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Modulation of leukocytic populations of gilthead sea bream (Sparus aurata) by the intestinal parasite Enteromyxum leei (Myxozoa: Myxosporea)

Published online by Cambridge University Press:  07 November 2013

ITZIAR ESTENSORO*
Affiliation:
Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS-CSIC), 12595 Ribera de Cabanes, Castellón, Spain
IVÁN MULERO
Affiliation:
Department of Cell Biology and Histology, Faculty of Biology, University of Murcia (UM), 30100 Murcia, Spain
MARÍA J. REDONDO
Affiliation:
Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS-CSIC), 12595 Ribera de Cabanes, Castellón, Spain
PILAR ÁLVAREZ-PELLITERO
Affiliation:
Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS-CSIC), 12595 Ribera de Cabanes, Castellón, Spain
VICTORIANO MULERO
Affiliation:
Department of Cell Biology and Histology, Faculty of Biology, University of Murcia (UM), 30100 Murcia, Spain
ARIADNA SITJÀ-BOBADILLA
Affiliation:
Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS-CSIC), 12595 Ribera de Cabanes, Castellón, Spain
*
*Corresponding author: Instituto de Acuicultura Torre de la Sal, Consejo Superior de Investigaciones Científicas (IATS-CSIC), 12595 Ribera de Cabanes, Castellón, Spain. E-mail: [email protected]

Summary

The cellular mucosal and systemic effectors of gilthead sea bream (GSB) (Sparus aurata) involved in the acute immune response to the intestinal parasite Enteromyxum leei were studied in fish experimentally infected by the anal route. In the intestinal inflammatory infiltrates and in lymphohaematopoietic organs (head kidney and spleen) of parasitized fish, the number of plasma cells, B cells (IgM immunoreactive) and mast cells (histamine immunoreactive) were significantly higher, whereas the number of acidophilic granulocytes (G7 immunoreactive) decreased, compared with non-parasitized and unexposed fish. These differences were stronger at the posterior intestine, the main target of the parasite, and no differences were found in the thymus. In non-parasitized GSB, the percentage of splenic surface occupied by melanomacrophage centres was significantly higher. These results suggest that the cellular response of GSB to E. leei includes proliferation of leukocytes in lymphohaematopoietic organs and recruitment into intestines via blood circulation involving elements of innate and adaptive immunity. Acidophilic granulocytes and mast cells presented opposite patterns of response to the parasite infection, with an overall depletion of the former and an increased amount of the latter. Some differences between both cell types were also detected in regard to their granule density and cell morphology.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Agius, C. and Roberts, R. J. (2003). Melano-macrophage centres and their role in fish pathology. Journal of Fish Diseases 26, 499509. doi: 10.1046/j.1365-2761.2003.00485.x. CrossRefGoogle ScholarPubMed
Águila, S., Castillo-Briceno, P., Sánchez, M., Cabas, I., García-Alcázar, A., Meseguer, J., Mulero, V. and García-Ayala, A. (2013). Specific and non-overlapping functions of testosterone and 11-ketotestosterone in the regulation of professional phagocyte responses in the teleost fish gilthead sea bream. Molecular Immunology 53, 218226. doi: 10.1016/j.molimm.2012.08.002. Google Scholar
Álvarez-Pellitero, P. (2008). Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Veterinary Immunology and Immunopathology 126, 171198.CrossRefGoogle ScholarPubMed
Álvarez-Pellitero, P. (2011). Mucosal Intestinal Immunity and Response to Parasite Infections in Ectothermic Vertebrates. Nova Science Publishers, Haupage, NY, USA.Google Scholar
Álvarez-Pellitero, P., Palenzuela, O. and Sitjà-Bobadilla, A. (2008). Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitology International 57, 110120.Google Scholar
Bermúdez, R., Vigliano, F., Marcaccini, A., Sitjà-Bobadilla, A., Quiroga, M. I. and Nieto, J. M. (2006). Response of Ig-positive cells to Enteromyxum scophthalmi (Myxozoa) experimental infection in turbot, Scophthalmus maximus (L.): a histopathological and immunohistochemical study. Fish and Shellfish Immunology 21, 501512.CrossRefGoogle ScholarPubMed
Bowden, T. J., Cook, P. and Rombout, J. (2005). Development and function of the thymus in teleosts. Fish and Shellfish Immunology 19, 413427. doi: 10.1016/j.fsi.2005.02.003. Google Scholar
Cabas, I., Liarte, S., Garcia-Alcazar, A., Meseguer, J., Mulero, V. and García-Ayala, A. (2012). 17 alpha-Ethynylestradiol alters the immune response of the teleost gilthead sea bream (Sparus aurata L.) both in vivo and in vitro . Developmental and Comparative Immunology 36, 547556. doi: 10.1016/j.dci.2011.09.011. Google Scholar
Corrales, J., Mulero, I., Mulero, V. and Noga, E. J. (2010). Detection of antimicrobial peptides related to piscidin 4 in important aquacultured fish. Developmental and Comparative Immunology 34, 331343. doi: http://dx.doi.org/10.1016/j.dci.2009.11.004.Google Scholar
Couso, N., Castro, R., Noya, M., Obach, A. and Lamas, J. (2001). Location of superoxide production sites in turbot neutrophils and gilthead sea bream acidophilic granulocytes during phagocytosis of glucan particles. Developmental and Comparative Immunology 25, 607618.CrossRefGoogle ScholarPubMed
Criscitiello, M. F. and De Figueiredo, P. (2013). Fifty shades of immune defense. PLoS Pathogens 9, doi: 10.1371/journal.ppat.1003110. Google Scholar
Cuadrado, M. (2009). Enteromixosi produïda per Enteromyxum leei (Diamant, Lom i Dyková, 1994) en espàrids d'interès comercial del Mediterrani. Ph.D. thesis. Departament de Biologia Animal, de Biologia Vegetal i d'Ecologia, Facultad de Cienciès; Universitat Autònoma de Barcelona, Barcelona.Google Scholar
Cuadrado, M., Marques, A., Diamant, A., Sitjà-Bobadilla, A., Palenzuela, O., Álvarez-Pellitero, P., Padrós, F. and Crespo, S. (2008). Ultrastructure of Enteromyxum leei (Diamant, Lom, & Dyková, 1994) (Myxozoa), an enteric parasite infecting gilthead sea bream (Sparus aurata) and sharpsnout sea bream (Diplodus puntazzo). Journal of Eukaryotic Microbiology 55, 178184. doi: 10.1111/j.1550-7408.2008.00325.x. CrossRefGoogle ScholarPubMed
Cuesta, A., Esteban, M. A. and Meseguer, J. (2005). Molecular characterization of the nonspecific cytotoxic cell receptor (NCCRP-1) demonstrates gilthead sea bream NCC heterogeneity. Developmental and Comparative Immunology 29, 637650. doi: 10.1016/j.dci.2004.11.003. Google Scholar
Cuesta, A., Esteban, M. A. and Meseguer, J. (2006 a). Cloning, distribution and up-regulation of the teleost fish MHC class II alpha suggests a role for granulocytes as antigen-presenting cells. Molecular Immunology 43, 12751285. doi: 10.1016/j.molimm.2005.07.004. CrossRefGoogle ScholarPubMed
Cuesta, A., Muñoz, P., Rodríguez, A., Salinas, I., Sitjà-Bobadilla, A., Álvarez-Pellitero, P., Esteban, M. A. and Meseguer, J. (2006 b). Gilthead sea bream (Sparus aurata L.) innate defence against the parasite Enteromyxum leei (Myxozoa). Parasitology 132, 95104.Google Scholar
Cuesta, A., Salinas, I., Rodríguez, A., Muñoz, P., Sitjà-Bobadilla, A., Álvarez-Pellitero, P., Meseguer, J. and Esteban, M. Á. (2006 c). Cell-mediated cytotoxicity is the main innate immune mechanism involved in the cellular defence of gilthead sea bream (Teleostei: Sparidae) against Enteromyxum leei (Myxozoa). Parasite Immunology 28, 657665. doi: 10.1111/j.1365-3024.2006.00905.x. Google Scholar
Cuesta, A., Cerezuela, R., Esteban, M. A. and Meseguer, J. (2008). In vivo actions of melatonin on the innate immune parameters in the teleost fish gilthead sea bream. Journal of Pineal Research 45, 7078. doi: 10.1111/j.1600-079X.2008.00557.x. CrossRefGoogle Scholar
Chaves-Pozo, E., Pelegrin, P., García-Castillo, J., García-Ayala, A., Mulero, V. and Meseguer, J. (2004). Acidophilic granulocytes of the marine fish gilthead sea bream (Sparus aurata L.) produce interleukin-1 beta following infection with Vibrio anguillarum . Cell and Tissue Research 316, 189195. doi: 10.1007/s00441-004-0875-9. CrossRefGoogle ScholarPubMed
Chaves-Pozo, E., Muñoz, P., López-Muñoz, A., Pelegrin, P., Ayala, A. G., Mulero, V. and Meseguer, J. (2005). Early innate immune response and redistribution of inflammatory cells in the bony fish gilthead sea bream experimentally infected with Vibrio anguillarum . Cell and Tissue Research 320, 6168.CrossRefGoogle ScholarPubMed
Chaves-Pozo, E., Guardiola, F. A., Meseguer, J., Esteban, M. A. and Cuesta, A. (2012). Nodavirus infection induces a great innate cell-mediated cytotoxic activity in resistant, gilthead sea bream, and susceptible, European sea bass, teleost fish. Fish and Shellfish Immunology 33, 11591166. doi: 10.1016/j.fsi.2012.09.002. Google Scholar
Davey, G. C., Calduch-Giner, J. A., Houeix, B., Talbot, A., Sitjà-Bobadilla, A., Prunet, P., Pérez-Sánchez, J. and Cairns, M. T. (2011). Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei . Molecular Immunology 48, 21022112. doi: 10.1016/j.molimm.2011.07.003. Google Scholar
Dezfuli, B. S., Castaldelli, G., Bo, T., Lorenzoni, M. and Giari, L. (2011 a). Intestinal immune response of Silurus glanis and Barbus barbus naturally infected with Pomphorhynchus laevis (Acanthocephala). Parasite Immunology 33, 116123. doi: 10.1111/j.1365-3024.2010.01266.x. Google Scholar
Dezfuli, B. S., Giari, L., Squerzanti, S., Lui, A., Lorenzoni, M., Sakalli, S. and Shinn, A. P. (2011 b). Histological damage and inflammatory response elicited by Monobothrium wageneri (Cestoda) in the intestine of Tinca tinca (Cyprinidae). Parasites and Vectors 4, doi: 10.1186/1756-3305-4-225. Google ScholarPubMed
Dezfuli, B. S., Giari, L., Lui, A., Squerzanti, S., Castaldelli, G., Shinn, A. P., Manera, M. and Lorenzoni, M. (2012 a). Proliferative cell nuclear antigen (PCNA) expression in the intestine of Salmo trutta trutta naturally infected with an acanthocephalan. Parasites and Vectors 5, doi: 10.1186/1756-3305-5-198. CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Lui, A., Giari, L., Castaldelli, G., Mulero, V. and Noga, E. J. (2012 b). Infiltration and activation of acidophilic granulocytes in skin lesions of gilthead sea bream, Sparus aurata, naturally infected with lymphocystis disease virus. Developmental and Comparative Immunology 36, 174182. doi: 10.1016/j.dci.2011.06.017. Google Scholar
Dezfuli, B. S., Lui, A., Giari, L., Castaldelli, G., Shinn, A. P. and Lorenzoni, M. (2012 c). Innate immune defence mechanisms of tench, Tinca tinca (L.), naturally infected with the tapeworm Monobothrium wageneri . Parasite Immunology 34, 511519. doi: 10.1111/j.1365-3024.2012.01373.x Google Scholar
Dezfuli, B. S., Lui, A., Pironi, F., Manera, M., Shinn, A. P. and Lorenzoni, M. (2013). Cell types and structures involved in tench, Tinca tinca (L.), defence mechanisms against a systemic digenean infection. Journal of Fish Diseases 36, 577585. doi: 10.1111/jfd.12049. Google Scholar
Estensoro, I., Redondo, M. J., Álvarez-Pellitero, P. and Sitjà-Bobadilla, A. (2010). Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata . Diseases of Aquatic Organisms 92, 5158.CrossRefGoogle ScholarPubMed
Estensoro, I., Benedito-Palos, L., Palenzuela, O., Kaushik, S., Sitjà-Bobadilla, A. and Pérez-Sánchez, J. (2011). The nutritional background of the host alters the disease course in a fish-myxosporean system. Veterinary Parasitology 175, 141150. doi: 10.1016/j.vetpar.2010.09.015. CrossRefGoogle Scholar
Estensoro, I., Calduch-Giner, J. A., Kaushik, S., Pérez-Sánchez, J. and Sitjà-Bobadilla, A. (2012 a). Modulation of the IgM gene expression and the IgM immunoreactive cell distribution by the nutritional background in gilthead sea bream (Sparus aurata) challenged with Enteromyxum leei (Myxozoa). Fish and Shellfish Immunology 33, 401410.Google Scholar
Estensoro, I., Redondo, M. J., Salesa, B., Kaushik, S., Pérez-Sánchez, J. and Sitjà-Bobadilla, A. (2012 b). Effect of the nutritional background and the infection by the parasite Enteromyxum leei (Myxozoa: Myxosporea) on the mucosal carbohydrate pattern of the intestine of gilthead sea bream (Sparus aurata). Diseases of Aquatic Organisms 100, 2942. doi: 10.3354/dao02486. Google Scholar
Estensoro, I., Jung-Schroers, V., Álvarez-Pellitero, P., Steinhagen, D. and Sitjà-Bobadilla, A. (2013). Effects of Enteromyxum leei (Myxozoa) infection on gilthead sea bream (Sparus aurata) (Teleostei) intestinal mucus: glycoprotein profile and bacterial adhesion. Parasitology Research 112, 567576. doi: 10.1007/s00436-012-3168-3. Google Scholar
Fleurance, R., Sauvegrain, C., Marques, A., Le Breton, A., Guereaud, C., Cherel, Y. and Wyers, M. (2008). Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata . Diseases of Aquatic Organisms 79, 219228.Google Scholar
Gómez, G. D. and Balcázar, J. L. (2008). A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology 52, 145154. doi: 10.1111/j.1574-695X.2007.00343.x CrossRefGoogle ScholarPubMed
Grove, S., Tryland, M., Press, C. M. and Reitan, L. J. (2006). Serum immunoglobulin M in Atlantic halibut (Hippoglossus hippoglossus): characterisation of the molecule and its immunoreactivity. Fish and Shellfish Immunology 20, 97112. doi: 10.1016/j.fsi.2005.05.002. CrossRefGoogle ScholarPubMed
Hansen, R. D. E., Trees, A. J., Bah, G. S., Hetzel, U., Martin, C., Bain, O., Tanya, V. N. and Makepeace, B. L. (2011). A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi . Proceedings of the Royal Society B – Biological Sciences 278, 22932302. doi: 10.1098/rspb.2010.2367. Google Scholar
Hu, Y. L., Zhu, L. Y., Xiang, L. X. and Shao, J. Z. (2011). Discovery of an unusual alternative splicing pathway of the immunoglobulin heavy chain in a teleost fish, Danio rerio . Developmental and Comparative Immunology 35, 253257. doi: 10.1016/j.dci.2010.10.009. CrossRefGoogle Scholar
Jones, S. R. M. (2001). The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25, 841852. doi: 10.1016/s0145-305x(01)00039-8. Google Scholar
Jorgensen, L. V., Heinecke, R. D., Skjodt, K., Rasmussen, K. J. and Buchmann, K. (2011). Experimental evidence for direct in situ binding of IgM and IgT to early trophonts of Ichthyophthirius multifiliis (Fouquet) in the gills of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 34, 749755.Google Scholar
Katharios, P., Rigos, G. and Divanach, P. (2011). Enteromyxum leei (Myxozoa), a lethal intruder of tropical pet fish: first case in humphead wrasse, Cheilinus undulatus (Ruppell, 1835). Journal of Exotic Pet Medicine 20, 138143. doi: 10.1053/j.jepm.2011.02.009. Google Scholar
Li, J., Barreda, D. R., Zhang, Y. A., Boshra, H., Gelman, A. E., Lapatra, S., Tort, L. and Sunyer, J. O. (2006). B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nature Immunology 7, 11161124. doi: 10.1038/ni1389. Google Scholar
López-Ruiz, A., Esteban, M. A. and Meseguer, J. (1992). Blood-cells of the gilthead sea bream (Sparus aurata) – light and electron-microscopic studies. Anatomical Record 234, 161171. doi: 10.1002/ar.1092340203. Google Scholar
Lovy, J., Goodwin, A. E., Speare, D. J., Wadowska, D. W. and Wright, G. M. (2011). Histochemical and ultrastructural analysis of pathology and cell responses in gills of channel catfish affected with proliferative gill disease. Diseases of Aquatic Organisms 94, 125134. doi: 10.3354/dao02322. Google Scholar
Magnadottir, B., Gudmundsdottir, S., Gudmundsdottir, B. K. and Helgason, S. (2009). Natural antibodies of cod (Gadus morhua L.): specificity, activity and affinity. Comparative Biochemistry and Physiology B – Biochemistry and Molecular Biology 154, 309316. doi: 10.1016/j.cbpb.2009.07.005. Google Scholar
Martyn, A. A., Hong, H., Ringuette, M. J. and Desser, S. S. (2002). Changes in host and parasite-derived cellular and extracellular matrix components in developing cysts of Myxobolus pendula (Myxozoa). Journal of Eukaryotic Microbiology 49, 175182. doi: 10.1111/j.1550-7408.2002.tb00362.x. Google Scholar
Matsuyama, T. and Iida, T. (1999). Degranulation of eosinophilic granular cells with possible involvement in neutrophil migration to site of inflammation in tilapia. Developmental and Comparative Immunology 23, 451457. doi: 10.1016/s0145-305x(99)00027-0. Google Scholar
Matsuyama, T. and Iida, T. (2001). Influence of tilapia mast cell lysate on vascular permeability. Fish and Shellfish Immunology 11, 549556. doi: 10.1006/fsim.2000.0332. Google Scholar
Mekori, Y. A. (2004). The mastocyte: the “other” inflammatory cell in immunopathogenesis. Journal of Allergy and Clinical Immunology 114, 5257. doi: http://dx.doi.org/10.1016/j.jaci.2004.04.015.CrossRefGoogle ScholarPubMed
Meseguer, J., López-Ruiz, A. and Esteban, M. A. (1994 a). Cytochemical characterization of leukocytes from the seawater teleost, gilthead sea bream (Sparus aurata L). Histochemistry 102, 3744. doi: 10.1007/bf00271047. Google Scholar
Meseguer, J., López-Ruiz, A. and Esteban, M. A. (1994 b). Melanomacrophages of the seawater teleosts, sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) – morphology, formation and possible function. Cell and Tissue Research 277, 110.Google Scholar
Meseguer, J., Esteban, M. A. and Mulero, V. (1996). Nonspecific cell-mediated cytotoxicity in the seawater teleosts (Sparus aurata and Dicentrarchus labrax): ultrastructural study of target cell death mechanisms. Anatomical Record 244, 499505. doi: 10.1002/(sici)1097-0185(199604)244:4<499::aid-ar8>3.0.co;2-q. Google Scholar
Mulero, I., Sepulcre, M. P., Meseguer, J., García-Ayala, A. and Mulero, V. (2007). Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response. Proceedings of the National Academy of Sciences USA 104, 1943419439.Google Scholar
Mulero, I., Noga, E. J., Meseguer, J., García-Ayala, A. and Mulero, V. (2008). The antimicrobial peptides piscidins are stored in the granules of professional phagocytic granulocytes of fish and are delivered to the bacteria-containing phagosome upon phagocytosis. Developmental and Comparative Immunology 32, 15311538.Google Scholar
Murray, H. M., Leggiadro, C. T. and Douglas, S. E. (2007). Immunocytochemical localization of pleurocidin to the cytoplasmic granules of eosinophilic granular cells from the winter flounder gill. Journal of Fish Biology 70, 336345. doi: 10.1111/j.1095-8649.2007.01452.x. Google Scholar
Noya, M. and Lamas, J. (1996). Morphology and histochemistry of a PAS-positive granular cell in the gills of the gilthead sea bream, Sparus aurata L. Journal of Anatomy 189, 439443.Google Scholar
Olsen, M. M., Kania, P. W., Heinecke, R. D., Skjoedt, K., Rasmussen, K. J. and Buchmann, K. (2011). Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: molecular and immunohistochemical studies. Fish and Shellfish Immunology 30, 859869.CrossRefGoogle ScholarPubMed
Ordas, M. C., Castro, R., Dixon, B., Sunyer, J. O., Bjork, S., Bartholomew, J., Korytar, T., Kollner, B., Cuesta, A. and Tafalla, C. (2012). Identification of a novel CCR7 gene in rainbow trout with differential expression in the context of mucosal or systemic infection. Developmental and Comparative Immunology 38, 302311. doi: 10.1016/j.dci.2012.07.001 CrossRefGoogle ScholarPubMed
Overland, H. S., Pettersen, E. F., Ronneseth, A. and Wergeland, H. I. (2010). Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Fish and Shellfish Immunology 28, 193204.Google Scholar
Palenzuela, O., Sitjà-Bobadilla, A., Álvarez-Pellitero, P. (1996). Isolation and partial characterization of serum immunoglobulins from sea bass (Dicentrarchus labrax L) and gilthead sea bream (Sparus aurata L). Fish and Shellfish Immunology 6, 8194.Google Scholar
Pettersen, E. F., Bjerknes, R. and Wergeland, H. I. (2000). Studies of Atlantic salmon (Salmo salar L.) blood, spleen and head kidney leucocytes using specific monoclonal antibodies, immunohistochemistry and flow cytometry. Fish and Shellfish Immunology 10, 695710. doi: 10.1006/fsim.2000.0284 Google Scholar
Reite, O. B. (1996). The mast cell nature of granule cells in the digestive tract of the pike, Esox lucius: similarity to mammalian mucosal mast cells and globule leucocytes. Fish and Shellfish Immunology 6, 363369.Google Scholar
Reite, O. B. (1998). Mast cells eosinophilic granule cells of teleostean fish: a review focusing on staining properties and functional responses. Fish and Shellfish Immunology 8, 489513.Google Scholar
Reite, O. B. and Evensen, O. (2006). Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish and Shellfish Immunology 20, 192208.Google Scholar
Reyes-Becerril, M., Ascencio-Valle, F., Tovar-Ramírez, D., Meseguer, J. and Esteban, M. A. (2011 a). Effects of polyamines on cellular innate immune response and the expression of immune-relevant genes in gilthead seabream leucocytes. Fish and Shellfish Immunology 30, 248254.Google Scholar
Reyes-Becerril, M., López-Medina, T., Ascencio-Valle, F. and Esteban, M. A. (2011 b). Immune response of gilthead sea bream (Sparus aurata) following experimental infection with Aeromonas hydrophila . Fish and Shellfish Immunology 31, 564570.Google Scholar
Rocha, J. S. and Chiarini-Garcia, H. (2007). Mast cell heterogeneity between two different species of Hoplias sp. (Characiformes: Erythrinidae): response to fixatives, anatomical distribution, histochemical contents and ultrastructural features. Fish and Shellfish Immunology 22, 218229.Google Scholar
Rombout, J. H. W. M., Abelli, L., Picchietti, S., Scapigliati, G. and Kiron, V. (2011). Teleost intestinal immunology. Fish and Shellfish Immunology 31, 616626.Google Scholar
Ronza, P., Coscelli, G., Losada, A. P., Bermúdez, R. and Quiroga, M. I. (2013). Changes in splenic melanomacrophage centres of turbot, Psetta maxima (L.), infected experimentally with Enteromyxum scophthalmi (Myxozoa). Journal of Comparative Pathology 148, 9292.Google Scholar
Salinas, I., Zhang, Y.-A. and Sunyer, J. O. (2011). Mucosal immunoglobulins and B cells of teleost fish. Developmental and Comparative Immunology 35, 13461365. doi: 10.1016/j.dci.2011.11.009 Google Scholar
Sepulcre, M. P., Pelegrin, P., Mulero, V. and Meseguer, J. (2002). Characterisation of gilthead sea bream acidophilic granulocytes by a monoclonal antibody unequivocally points to their involvement in fish phagocytic response. Cell and Tissue Research 308, 97102.Google Scholar
Sepulcre, M. P., López-Castejón, G., Meseguer, J. and Mulero, V. (2007). The activation of gilthead sea bream professional phagocytes by different PAMPs underlines the behavioural diversity of the main innate immune cells of bony fish. Molecular Immunology 44, 20092016. doi: 10.1016/j.molimm.2006.09.022. Google Scholar
Sitjà-Bobadilla, A. (2008). Living off a fish: a trade-off between parasites and the immune system. Fish and Shellfish Immunology 25, 358372.Google Scholar
Sitjà-Bobadilla, A. and Palenzuela, O. (2012). Enteromyxum species. In Fish Parasites: Pathology and Protection (ed. Woo, P. T. K. and Buchmann, K.), pp. 163176. CABI, Wallingford, UK.Google Scholar
Sitjà-Bobadilla, A. and Palenzuela, O. (2013). Myxozoan biology and ecology. In Fisheries and Aquaculture (ed. UNESCO-EOLSS Joint Committee), in Encyclopedia of Life Support Systems (EOLSS). Developed under the Auspices of the UNESCO, Eolss Publishers, Oxford, UK.Google Scholar
Sitjà-Bobadilla, A., Redondo, M. J., Bermúdez, R., Palenzuela, O., Ferreiro, I., Riaza, A., Quiroga, I., Nieto, J. M. and Álvarez-Pellitero, P. (2006). Innate and adaptive immune responses of turbot, Scophthalmus maximus (L.), following experimental infection with Enteromyxum scophthalmi (Myxosporea : Myxozoa). Fish and Shellfish Immunology 21, 485500. doi: 10.1016/j.fsi.2006.02.004. Google Scholar
Sitjà-Bobadilla, A., Diamant, A., Palenzuela, O. and Álvarez-Pellitero, P. (2007). Effect of host factors and experimental conditions on the horizontal transmission of Enteromyxum leei (Myxozoa) to gilthead sea bream, Sparus aurata L., and European sea bass, Dicentrarchus labrax (L.). Journal of Fish Diseases 30, 243250.Google Scholar
Sitjà-Bobadilla, A., Calduch-Giner, J., Saera-Vila, A., Palenzuela, O., Álvarez-Pellitero, P. and Pérez-Sánchez, J. (2008). Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish and Shellfish Immunology 24, 610619.Google Scholar
Sunyer, J. O. (2012). Evolutionary and functional relationships of B cells from fish and mammals: insights into their novel roles in phagocytosis and presentation of particulate antigen. Infectious Disorders Drug Targets 12, 200212.Google Scholar
Tian, J. Y., Xie, H. X., Zhang, Y. A., Xu, Z., Yao, W. J. and Nie, P. (2009). Ontogeny of IgM-producing cells in the mandarin fish Siniperca chuatsi identified by in situ hybridisation. Veterinary Immunology and Immunopathology 132, 146152. doi: 10.1016/j.vetimm.2009.05.018. Google Scholar
Tun, T., Ogawa, K. and Wakabayashi, H. (2002). Pathological changes induced by three myxosporeans in the intestine of cultured tiger puffer, Takifugu rubripes (Temminck and Schlegel). Journal of Fish Diseases 25, 6372. doi: 10.1046/j.1365-2761.2002.00333.x. Google Scholar
Vigliano, F. A., Bermúdez, R., Quiroga, M. I. and Nieto, J. M. (2006). Evidence for melano-macrophage centres of teleost as evolutionary precursors of germinal centres of higher vertebrates: an immunohistochemical study. Fish and Shellfish Immunology 21, 467471. doi: 10.1016/j.fsi.2005.12.012. CrossRefGoogle ScholarPubMed
Vigliano, F. A., Losada, A. P., Castello, M., Bermúdez, R. and Quiroga, M. I. (2011). Morphological and immunohistochemical characterisation of the thymus in juvenile turbot (Psetta maxima, L.). Cell and Tissue Research 346, 407416. doi: 10.1007/s00441-011-1282-7. Google Scholar
Whyte, S. K. (2007). The innate immune response of finfish – a review of current knowledge. Fish and Shellfish Immunology 23, 11271151.Google Scholar
Zuasti, A. and Ferrer, C. (1988). Granulopoiesis in the head kidney of Sparus auratus . Archives of Histology and Cytology 51, 425431. doi: 10.1679/aohc.51.425. Google Scholar
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