Biology and mucosal immunity to myxozoans

Developmental and Comparative Immunology

Volumn 43, Issue 2, 2014, Pages 243-256

  Gómez, Daniela ^a   Bartholomew, Jerri ^b   Sunyer, J Oriol ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Fish; Gill; Intestine; Mucosal immune response; Myxozoan; Skin

Indexed keywords

IMMUNOGLOBULIN; IMMUNOGLOBULIN T, TELEOST;

ANIMAL; FISH; IMMUNOLOGY; MUCOSAL IMMUNITY; MYXOZOA; PARASITIC DISEASES, ANIMAL;

ANIMALS; FISHES; IMMUNITY, MUCOSAL; IMMUNOGLOBULINS; MYXOZOA; PARASITIC DISEASES, ANIMAL;

EID: 84891831448     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.08.014     Document Type: Review

References (138)

1. Adriano E.A., Arana S., Alves A.L., Silva M.R.M., Ceccarelli P.S., Henrique-Silva F., Maia A.A.M. Myxobolus cordeiroi n. sp., a parasite of Zungaro jahu (Siluriformes: Pimelodiade) from Brazilian Pantanal: morphology, phylogeny and histopathology. Vet. Parasitol. 2009, 162:221-229.
2. Adriano E.A., Carriero M.M., Maia A.A.M., Silva M.R.M., Naldoni J., Ceccarelli P.S., Arana S. Phylogenetic and host-parasite relationship analysis of Henneguya multiplasmodialis n. sp. infecting Pseudoplatystoma spp. in Brazilian Pantanal wetland. Vet. Parasitol. 2012, 185:110-120.
3. Alvarez-Pellitero P. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet. Immunol. Immunopathol. 2008, 126:171-198.
4. Alvarez-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. Amandi A., Holt R., Fryer J. Observations on Myxobolus insidiosus (Myxozoa: Myxosporea) a parasite of salmonid fishes. Fish Pathol. 1985, 20:287-304.
6. Angelucci G., Viale I., Fenza A., Salati F. Fish-farm application of a direct prophylaxis plan against flexibacteriosis and myxosporidiosis. Bull. Eur. Assoc. Fish Pathol. 2008, 28:245-251.
7. Antonio D., Andree K., McDowell T., Hedrick R. Detection of Myxobolus cerebralis in rainbow trout and oligochaete tissues by using a nonradioactive in situ hybridization (ISH) protocol. J. Aquat. Anim. Health 1998, 10:338-347.
8. Arkush K., Hedrick R. Experimental transmission of PKX, the causative agent of proliferative kidney disease, to three species of Pacific salmon. J. Appl. Ichthyol. 1990, 6:237-243.
9. Athanassopoulou F., Karagouni E., Dotsika E., Ragias V., Tavla J., Christofilloyanis P., Vatsos I. Efficacy and toxicity of orally administrated anti-coccidial drugs for innovative treatments of Myxobolus sp. infection in Puntazzo puntazzo. Dis. Aquat. Organ. 2004, 62:217-226.
10. Baerwald M., Petersen J., Hedrick R., Schisler G., May B. A major effect quantitative trait locus for whirling disease resistance identified in rainbow trout (Oncorhynchus mykiss). Heredity 2010, 106:920-926.
11. Bartholomew J. Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. J. Aquat. Anim. Health 1998, 10:112-120.
12. Bartholomew J.L., Smith C.E., Rohovec J.S., Fryer J.L. Characterization of a host response to the myxosporean parasite, Ceratomyxa shasta (Noble), by histology, scanning electron microscopy and immunological techniques. J. Fish Dis. 1989, 12:509-522.
13. Bartholomew J., Whipple M., Stevens D., Fryer J. The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. J. Parasitol. 1997, 83:859-868.
14. Bartholomew J.L., Ray E., Torell B., Whipple M.J., Heidel J.R. Monitoring Ceratomyxa shasta infection during a hatchery rearing cycle: comparison of molecular, serological and histological methods. Dis. Aquat. Organ. 2004, 62:85-92.
15. Baska F., Voronin V.N., Eszterbauer E., Muller L., Marton S., Molnar K. Occurrence of two myxosporean species, Myxobolus hakyi sp. n. and Hoferellus pulvinatus sp. n., in Pangasianodon hypophthalmus fry imported from Thailand to Europe as ornamental fish. Parasitol. Res. 2009, 105:1391-1398.
16. Belem A.M.G., Pote L.M. Portals of entry and systemic localization of proliferative gill disease organisms in channel catfish Ictalurus punctatus. Dis. Aquat. Organ. 2001, 48:37-42.
17. Bermudez R., Vigliano F., Marcaccini A., Sitjà-Bobadilla A., Quiroga M.I., Nieto J.M. Response of Ig-positive cells to Enteromyxum scophthalmi (Myxozoa) experimental infection in turbot, Scophthalmus maximus (L.): a histopathological and immunohistochemical study. Fish Shellfish Immunol. 2006, 21:501-512.
18. Bjork S., Bartholomew J. The effects of water velocity on the Ceratomyxa shasta infectious cycle. J. Fish Dis. 2009, 32:131-142.
19. Bjork S.J., Bartholomew J.L. Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. Int. J. Parasitol. 2010, 40:1087-1095.
20. Bütschli O. Myxosporidia, Bronn's Klassens und Ordnungen des Tierreichs 1882, 590-603. C.F. Winter, Leipzig. Second ed.
21. Calduch-Giner J.A., Sitjà-Bobadilla A., Davey G.C., Cairns M.T., Kaushik S., Perez-Sanchez J. Dietary vegetable oils do not alter the intestine transcriptome of gilthead sea bream (Sparus aurata), but modulate the transcriptomic response to infection with Enteromyxum leei. BMC Genomics 2012, 13.
22. Canning E.U., Curry A., Feist S.W., Longshaw M., Okamura B. A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J. Eukaryot. Microbiol. 2000, 47:456-468.
23. Cobcroft J.M., Battaglene S.C. Ultraviolet irradiation is an effective alternative to ozonation as a sea water treatment to prevent Kudoa neurophila (Myxozoa: Myxosporea) infection of striped trumpeter, Latris lineata (Forster). J. Fish Dis. 2013, 36:57-65.
24. Cone D.K., Frasca S. Revised diagnosis, site of development, and lesions due to Myxobolus hyborhynchi (Myxozoa) parasitizing fathead minnow in Minnesota. J. Aquat. Anim. Health 2002, 14:209-215.
25. Cone D.K., Melendy J.S. Infections of Unicauda clavicauda (Kudo, 1934) (Myxozoa) in the skin of Notropis hudsonius (Cyprinidae) from Montana, with a synopsis of the genus Unicauda Davis, 1944. Folia Parasitol. 2000, 47:273-278.
26. Cuesta A., Muñoz P., Rodriguez A., Salinas I., Sitjà-Bobadilla A., Alvarez-Pellitero P., Esteban M.A., Meseguer J. Gilthead seabream (Sparus aurata L.) innate defence against the parasite Enteromyxum leei (Myxozoa). Parasitology 2006, 132:95-104.
27. Cuesta A., Salinas I., Rodriguez A., Muñoz P., Sitjà-Bobadilla A., Alvarez-Pellitero P., Meseguer J., Esteban M.A. Cell-mediated cytotoxicity is the main innate immune mechanism involved in the cellular defence of gilthead seabream (Teleostei: Sparidae) against Enteromyxum leei (Myxozoa). Parasite Immunol. 2006, 28:657-665.
28. Davey G.C., Calduch-Giner J.A., Houeix B., Talbot A., Sitjà-Bobadilla A., Prunet P., Perez-Sanchez J., Cairns M.T. Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei. Mol. Immunol. 2011, 48:2102-2112.
29. de Sant'Ana F.J.F., de Oliveira S.L., Rabelo R.E., Vulcani V.A.S., da Silva S.M.G., Ferreira J.A. Outbreaks of Piscinoodinium pillulare and Henneguya spp. infection in intensively raised Piaractus mesopotamicus in Southwestern Goias. Brazil. Pesqui. Vet. Bras. 2012, 32:121-125.
30. Diamant A. Fish-to-fish transmission of a marine myxosporean. Dis. Aquat. Organ. 1997, 30:99-105.
31. 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.
32. Dykova I., Lom J. Review of pathogenic myxosporeans in intensive culture of carp (Cyprinus carpio) in Europe. Folia Parasitol. 1988, 35:289-&.
33. El-Matbouli M., Hoffmann R., Mandok C. Light and electron microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. J. Fish Biol. 1995, 46:919-935.
34. El-Matbouli M., Hoffmann R., Schoel H., McDowell T., Hedrick R. Whirling disease: host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and rainbow trout Oncorhynchus mykiss. Dis. Aquat. Organ. 1999, 35:1-12.
35. Estensoro I., Calduch-Giner J.A., Kaushik S., Perez-Sanchez J., Sitjà-Bobadilla A. Modulation of the IgM gene expression and IgM immunoreactive cell distribution by the nutritional background in gilthead sea bream (Sparus aurata) challenged with Enteromyxum leei (Myxozoa). Fish Shellfish Immunol. 2012, 33:401-410.
36. Estensoro I., Jung-Schroers V., Álvarez-Pellitero P., Steinhagen D., Sitjà-Bobadilla A. Effects of Enteromyxum leei (Myxozoa) infection on gilthead sea bream (Sparus aurata)(Teleostei) intestinal mucus: glycoprotein profile and bacterial adhesion. Parasitol. Res. 2013, 112:567-576.
37. Eszterbauer E., Sipos D., Forro B., Bartosova P., Holzer A.S. Molecular characterization of Sphaerospora molnari (Myxozoa), the agent of gill sphaerosporosis in common carp Cyprinus carpio carpio. Dis. Aquat. Organ. 2013, 104:59-67.
38. Feist S.W., Longshaw M., Canning E.U., Okamura B. Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Dis. Aquat. Organ. 2001, 45:61-68.
39. Ferguson J.A., Atkinson S.D., Whipps C.M., Kent M.L. Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. J. Parasitol. 2008, 94:1322-1334.
40. 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.
41. Fomena A., Abakar O., Ngassam P., Bouix G. Three new species of Myxosporidia (Myxozoa: Myxosporea) parasites of Citharinus citharus (Geoffroy Saint-Hilaire, 1809) (Citharinidae) in Chad (Central Africa). Parasite-J. Soc. Fr. Parasitol. 2004, 11:83-88.
42. Foott J.S., Hedrick R.P. Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. J. Fish Biol. 1987, 30:477-483.
43. Funk V.A., Olafson R.W., Raap M., Smith D., Aitken L., Haddow J.D., Wang D., Dawson-Coates J.A., Burke R.D., Miller K.M. Identification, characterization and deduced amino acid sequence of the dominant protease from Kudoa paniformis and K. thyrsites: a unique cytoplasmic cysteine protease. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 2008, 149:477-489.
44. 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.
45. Golomazou E., Athanassopoulou F., Karagouni E., Vagianou S., Tsantilas H., Karamanis D. Efficacy and toxicity of orally administrated anti-coccidial drug treatment on Enteromyxum leei infections in sharpsnout seabream (Diplodus puntazzo C.). Isr. J. Aquac. -Bamidgeh 2006, 58:157-169.
46. Grabner D.S., El-Matbouli M. Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) portal of entry into the fish host. Dis. Aquat. Organ. 2010, 90:197-206.
47. Griffin M.J., Pote L.M., Wise D.J., Greenway T.E., Mauel M.J., Camus A.C. A novel Henneguya species from channel catfish described by morphological, histological, and molecular characterization. J. Aquat. Anim. Health 2008, 20:127-135.
48. Griffin M.J., Khoo L.H., Torrans L., Bosworth B.G., Quiniou S.M., Gaunt P.S., Pote L.M. New Data on Henneguya pellis (Myxozoa: Myxobolidae), a parasite of blue catfish Ictalurus furcatus. J. Parasitol. 2009, 95:1455-1467.
49. Hallet S.L., Bartholomew J.L. Myxobolus cerebralis and Ceratomyxa shasta. Fish Parasites: Pathobiology and Protection 2012, CAB International, Wallingford. P.T.K. Woo, W.K. Buckmann (Eds.).
50. Hedrick R. Relationships of the host, pathogen, and environment: implications for diseases of cultured and wild fish populations. J. Aquat. Anim. Health 1998, 10:107-111.
51. Hedrick R.P., McDowell T.S., Marty G.D., Fosgate G.T., Mukkatira K., Myklebust K., El-Matbouli M. Susceptibility of two strains of rainbow trout (one with suspected resistance to whirling disease) to Myxobolus cerebralis infection. Dis. Aquat. Organ. 2003, 55:37-44.
52. Hedrick R.P., McDowell T.S., Adkison M.A., Myklebust K.A., Mardones F.O., Petri B. Invasion and initial replication of ultraviolet irradiated waterborne infective stages of Myxobolus cerebralis results in immunity to whirling disease in rainbow trout. Int. J. Parasitol. 2012, 42:657-666.
53. Hemananda T., Mohilal N., Bandyopadhyay P.K., Mitra A.K. Two new Myxosporidia (Myxozoa: Myxosporea) of the genus Myxobolus Butschli, 1882 from cornea of Clarias batrachus (Linnaeus, 1758) caught from a fish farm in India. North-West. J. Zool. 2009, 5:165-169.
54. Henderson M., Okamura B. The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proc. R. Soc. B Biol. Sci. 2004, 271:1729-1736.
55. Hofer B. Uber die drehkrankheit der regenbogenforelle. Allgemeine Fischerei Zeitschrift 1903, 28:7-8.
56. Holzer A., Sommerville C., Wootten R. Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. J. Fish Dis. 2003, 26:647-655.
57. Ibarra A.M., Gall G.A.E., Hedrick R.P. Trials with fumagillin DCH and malachite green to control ceratomyxosis in rainbow trout (Oncorhynchus mykiss). Fish Pathol. 1990, 25:217-223.
58. Iversen E.S. A new myxosporidian, Myxosoma squamalis, parasite of some salmonoid fishes. J. Parasitol. 1954, 40:397-404.
59. Jiménez-Guri E., Philippe H., Okamura B., Holland P.W. Buddenbrockia is a cnidarian worm. Science 2007, 317:116-118.
60. Kallert D.M., Eszterbauer E., Erseus C., El-Matbouli M., Haas W. Life cycle studies of Myxobolus parviformis sp. n. (Myxozoa: Myxobolidae) from bream. Dis. Aquat. Org. 2005, 66:233-243.
61. Kallert D., Ponader S., Eszterbauer E., El-Matbouli M., Haas W. Myxozoan transmission via actinospores: new insights into mechanisms and adaptations for host invasion. Parasitology 2007, 134:1741-1750.
62. Kallert D.M., Eszterbauer E., Grabner D., El-Matbouli M. In vivo exposure of susceptible and non-susceptible fish species to Myxobolus cerebralis actinospores reveals non-specific invasion behaviour. Dis. Aquat. Organ. 2009, 84:123-130.
63. Kallert D.M., Ponader S., Adelt S., Kaese P., Geyer R., Haas W., El-Matbouli M. Analysis of rainbow trout Oncorhynchus mykiss epidermal mucus and evaluation of semiochemical activity for polar filament discharge in Myxobolus cerebralis actinospores. J. Fish Biol. 2010, 77:1579-1598.
64. Kaltner H., Stippl M., Knaus M., El-Matbouli M. Characterization of glycans in the developmental stages of Myxobolus cerebralis (Myxozoa), the causative agent of whirling disease. J. Fish Dis. 2007, 30:637-647.
65. Karlsbakk E., Sæther P., Hostlund C., Fjellsoy K., Nylund A. Parvicapsula pseudobranchicola n. sp. (Myxozoa), a myxosporidian infecting the pseudobranch of cultured Atlantic salmon (Salmo salar) in Norway. Bull. Eur. Assoc. Fish Pathol. 2002, 22:381-387.
66. Kelley G.O., Adkison M.A., Leutenegger C.M., Hedrick R.P. Myxobolus cerebralis: identification of a cathepsin Z-like protease gene (Myx CP-1) expressed during parasite development in rainbow trout, Oncorhynchus mykiss. Exp. Parasitol. 2003, 105:201-210.
67. Kelley G.O., Zagmutt-Vergara F.J., Leutenegger C.M., Adkison M.A., Baxa D.V., Hedrick R.P. Identification of a serine protease gene expressed by Myxobolus cerebralis during development in rainbow trout Oncorhynchus mykiss. Dis. Aquat. Organ. 2004, 59:235-248.
68. Kent M.L., Hedrick R.P. PKX, the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa1. J. Eukaryot. Microbiol. 1985, 32:254-260.
69. Kent M., Margolis L., Corliss J. The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protest phylum Myxozoa Grassé, 1970. Can. J. Zool. 1994, 72:932-937.
70. Koehler A., Romans P., Desser S., Ringuette M. Encapsulation of Myxobolus pendula (myxosporidia) by epithelioid cells of its cyprinid host Semotilus atromaculatus. J. Parasitol. 2004, 90:1401-1405.
71. Liyanage Y.S., Yokoyama H., Matoyama H., Hosoya H., Wakabayashi H. Experimentally induced hemorrhagic thelohanellosis of carp caused by Thelohanellus hovorkai (Myxosporea: Myxozoa). Fish Pathol. 1998, 33:489-494.
72. Lom J., Dykova I. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 2006, 53:1-36.
73. Longshaw M., Le Deuff R.M., Harris A.F., Feist S.W. Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans. J. Fish Dis. 2002, 25:443-449.
74. Losada A.P., Bermudez R., Failde L.D., Quiroga M.I. Quantitative and qualitative evaluation of iNOS expression in turbot (Psetta maxima) infected with Enteromyxum scophthalmi. Fish Shellfish Immunol. 2012, 32:243-248.
75. Lovy J., Goodwin A.E., Speare D.J., Wadowska D.W., Wright G.M. Histochemical and ultrastructural analysis of pathology and cell responses in gills of channel catfish affected with proliferative gill disease. Dis. Aquat. Organ. 2011, 94:125-134.
76. Lu Y.S., Nie P., Sun B.J. Detection of Myxobolus rotundus (Myxozoa: Myxosporea) in skin mucus of crucian carp Carassius auratus auratus using a monoclonal antibody. Dis. Aquat. Organ. 2003, 54:171-173.
77. MacConnell, E., Bartholomew, J., 2010. Whirling Disease of Salmonids. In: AFS-FHS (Ed.), FHS Blue Book: Suggested Procedures for the Detection and Identification of Certain Finfish and Shellfish Pathogens. AFS-FHS, Bethesda, Maryland.
78. MacConnell, E., Vincent, E.R., 2002. The effects of Myxobolus cerebralis on the salmonid host, American Fisheries Society Symposium Series. Bethesda, Maryland.
79. Manning B.B., Griffin M.J., Khoo L.H., Wise D.J., Greenway T. Palatability of diets for channel catfish that contain amprolium or salinomycin using feed conversion ratio as the criterion. N. Am. J. Aqualcult. 2013, 75:99-101.
80. Markiw M.E. Portals of entry for salmonid whirling disease in rainbow trout. Dis. Aquat. Organ. 1989, 6:7-10.
81. Markiw M.E., Wolf K. Myxosoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worm (Annelida: Oligochaeta) in its life cycle. J. Eukaryot. Microbiol. 1983, 30:561-564.
82. Martínez Cruz P., Ibáñez A.L., Monroy Hermosillo O.A., Saad R., Hugo C. Use of probiotics in aquaculture. ISRN Microbiology 2012, 2012.
83. Martone C.B., Spivak E., Busconi L., Folco E.J.E., Sanchez J.J. A cysteine protease from myxosporean degrades host myofibrils in vitro. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1999, 123:267-272.
84. Masoumian M., Barzegar M., Mehdipoor M., Asadollah S., Jalali B. Myxobolus spp. (Myxdsporea: Myxobolidea) from fishes of the Zayandeh-rud river (Esfahan, Iran); new hosts and locality record. Iran. J. Fish. Sci. 2007, 7:89-100.
85. McGeorge J., Sommerville C., Wootten R. Epizootiology of Sphaerospora truttae (Myxozoa: Myxosporea) infections of Atlantic salmon salmo salar at freshwater smolt producing hatcheries in Scotland. Dis. Aquat. Organ. 1996, 26:33-41.
86. Molnar M. Site preference of myxosporean spp. on the fins of some Hungarian fish species. Dis. Aquat. Organ. 2002, 52:123-128.
87. Morris D.J., Adams A. Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease, to the freshwater bryozoan Fredericella sultana. Parasitol. Cambridge 2006, 133:701.
88. Morris D., Adams A., Richards R. In situ hybridisation identifies the gill as a portal of entry for PKX (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids. Parasitol. Res. 2000, 86:950-956.
89. Muñoz P., Cuesta A., Athanassopoulou F., Golomazou H., Crespo S., Padros F., Sitjà-Bobadilla A., Albinana G., Esteban M.A., Alvarez-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.
90. Naldoni J., Arana S., Maia A.A.M., Ceccarelli P.S., Tavares L.E.R., Borges F.A., Pozo C.F., Adriano E.A. Henneguya pseudoplatystoma n. sp causing reduction in epithelial area of gills in the farmed pintado, a South American catfish: histopathology and ultrastructure. Vet. Parasitol. 2009, 166:52-59.
91. Nesnidal M.P., Helmkampf M., Bruchhaus I., El-Matbouli M., Hausdorf B. Agent of whirling disease meets orphan worm: phylogenomic analyses firmly place myxozoa in cnidaria. PLoS One 2013, 8:e54576.
92. Nichols K.M., Bartholomew J., Thorgaard G.H. Mapping multiple genetic loci associated with Ceratomyxa shasta resistance in Oncorhynchus mykiss. Dis. Aquat. Organ. 2003, 56:145-154.
93. Noble E.R. On a Myxosporidian (Protozoan) parasite of California trout. J. Parasitol. 1950, 36:457-460.
94. Obiekezie A., Schmahl G. Henneguya laterocapsulata Landsberg, 1987 (Myxosporea, Myxozoa) in cultured hybrid agrican catfish-ultrastructure of the parasite - host interface. Eur. J. Protistol. 1993, 29:38-41.
95. Olsen M.M., Kania P.W., Heinecke R.D., Skjoedt K., Rasmussen K.J., Buchmann K. Cellular and humoral factors involved in the response of rainbow trout gills to Ichthyophthirius multifiliis infections: molecular and immunohistochemical studies. Fish Shellfish Immunol. 2011, 30:859-869.
96. Ordas M.C., Castro R., Dixon B., Sunyer J.O., Bjork S., Bartholomew J., Korytar T., Kollner B., Cuesta A., Tafalla C. Identification of a novel CCR7 gene in rainbow trout with differential expression in the context of mucosal or systemic infection. Dev. Comp. Immunol. 2012, 38:302-311.
97. 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.
98. Palenzuela O., Redondo M., Lopez E., Álvarez-Pellitero P. Cultured sole, Solea senegalensis is susceptible to Enteromyxum scophthalmi, the myxozoan parasite causing turbot emaciative enteritis. Parassitologia 2007, 49:73.
99. Plant K.P., LaPatra S.E. Advances in fish vaccine delivery. Dev. Comp. Immunol. 2011, 35:1256-1262.
100. Pote L.M., Hanson L.A., Shivaji R. Small subunit ribosomal RNA sequences link the cause of proliferative gill disease in channel catfish to Henneguya n. sp. (Myxozoa: Myxosporea). J. Aquat. Anim. Health 2000, 12:230-240.
101. Pote L., Khoo L., Griffin M., Woo P., Buchmann K. Henneguya ictaluri. Fish parasites: pathobiology and protection 2012, 177-192.
102. Quigley D., McArdle J. Management and control of proliferative kidney disease (PKD) in a freshwater Atlantic salmon (Salmo salar L.) farm in Ireland: a case history. Fish Vet. J. 1998, 2:1-12.
103. Quiroga M., Redondo M., Sitjà-Bobadilla A., Palenzuela O., Riaza A., Macías A., Vázquez S., Pérez A., Nieto J., Álvarez-Pellitero P. Risk factors associated with Enteromyxum scophthalmi (Myxozoa) infection in cultured turbot, Scophthalmus maximus (L.). Parasitology 2006, 133:433-442.
104. Ray R.A., Holt R.A., Bartholomew J.L. Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath river salmonids. J. Parasitol. 2012, 98:520-526.
105. Redondo M.J., Alvarez-Pellitero P. Lectinhistochemical detection of terminal carbohydrate residues in the enteric myxozoan Enteromyxum leei parasitizing gilthead seabream Sparus aurata (Pisces: Teleostei): a study using light and transmission electron microscopy. Folia Parasitol. 2009, 56:259-267.
106. Redondo M.J., Alvarez-Pellitero P. Carbohydrate patterns in the digestive tract of Sparus aurata L. and Psetta maxima (L.)(Teleostei) parasitized by Enteromyxum leei and E. scophthalmi (Myxozoa). Parasitol. Int. 2010, 59:445-453.
107. Redondo M.J., Palenzuela O., Riaza A., Macias A., Alvarez-Pellitero P. Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. J. Parasitol. 2002, 88:482-488.
108. Redondo M.J., Palenzuela O., Alvarez-Pellitero P. Studies on transmission and life cycle of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Folia Parasitol. 2004, 51:188-198.
109. Redondo M.J., Cortadellas N., Palenzuela O., Alvarez-Pellitero P. Detection of carbohydrate terminals in the enteric parasite Enteromyxum scophthalmi (Myxozoa) and possible interactions with its fish host Psetta maxima. Parasitol. Res. 2008, 102:1257-1267.
110. Reimschuessel R., Gieseker C.M., Driscoll C., Baya A., Kane A.S., Blazer V.S., Evans J.J., Kent M.L., Moran J.D.W., Poynton S.L. Myxosporean plasmodial infection associated with ulcerative lesions in young-of-the-year Atlantic menhaden in a tributary of the Chesapeake Bay, and possible links to Kudoa clupeidae. Dis. Aquat. Organ. 2003, 53:143-166.
111. Rothwell J.T., Virgona J.L., Callinan R.B., Nicholls P.J., Langdon J.S. Occurrence of cutaneous infections of Myxobolus episquamalis (Myxozoa: Myxobolidae) in sea mullet, Mugil cephalus L, in Australia. Aust. Vet. J. 1997, 75:349-352.
112. Ryce, E.K.N., 2003. Factors affecting the resistance of juvenile rainbow trout to whirling disease. Montana State University-Bozeman.
113. Salinas I., Zhang Y.A., Sunyer J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 2011, 35:1346-1365.
114. Schmahl G., Obiekezie A., Raether W. Treatment of fish parasites. 11. Morphogenesis of Henneguya laterocapsulata Landsberg, 1987 (Myxosporea, Myxozoa), and the effects of a new triazine derivative, HOE 092 V, on its developmental stages: a light and electron microscopy study. Parasitol. Res. 1993, 79:667-674.
115. Sitjà-Bobadilla A. Fish immune response to Myxozoan parasites. Parasite-J. Soc. Fr. Parasitol. 2008, 15:420-425.
116. Sitjà-Bobadilla A. Living off a fish: a trade-off between parasites and the immune system. Fish Shellfish Immunol. 2008, 25:358-372.
117. Sitjà-Bobadilla A., Alvarez-Pellitero P. Sphaerospora testicularis sp. nov. (Myxosporea: Sphaerosporidae) in wild and cultured sea bass, Dicentrarchus labrax (L.), from the Spanish Mediterranean area. J. Fish Dis. 1990, 13:193-203.
118. Sitjà-Bobadilla A., Palenzuela O. Myxozoan Biology and Ecology. Fisheries and Aquaculture 2013, EOLSS, Oxford, UK. Committee, U.-E.J. (Ed.).
119. Sitjà-Bobadilla A., Redondo M.J., Macias M.A., Ferreiro I., Riaza A., Alvarez-Pellitero P. Development of immunohistochemistry and enzyme-linked immunosorbent assays for the detection of circulating antibodies against Enteromyxum scophthalmi (Myxozoa) in turbot (Scophthalmus maximus L.). Fish Shellfish Immunol. 2004, 17:335-345.
120. Sitjà-Bobadilla A., de Felipe M.C., Alvarez-Pellitero P. In vivo and in vitro treatments against Sparicotyle chrysophrii (Monogenea: Microcotylidae) parasitizing the gills of gilthead sea bream (Sparus aurata L.). Aquaculture 2006, 261:856-864.
121. Sitjà-Bobadilla A., Redondo M.J., Bermudez R., Palenzuela O., Ferreiro I., Riaza A., Quiroga I., Nieto J.M., Alvarez-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.
122. Sitjà-Bobadilla A., Diamant A., Palenzuela O., Alvarez-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.
123. Sitjà-Bobadilla A., Palenzuela O., Riaza A., Macias M.A., Alvarez-Pellitero P. Protective acquired immunity to Enteromyxum scophthalmi (myxozoa) is related to specific antibodies in Psetta maxima (L.) (teleostei). Scand. J. Immunol. 2007, 66:26-34.
124. Sitjà-Bobadilla A., Calduch-Giner J., Saera-Vila A., Palenzuela O., Alvarez-Pellitero P., Perez-Sanchez 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.
125. Smothers J.F., von Dohlen C.D., Smith L., Spall R. Molecular evidence that the myxozoan protists are metazoans. Science 1994, 265:1719-1721.
126. Szekely C., Hallett S.L., Atkinson S.D., Molnar K. Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Dis. Aquat. Org. 2009, 85:147-155.
127. Verschuere L., Rombaut G., Sorgeloos P., Verstraete W. Probiotic bacteria as biological control agents in aquaculture. Microbiol. Mol. Biol. Rev. 2000, 64:655-671.
128. Whipple M.J., Gannam A.L., Bartholomew J.L. Inability to control ceratomyxosis in rainbow trout and steelhead with oral treatments of glucan immunostimulant or the fumagillin analog TNP-470. N. Am. J. Aqualcult. 2002, 64:1-9.
129. Wolf K., Markiw M.E. Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 1984, 225:1449-1452.
130. Xu Z., Parra D., Gómez D., Salinas I., Zhang Y.A., von Gersdorff Jørgensen L., Heinecke R.D., Buchmann K., LaPatra S.E., Sunyer J.O. Teleost skin, an ancient mucosal surface that elicits gut-like mucosal immune responses. Proc. Natl. Acad. Sci. USA 2013, 110:13097-13102.
131. Yamamoto T., Sanders J. Light and electron microscopic observations of sporogenesis in the myxosporida, Ceratomyxa shasta (Noble, 1950). J. Fish Dis. 1979, 2:411-428.
132. Yanagida T., Sameshima M., Nasu H., Yokoyama H., Ogawa K. Temperature effects on the development of Enteromyxum spp. (Myxozoa) in experimentally infected tiger puffer, Takifugu rubripes (Temminck & Schlegel). J. Fish Dis. 2006, 29:561-567.
133. Yasuda H., Ooyama T., Iwata K., Tun T., Yokoyama H., Ogawa K. Fish-to-fish transmission of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathol. 2002, 37:29-33.
134. Yokoyama H., Shirakashi S. Evaluation of hyposalinity treatment on infection with Enteromyxum leei (Myxozoa) using anemonefish Amphiprion spp. as experimental host. Bull. Eur. Assoc. Fish Pathol. 2007, 27:74-78.
135. Yokoyama H., Ogawa K., Wakabayashi H. Chemoresponse of actinosporean spores of Myxobolus cultus to skin mucus of goldfish Carassius auratus. Dis. Aquat. Organ. 1995, 21:7-11.
136. Yokoyama H., Inoue D., Kumamaru A., Wakabayashi H. Myxobolus koi (Myxozoa: Myxosporea) forms large- and small-type 'cysts' in the gills of common carp. Fish Pathol. 1997, 32:211-217.
137. Yokoyama H., Grabner D., Shirakashi S. Transmission Biology of The Myxozoa. Health and Environment in Aquaculture 2012, 3-42. InTech, Rijeka, Croatia. E. Carvalho (Ed.).
138. Zhang Y.A., Salinas I., Li J., Parra D., Bjork S., Xu Z., LaPatra S.E., Bartholomew J., Sunyer J.O. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 2010, 11:827-835.