 b). Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophtirius multifiliis. Fish and Shellfish Immunology 17, 7586.Google Scholar
Sitjà-Bobadilla, A., Redondo, M. J., Palenzuela, O., Leyva, M. O., Macías, M. A., Riaza, A., Quiroga, I., Nieto, J. M. and Álvarez-Pellitero, P. ( 2003). Immune response of turbot (Scophthalmus maximus L.) after experimental infection with Enteromyxum scophthlai (Myxozoa). 11th International Conference of the EAFP on Diseases of Fish and Shellfish. Abstract Book, pp: O96, Saint Julians, Malta, Sept. 2003.
Sitjà-Bobadilla, A., Redondo, M. J., Macías, M. A., Ferreiro, I., Riaza, A. and Álvarez-Pellitero, P. ( 2004). Development of immunohistochemistry and enzyme-linked immunosorbent assays for the detection of circulating antibodies against Enteromyxum scophthalmi (Myxozoa) in turbot (Scophthalmus maximus L.). Fish and Shellfish Immunology 17, 335345.CrossRefGoogle Scholar
Thoney, D. A. and Burreson, E. M. ( 1988). Lack of a specific humoral antibody response in Leiostomus xanthurus (Pisces: Sciaenidae) to parasitic copepods and monogeneans. Journal of Parasitology 74, 191193.CrossRefGoogle Scholar
Wehnert, S. D. and Woo, P. T. ( 1980). In vivo and in vitro studies on the specificity of Trypanoplasma salmositica. Journal of Wildlife Diseases 16, 183187.CrossRefGoogle Scholar
Woo, P. T. ( 1996). Protective immune response of fish to parasitic flagellates. Annual Review of Fish Diseases 6, 121131.CrossRefGoogle Scholar
Woo, P. T. ( 2001). Cryptobiosis and its control in North American fishes. International Journal for Parasitology 31, 566574.CrossRefGoogle Scholar
Wood, B. P. and Matthews, R. A. ( 1987). The immune response of the thicklipped grey mullet, Chelon labrosus (Risso, 1826), to metacercarial infections of Cryptocotyle lingua (Creplin, 1825). Journal of Fish Biology 31A, 175183.CrossRefGoogle Scholar
Xu, D., Klesius, K., Shoemaker, C. A. and Evans, J. J. ( 2000). The early development of Ichthyophthirius multifiliis in channel catfish in vitro. Journal of Aquatic Animal Health 12, 290296.2.0.CO;2>CrossRefGoogle Scholar
Xu, D., Klesius, K. and Shelby, R. A. ( 2004). Immune responses and host protection of channel catfish, Ictalurus punctatus, against Ichthyophthirius multifiliis after immunization with live theronts and sonicated trophonts. Journal of Fish Diseases 27, 135141.CrossRefGoogle Scholar
Yaganida, T., Nomura, Y., Kimura, T., Fukuda, Y., Yokoyama, H. and Ogawa, K. ( 2004). Molecular and morphological redescriptions of enteric myxozoans, Enteromyxum leei (formerly Myxidium sp. TP) and Enteromyxum fugu comb.n. (syn. Myxidium fugu) from cultured tiger puffer. Fish Pathology 39, 137143.Google Scholar