Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei

Molecular Immunology

Volumn 48, Issue 15-16, 2011, Pages 2102-2112

  Davey, Grace C ^a   Calduch Giner, Josep A ^b   Houeix, Benoit ^a   Talbot, Anita ^a   Sitjà Bobadilla, Ariadna ^b   Prunet, Patrick ^c   Pérez Sánchez, Jaume ^b   Cairns, Michael T ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

^c CEMAGREF   (France)

Author keywords

Gene expression; Immune response; Microarray; Myxozoa; Resistance; Sparidae

Indexed keywords

COMPLEMENTARY DNA; TRANSCRIPTOME;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; DEATH; DNA FINGERPRINTING; DNA MICROARRAY; DOWN REGULATION; EFFLUENT; ENTERITIS; ENTEROMYXUM LEEI; FISH; GENETIC DIFFERENCE; HOST PARASITE INTERACTION; IMMUNE RESPONSE; INTESTINE; KIDNEY; MYXOZOA; NONHUMAN; PARASITE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEA BREAM; SPARUS AURATA;

ANIMALS; FISH DISEASES; GENE EXPRESSION; GENE EXPRESSION PROFILING; IN SITU HYBRIDIZATION; MYXOZOA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARASITIC DISEASES, ANIMAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEA BREAM;

ARCHOSARGUS RHOMBOIDALIS; ENTEROMYXUM LEEI; MYXOSPOREA; MYXOZOA; SPARIDAE; SPARUS AURATA;

EID: 80051928696     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.07.003     Document Type: Article

References (112)

1. Adema C.M., Hanington P.C., Lun C.M., Rosenberg G.H., Aragon A.D., Stout B.A., Richard M.L.L., Gross P.S., Loker E.S. 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. Alonso M., Leong J.A. Suppressive subtraction libraries to identify interferon-inducible genes in fish. Mar. Biotechnol. 2002, 4:74-80.
3. Altschul S., Gish W., Miller W., Myers E., Lipman D. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
4. Álvarez-Pellitero P., Palenzuela O., Sitjà-Bobadilla A. Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol. Int. 2008, 57:110-120.
5. APROMAR, 2010. La acuicultura marina de peces en España, http://www.apromar.es/Informes/Informe-APROMAR-2010.pdf.
6. Baerwald M.R., Welsh A.B., Hedrick R.P., May B. Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling. BMC Genomics 2008, 9:37.
7. Bermúdez R., Losada A.P., Vázquez S., Redondo M.J., Álvarez-Pellitero P., Quiroga M.I. Light and electron microscopic studies on turbot Psetta maxima infected with Enteromyxum scophthalmi: histopathology of turbot enteromyxosis. Dis. Aquat. Organ. 2010, 89:209-221.
8. Boehm U., Klamp T., Groot M., Howard J. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 1997, 15:749-795.
9. Botto M., Kirschfink M., Macor P., Pickering M.C., Würzner R., Tedesco F. Complement in human diseases: lessons from complement deficiencies. Mol. Immunol. 2009, 46:2774-2783.
10. Byon J.Y., Ohira T., Hirono I., Aoki T. Use of a cDNA microarray to study immunity against viral hemorrhagic septicaemia (VHS) in Japanese flounder (Paralichthys olivaceus) following DNA vaccination. Fish Shellfish Immunol. 2005, 18:135-147.
11. Byon J.Y., Takano T., Hirono I., Aoki T. Genome analysis of viral hemorrhagic septicaemia virus isolated from Japanese flounder Paralichthys olivaceus in Japan. Fish. Sci. 2006, 72:906-908.
12. Cairns M.T., Johnson M.C., Talbot A.T., Pemmasani J.K., McNeill R.E., Houeix B., Sangrador-Vegas A., Pottinger T.G. A cDNA microarray assessment of gene expression in the liver of rainbow trout (Oncorhynchus mykiss) in response to a handling and confinement stressor. Comp. Biochem. Physiol. Part D: Genomics Proteomics 2008, 3:51-66.
13. Calduch-Giner J.A., Davey G., Saera-Vila A., Houeix B., Talbot A., Prunet P., Cairns M.T., Pérez-Sánchez J. Use of microarray technology to assess the time course of liver stress response after confinement exposure in gilthead sea bream (Sparus aurata L.). BMC Genomics 2010, 11:193.
14. Carbon S., Ireland A., Mungall C., Shu S., Marshall B., Lewis S., Hub A., Grp W.P.W. AmiGO: online access to ontology and annotation data. Bioinformatics 2009, 25:288-289.
15. Cerdá J., Mercade J., Lozano J., Manchado M., Tingaud-Sequeira A., Astola A., Infante C., Halm S., Vinas J., Castellana B., Asensio E., Canavate P., Martinez-Rodriguez G., Piferrer F., Planas J., Prat F., Yufera M., Durany O., Subirada F., Rosell E., Maes T. Genomic resources for a commercial flatfish, the Senegalese sole (Solea senegalensis): EST sequencing, oligo microarray design, and development of the Soleamold bioinformatic platform. BMC Genomics 2008, 9:508.
16. Chang M.X., Nie P., Liu G.Y., Song Y., Gao Q. Identification of immune genes in grass carp Ctenopharyngodon idella in response to infection of the parasitic copepod Sinergasilus major. Parasitol. Res. 2005, 96:224-229.
17. Conesa A., Götz S., García-Gómez J.M., Perol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
18. Crouch E., Wright J.R. Surfactant proteins A and D and pulmonary host defence. Annu. Rev. Physiol. 2001, 63:521-554.
19. Cuesta A., Salinas I., Rodriguez A., Muñoz P., Sitjà-Bobadilla A., Álvarez-Pellitero P., Meseguer J., Esteban M.Á. Cell-mediated cytotoxicity is the main innate immune mechanism involved in the cellular defense of gilthead sea bream (Teleostei: Sparidae) against Enteromyxum leei (Myxozoa). Parasite Immunol. 2006, 28:657-665.
20. Cuesta A., Muñoz P., Rodriguez A., Salinas I., Sitjà-Bobadilla A., Álvarez-Pellitero P., Esteban M.Á., Meseguer J. Gilthead sea bream (Sparus aurata L.) innate defence against the parasite Enteromyxum leei (Myxozoa). Parasitology 2006, 132:95-104.
21. Darrah P., Hondalus M., Chen Q., Ischiropoulos H., Mosser D. Cooperation between reactive oxygen and nitrogen intermediates in killing of Rhodococcus equi by activated macrophages. Infect. Immun. 2000, 68:3587-3593.
22. Diamant A. A new pathogenic histozoic Myxidium (Myxosporea) in cultured gilt-head sea bream Sparus aurata L. Bull. Eur. Assoc. Fish Pathol. 1992, 12:64-66.
23. Diamant A. Fish-to-fish transmission of a marine myxosporean. Dis. Aquat. Organ. 1997, 30:99-105.
24. Diamant A., Wajsbrot N. Experimental transmission of Myxidium leei in gilthead sea bream Sparus aurata. Bull. Eur. Assoc. Fish Pathol. 1997, 17:99-103.
25. Dörfler C., El-Matbouli M. Isolation of a subtilisin-like serine protease gene (MyxSubtSP) from spores of Myxobolus cerebralis, the causative agent of whirling disease. Dis. Aquat. Organ. 2007, 73:245-251.
26. Drakesmith H., Prentice A. Viral infection and iron metabolism. Nat. Rev. Microbiol. 2008, 6:541-552.
27. Ellis A.E., Cavaco A., Petrie A., Lockhart K., Snow M., Collet B. Histology, immunocytochemistry and qRT-PCR analysis of Atlantic salmon, Salmo salar L., post-smolts following infection with infectious pancreatic necrosis virus (IPNV). J. Fish Dis. 2010, 33:803-818.
28. Estensoro I., Redondo M.J., Álvarez-Pellitero P., Sitjà-Bobadilla A. Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis. Aquat. Organ. 2010, 92:51-58.
29. Estensoro I., Benedito-Palos L., Palenzuela O., Kaushik S., Sitjà-Bobadilla A., Pérez-Sánchez J. The nutritional background of the host alters the disease course in a fish-myxosporean system. Vet. Parasitol. 2011, 175:141-150.
30. Ewart K.V., Johnson S.C., Ross N.W. Identification of a pathogen-binding lectin in salmon serum. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 1999, 123:9-15.
31. Ewart K.V., Belanger J.C., Williams J., Karakach T., Penny S., Tsoi S.C.M., Richards R.C., Douglas S.E. Identification of genes differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Dev. Comp. Immunol. 2005, 29:333-347.
32. Fast M.D., Ross N.W., Mustafa A., Sims D.E., Johnson S.C., Conboy G.A., Speare D.J., Johnson G., Burka J.F. Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Dis. Aquat. Organ. 2002, 52:57-68.
33. Ferraresso S., Vitulo N., Mininni A.N., Romualdi C., Cardazzo B., Negrisolo E., Reinhardt R., Canario A.V.M., Patarnello T., Bargelloni L. Development and validation of a gene expression oligo microarray for the gilthead sea bream (Sparus aurata). BMC Genomics 2008, 9:580.
34. Fleurance R., Sauvegrain C., Marques A., Le Breton A., Guereaud C., Cherel Y., Wyers M. Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis. Aquat. Organ. 2008, 79:219-228.
35. Gabay C., Kushner I. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 1999, 340:448-454.
36. Golomazou E., Karagouni E., Athanassopoulou F. The most important myxosporean parasite species affecting cultured Mediterranean fish. J. Hell. Vet. Med. Soc. 2004, 55:342-352.
37. Golomazou E., Athanassopoulou F., Karagouni E., Tsagozis P., Tsantilas H., Vagianou S. Experimental transmission of Enteromyxum leei Diamant, Lom and Dykova, 1994 in sharpsnout sea bream, Diplodus puntazzo C. and the effect on some innate immune parameters. Aquaculture 2006, 260:44-53.
38. Götz S., García-Gómez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talón M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36:3420-3435.
39. Gracey A.Y., Fraser E.J., Li W.Z., Fang Y.X., Taylor R.R., Rogers J., Brass A., Cossins A.R. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:16970-16975.
40. Guiry A., Flynn D., Hubert S., O'Keeffe A., LeProvost O., White S., Forde P., Davoren P., Houeix B., Smith T., Cotter D., Wilkins N., Cairns M. Testes and brain gene expression in precocious male and adult maturing Atlantic salmon (Salmo salar). BMC Genomics 2010, 11:211.
41. Hibberd M., Sumiya M., Summerfield J., Booy R., Levin M. Association of variants of the gene for mannose-binding lectin with susceptibility to meningococcal disease. Meningococcal Research Group. Lancet 1999, 353:1049-1053.
42. Holmskov U., Thiel S., Jensenius J.C. Collectins and ficolins: humoral lectins of the innate immune defense. Annu. Rev. Immunol. 2003, 21:547-578.
43. James E., Green D. Manipulation of apoptosis in the host-parasite interaction. Trends Parasitol. 2004, 20:280-287.
44. Jensen L.E., Thiel S., Petersen T.E., Jensenius J.C. A rainbow trout lectin with multimeric structure. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 1997, 116:385-390.
45. Jorgensen S.M., Afanasyev S., Krasnov A. Gene expression analyses in Atlantic salmon challenged with infectious salmon anaemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 2008, 9:179.
46. Jublanc E., Elkiric N., Toubiana M., Sri Widada J., Le Breton A., Lefebvre G., Sauvegrain C., Marques A. Observation on a Enteromyxum leei (Myxozoa Myxosporea) parasitosis on farming sea bream Sparus aurata. J. Eukaryot. Microbiol. 2005, 52:28S-34S.
47. Karagouni E., Athanassopoulou F., Tsagozis P., Ralli E., Moustakareas T., Lytra K., Dotsika E. The impact of a successful anti-myxosporean treatment on the phagocyte functions of juvenile and adult Sparus aurata L. Int. J. Immunopathol. Pharmacol. 2005, 18:121-132.
48. Kars M., Van Dijk H., Salimans M.M., Bartelink A.K., Van de Wiel A. Association of furunculosis and familial deficiency of mannose-binding lectin. Eur. J. Clin. Invest. 2005, 35:531-534.
49. Kishi K., Kitagawa E., Iwahashi H., Suzuki K., Hayashi Y. Medaka DNA microarray: a tool for evaluating physiological impacts of various toxicants. Interdisciplinary Studies on Environmental Chemistry-Biological Responses to Chemical Pollutants 2008, 143-154. Terra Scientific Publishing Company (TERRAPUB). Y. Murakami, K. Nakayama, S.-I. Kitamura, H. Iwata, S. Tanabe (Eds.).
50. Lillehoj H.S., Choi K.D. Recombinant chicken interferon-gamma-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Dis. 1998, 42:307-314.
51. Liu J., Deng M., Lancto C., Abrahamsen M., Rutherford M., Enomoto S. Biphasic modulation of apoptotic pathways in Cryptosporidium parvum-infected human intestinal epithelial cells. Infect. Immun. 2009, 77:837-849.
52. Louro B., Passos A.L.S., Souche E.L., Tsigenopoulos C., Beck A., Lagnel J., Bonhomme F., Cancela L., Cerdà J., Clark M.S., Lubzens E., Magoulas A., Planas J.V., Volckaert F.A.M., Reinhardt R., Canario A.V.M. Gilthead sea bream (Sparus aurata) and European sea bass (Dicentrarchus labrax) expressed sequence tags: characterization, tissue-specific expression and gene markers. Mar. Gen. 2010, 3:179-191.
53. Lovegrove F., Gharib S., Patel S., Hawkes C., Kain K., Liles W. Expression microarray analysis implicates apoptosis and interferon-responsive mechanisms in susceptibility to experimental cerebral malaria. Am. J. Pathol. 2007, 171:1894-1903.
54. Lüder C., Gross U., Lopes M. Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions. Trends Parasitol. 2001, 17:480-486.
55. MacKenzie S., Balasch J.C., Novoa B., Ribas L., Roher N., Krasnov A., Figueras A. Comparative analysis of the acute response of the trout, O-mykiss, head kidney to in vivo challenge with virulent and attenuated infectious haematopoietic necrosis virus and LPS-induced inflammation. BMC Genomics 2008, 9:141.
56. Martone C.B., Spivak E., Busconi L., Folco E.J.E., Sánchez J.J. A cysteine protease from myxosporean degrades host myofibrils in vitro. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 1999, 123:267-272.
57. Marx J. Iron and infection: competition between host and microbes for a precious element. Best Pract. Res. Clin. Haematol. 2002, 15:411-426.
58. Matsuyama T., Fujiwara A., Nakayasu C., Kamaishi T., Oseko N., Hirono I., Aoki T. Gene expression of leucocytes in vaccinated Japanese flounder (Paralichthys olivaceus) during the course of experimental infection with Edwardsiella tarda. Fish Shellfish Immunol. 2007, 22:598-607.
59. Matsuyama T., Fujiwara A., Nakayasu C., Kamaishi T., Oseko N., Tsutsumi N., Hirono I., Aoki T. Microarray analyses of gene expression in Japanese flounder Paralichthys olivaceus leucocytes during monogenean parasite Neoheterobothrium hirame infection. Dis. Aquat. Organ. 2007, 75:79-83.
60. McCall M.B., Sauerwein R.W. Interferon-gamma-central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J. Leukoc. Biol. 2010, 88:1131-1143.
61. McKerrow J.H., Caffrey C., Kelly B., Loke P., Sajid M. Proteases in parasitic diseases. Annu. Rev. Pathol.: Mech. Dis. 2006, 1:497-536.
62. McLean K.J., Sabri M., Marshall K.R., Lawson R.J., Lewis D.G., Clift D., Balding P.R., Dunford A.J., Warman A.J., McVey J.P., Quinn A.M., Sutcliffe M.J., Scrutton N.S., Munro A.W. Biodiversity of cytochrome P450 redox systems. Biochem. Soc. Trans. 2005, 33:796-801.
63. Mitra S., Das H.R. A novel mannose-binding lectin from plasma of Labeo rohita. Fish Physiol. Biochem. 2002, 25:121-129.
64. Miyagi K., Kawakami K., Saito A. Role of reactive nitrogen and oxygen intermediates in gamma interferon-stimulated murine macrophage bactericidal activity against Burkholderia pseudomallei. Infect. Immun. 1997, 65:4108-4113.
65. Morrison R.N., Cooper G.A., Koop B.F., Rise M.L., Bridle A.R., Adams M.B., Nowak B.F. Transcriptome profiling the gills of amoebic gill disease (AGD)-affected Atlantic salmon (Salmo salar L.): a role for tumor suppressor p53 in AGD pathogenesis?. Physiol. Genomics 2006, 26:15-34.
66. Muñoz P., Cuesta A., Athanassopoulou F., Golomazou H., Crespo S., Padrós F., Sitjà-Bobadilla A., Albiñana G., Esteban M.Á., Álvarez-Pellitero P., Meseguer J. Sharpsnout sea bream (Diplodus puntazzo) humoral immune response against the parasite Enteromyxum leei (Myxozoa). Fish Shellfish Immunol. 2007, 23:636-645.
67. Murakawa M., Jung S.K., Iijima K., Yonehara S. Apoptosis-inducing protein, AIP, from parasite-infected fish induces apoptosis in mammalian cells by two different molecular mechanisms. Cell Death Differ. 2001, 8:298-307.
68. Mustafa A., Speare D.J., Daley J., Conboy G.A., Burka J.F. Enhanced susceptibility of seawater cultured rainbow trout, Oncorhynchus mykiss (Walbaum), to the microsporidian Loma salmonae during a primary infection with the sea louse, Lepeophtheirus salmonis. J. Fish. Dis. 2000, 23:337-341.
69. Ourth D.D., Naffa M.B., Simco B.A. Comparative study of mannose-binding C-type lectin isolated from channel catfish (Ictalurus punctatus) and blue catfish (Ictalurus furcatus). Fish Shellfish Immunol. 2007, 23:1152-1160.
70. Ourth D.D., Rose W.M., Siefkes M.J. Isolation of mannose-binding C-type lectin from sea lamprey (Petromyzon marinus) plasma and binding to Aeromonas salmonicida. Vet. Immunol. Immunopathol. 2008, 126:407-412.
71. Pacelli R., Wink D., Cook J., Krishna M., DeGraff W., Friedman N., Tsokos M., Samuni A., Mitchell J. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J. Exp. Med. 1995, 182:1469-1479.
72. Padrós F., Palenzuela O., Hispano C., Tosas O., Zarza C., Crespo S., Alvarez-Pellitero P. Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Dis. Aquat. Organ. 2001, 47:57-62.
73. Paramá A., Castro R., Lamas J., Sanmartín M.L., Santamarina M.T., Leiro J. Scuticociliate proteinases may modulate turbot immune response by inducing apoptosis in pronephric leucocytes. Int. J. Parasitol. 2007, 37:87-95.
74. Palenzuela O. Myxozoan infections in Mediterranean mariculture. Parassitologia 2006, 48:27-29.
75. Peatman E., Baoprasertkul P., Terhune J., Xu P., Nandi S., Kucuktas H., Li P., Wang S.L., Somridhivej B., Dunham R., Liu Z.J. Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a Gram-negative bacterium. Dev. Comp. Immunol. 2007, 31:1183-1196.
76. Peatman E., Terhune J., Baoprasertkul P., Xu P., Nandi S., Wang S., Somridhivej B., Kucuktas H., Li P., Dunham R., Liu Z. Microarray analysis of gene expression in the blue catfish liver reveals early activation of the MHC class I pathway after infection with Edwardsiella ictaluri. Mol. Immunol. 2008, 45:553-566.
77. Pollock R.C.G., Farthing M.J.G., Bajaj-Elliott M., Sanderson I.R., McDonald V. Interferon gamma induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 2001, 120:99-107.
78. Rigos R., Katharios P. Pathological obstacles of newly-introduced fish species in Mediterranean mariculture: a review. Rev. Fish Biol. Fish. 2010, 20:47-70.
79. Rise M.L., Jones S.R.M., Brown G.D., von Schalburg K.R., Davidson W.S., Koop B.F. Microarray analyses identify molecular biomarkers of Atlantic salmon macrophage and haematopoietic kidney response to Piscirickettsia salmonis infection. Physiol. Genomics 2004, 20:21-35.
80. Roberge C., Páez D.J., Rossignol O., Guderley H., Dodson J., Bernatchez L. Genome-wide survey of the gene expression response to saprolegniasis in Atlantic salmon. Mol. Immunol. 2007, 44:1374-1383.
81. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 2006, 20:172-191.
82. Roy S., Knox K., Segal S., Griffiths D., Moore C.E., Welsh K.I., Smarason A., Day N.P., McPheat W.L., Crook D.W., Hill A.V.S. MBL genotype and risk of invasive pneumococcal disease: a case-control study. Lancet 2002, 359:1569-1573.
83. Saeij J.P.J., de Vries B.J., Wiegertjes G.F. The immune response of carp to Trypanoplasma borreli: kinetics of immune gene expression and polyclonal lymphocyte activation. Dev. Comp. Immunol. 2003, 27:859-874.
84. Samuel C. Antiviral actions of interferons. Clin. Microbiol. Rev. 2001, 14:778-809.
85. Sarropoulou E., Kotoulas G., Power D.M., Geisler R. Gene expression profiling of gilthead sea bream during early development and detection of stress-related genes by the application of cDNA microarray technology. Physiol. Genomics 2005, 23:182-191.
86. Schaible U., Kaufmann S. Iron and microbial infection. Nat. Rev. Microbiol. 2004, 2:946-953.
87. 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. Organ. 2004, 59:141-150.
88. Schrader M., Fahimi H. Peroxisomes and oxidative stress. Biochim. Biophys. Acta 2006, 1763:1755-1766.
89. Shultz U., Kaspers B., Staeheli P. The interferon system of non-mammalian vertebrates. Dev. Comp. Immunol. 2004, 28:499-508.
90. Sitjà-Bobadilla A., Redondo M., Bermúdez R., Palenzuela O., Ferreiro I., Riaza A., Quiroga I., Nieto J., Álvarez-Pellitero P. Innate and adaptive immune responses of turbot, Scophthalmus maximus (L.), following experimental infection with Enteromyxum scophthalmi (Myxosporea: Myxozoa). Fish Shellfish Immunol. 2006, 21:485-500.
91. Sitjà-Bobadilla A., Diamant A., Palenzuela O., Álvarez-Pellitero P. 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.). J. Fish Dis. 2007, 30:243-250.
92. Sitjà-Bobadilla A. Living off a fish: a trade-off between parasites and the immune system. Fish Shellfish Immunol. 2008, 25:358-372.
93. Sitjà-Bobadilla A., Calduch-Giner J., Saera-Vila A., Palenzuela O., Álvarez-Pellitero P., Pérez-Sánchez J. 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 Shellfish Immunol. 2008, 24:610-619.
94. Sitjà-Bobadilla A. Can myxosporean parasites compromise fish and amphibian reproduction?. Proc. R. Soc. B 2009, 276:2861-2870.
95. Sitjà-Bobadilla, A., Palenzuela, O., in press. Enteromyxum spp. In: Woo, P.T.K., Buchmann, K. (Eds.), Fish Parasites: Pathobiology and Protection. CABI Publishing, Wallingford, Oxfordshire, U.K. http://bookshop.cabi.org/default.aspx?site=191&page=2633&pid=2371.
96. Skugor S., Glover K.A., Nilsen F., Krasnov A. Local and Systemic gene expression responses of Atlantic salmon (Salmo salar L.) to infection with the salmon louse (Lepeophtheirus salmonis). BMC Genomics 2008, 9:498.
97. Sreenivasan R., Cai M.N., Bartfai R., Wang X.G., Christoffels A., Orban L. Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the Zebrafish Gonad and Brain. PLoS ONE 2008, 3:16.
98. Taggart J.B., Bron J.E., Martin S.A.M., Seear P.J., Høyheim B., Talbot R., Carmichael S.N., Villeneuve L.A.N., Sweeney G.E., Houlihan D.F., Secombes C.J., Tocher D.R., Teale A.J. A description of the origins, design and performance of the TRAITS-SGP Atlantic salmon Salmo salar L. cDNA microarray. J. Fish Biol. 2008, 72:2071-2094.
99. Thompson C. Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267:1456-1462.
100. Tort L., Balasch J.C., Mackenzie S. Fish immune system. A crossroads between innate and adaptive responses. Immunología 2003, 22:277-286.
101. Turner M.W. The role of mannose-binding lectin in health and disease. Mol. Immunol. 2003, 40:423-429.
102. Valko M., Leibfritz D., Moncol J., Cronin M., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
103. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (research0034.1-0034.11).
104. Vitved L., Holmskov U., Koch C., Teisner B., Hansen S., Salomonsen J., Skjødt K. The homologue of mannose-binding lectin in the carp family Cyprinidae is expressed at high level in spleen, and the deduced primary structure predicts affinity for galactose. Immunogenetics 2000, 52:155.
105. Wang S., Liu H., Bushek D., Ford S.E., Peatmann E., Kucuktas H., Quilang J., Li P., Wallace R., Wang Y., Guo X., Liu Z. Microarray analysis of gene expression in eastern oyster (Crassostrea virginica) reveals a novel combination of antimicrobial and oxidative stress host responses after dermo (Perkinsus marinus) challenge. Fish Shellfish Immunol. 2010, 29:921-929.
106. White E. Life, death, and the pursuit of apoptosis. Genes Dev. 1996, 10:1-15.
107. Williams D.R., Li W., Hughes M.A., Gonzalez S.F., Vernon C., Vidal M.C., Jeney Z., Jeney G., Dixon P., McAndrew B., Bartfai R., Orban L., Trudeau V., Rogers J., Matthews L., Fraser E.J., Gracey A.Y., Cossins A.R. Genomic resources and microarrays for the common carp Cyprinus carpio L. J. Fish Biol. 2008, 72:2095-2117.
108. Williams T.D., Diab A.M., George S.G., Godfrey R.E., Sabine V., Conesa A., Minchin S.D., Watts P.C., Chipman J.K. Development of the GENIPOL European flounder (Platichthys flesus) microarray and determination of temporal transcriptional responses to cadmium at low dose. Environ. Sci. Technol. 2006, 40:6479-6488.
109. Wynne J.W., O'Sullivan M.G., Cook M.T., Stone G., Nowak B.F., Lovell D.R., Elliott N.G. Transcriptome analyses of amoebic gill disease-affected Atlantic salmon (Salmo salar) tissues reveal localized host gene suppression. Mar. Biotechnol. 2008, 10:388-403.
110. Wynne J.W., O'Sullivan M.G., Stone G., Cook M.T., Nowak B.F., Lovell D.R., Taylor R.S., Elliott N.G. Resistance to amoebic gill disease (AGD) is characterised by the transcriptional dysregulation of immune and cell cycle pathways. Dev. Comp. Immunol. 2008, 32:1539-1560.
111. Xu D.H., Klesius P.H., Shoemaker C.A. Cutaneous antibodies from channel catfish, Ictalurus punctatus (Rafinesque), immune to Ichthyophthirius multifiliis (Ich) may induce apoptosis of Ich theronts. J. Fish Dis. 2005, 28:213-220.
112. Young N.D., Cooper G.A., Nowak B.F., Koop B.F., Morrison R.N. Coordinated down-regulation of the antigen processing machinery in the gills of amoebic gill disease-affected Atlantic salmon (Salmo salar L.). Mol. Immunol. 2008, 45:2581-2597.