3D morphology, ultrastructure and development of ceratomyxa puntazzi stages: First insights into the mechanisms of motility and budding in the myxozoa

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Alama Bermejo, Gema ^a   Bron, James Emmanuel ^b   Raga, Juan Antonio ^a   Holzer, Astrid Sibylle ^a,c  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF STIRLING   (United Kingdom)

^c INSTITUTE OF PARASITOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; 4',6 DIAMIDINO 2 PHENYLINDOLE; INDOLE DERIVATIVE; NILE RED; OXAZINE DERIVATIVE; PHALLOIDIN;

ARTICLE; BILE; CELL COMPOSITION; CELL FATE; CELL ULTRASTRUCTURE; CERATOMYXA PUNTAZZI; CONFOCAL LASER MICROSCOPY; CYTOKINESIS; CYTOSKELETON; DEVELOPMENTAL STAGE; DIPLODUS PUNTAZZO; FILOPODIUM; FISH; LOCOMOTION; MICROBIAL MORPHOLOGY; MYXOZOA; NONHUMAN; PARASITE BUDDING; PARASITE DEVELOPMENT; PARASITE MOTILITY; POLARIZATION; PRE SPOROGONIC PROLIFERATION; PROTEIN LOCALIZATION; SCANNING ELECTRON MICROSCOPY; SPOROGENESIS; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ANIMAL PARASITOSIS; BACTERIAL SPORE; CELL DIVISION; CELL MOTION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; FISH DISEASE; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; METHODOLOGY; PARASITOLOGY; PHYSIOLOGY; PSEUDOPODIUM; SEA BREAM; STAINING; ULTRASTRUCTURE;

CERATOMYXA; DIPLODUS PUNTAZZO; EUKARYOTA; MYXOZOA; PISCES;

ANIMALS; BILE; CELL DIVISION; CELL MOVEMENT; CELL PROLIFERATION; FISH DISEASES; INDOLES; LIFE CYCLE STAGES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MYXOZOA; OXAZINES; PARASITIC DISEASES, ANIMAL; PHALLOIDINE; PSEUDOPODIA; SEA BREAM; SPORES; STAINING AND LABELING;

EID: 84857680559     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032679     Document Type: Article

References (61)

1. Hickman CP, Roberts LS, Keen SL, Larson A, l'Anson H, et al. (2009) Soporte, protección y movimiento. In: Hickman CP, Roberts LS, Keen SL, Larson A, l'Anson H, editors. Principios integrales de Zoología McGraw-Hill pp. 654-655 (in Spanish).
2. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
3. Mitchison TJ, (1995) Evolution of a dynamic cytoskeleton. Philo T Roy Soc B 349: 299-304.
4. Small JV, Rottner K, (2002) Elementary cellular processes driven by actin assembly: lamellipodia and filopodia. In: Carlier MF, editors. Actin-based motility: cellular, molecular and physical aspects Springer pp. 3-33.
5. Charras G, Paluch E, (2008) Blebs lead the way: how to migrate without lamellipodia. Nature rev mol cell biol 9: 730-736.
6. Pelham RJ, Chang F, (2002) Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature 419: 82-86.
7. Uyeda TQP, Nagasaki A, (2004) Variations on a theme: the many modes of cytokinesis. Curr Opin Cell Biol 16: 55-60.
8. Neujahr R, Heizer C, Gerisch G, (1997) Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow. J Cell Sci 110: 123-137.
9. Burton K, Taylor DL, (1997) Traction forces of cytokinesis measured with optically modified elastic substrata. Nature 385: 450-454.
10. Borisy GG, Svitkina TM, (2000) Actin machinery: pushing the envelope. Curr Opin Cell Biol 12: 104-112.
11. Uyeda TQP, Kitayama C, Yumura S, (2000) Myosin II-independent cytokinesis in Dictyostelium: its mechanism and implications. Cell Struct Funct 25: 1-10.
12. Spudich JA, (1989) In pursuit of myosin function. Cell Regul 1: 1-11.
13. Uyeda TQP, Yumura S, (2000) Molecular biological approaches to study myosin functions in cytokinesis of Dictyostelium. Microsc Res Tech 49: 136-144.
14. Hibi M, Nagasaki A, Takahashi M, Yamagishi A, Uyeda TQP, (2004) Dictyostelium discoideum talin A is crucial for myosin II independent and adhesion-dependent cytokinesis. J Muscle Res Cell Motil 25: 127-140.
15. Tumova P, Kulda J, Nohynková E, (2007) Cell division of Giardia intestinalis: assembly and disassembly of the adhesive disc, and the cytokinesis. Cell motil cytoskeleton 64: 288-298.
16. Hammarton TC, Monnerat S, Mottram JC, (2007) Cytokinesis in trypanosomatids. Curr Opin Microbiol 10: 520-527.
17. Hofer B, (1903) Über die drehkrankheit der regenbogenforelle. Allgemeinen Fischerei-Ztg., Jahrg 28: 7-8 (in German).
18. Bartholomew JL, Rohovec JS, Fryer JL, (1989) Ceratomyxa shasta, a myxosporean parasite of salmonids. In: Fish Disease Leaflet, F.W.S. 80.
19. Bartholomew JL, Ray E, Torell B, Whipple MJ, Heidel JR, (2004) Monitoring Ceratomyxa shasta infection during a hatchery rearing cycle: comparison of molecular, serological and histological methods. Dis Aquat Organ 62: 85-92.
20. Feist SW, Peeler EJ, Gardiner R, Smith E, Longshaw M, (2002) Proliferative kidney disease and renal myxosporidiosis in juvenile salmonids from rivers in England and Wales. J Fish Dis 25: 451-458.
21. Canning EU, Curry A, Anderson CL, Okamura B, (1999) Ultrastructure of Myxidium trachinorum sp. nov. from the gallbladder of the lesser weever fish Echiichthys vipera. Parasitol Res 85: 910-919.
22. Redondo MJ, Quiroga MI, Palenzuela O, Nieto JM, Alvarez-Pellitero P, (2003) Ultrastructural studies on the development of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot (Scophthalmus maximus L.). Parasitol Res 90: 192-202.
23. Noble ER, (1941) Nuclear cycles in the life history of the protozoan genus Ceratomyxa. J Morph 69: 455-479.
24. Meglitsch P, (1960) Some coelozoic myxosporidia from New Zealand fishes I.-General, and family Ceratomyxidae. T Roy Soc N Zeal 88: 265-356.
25. Sitjà-Bobadilla A, Palenzuela O, Alvarez-Pellitero P, (1995) Ceratomyxa sparusaurati n. sp. (Myxosporea: Bivalvulida), a new parasite from cultured gilthead seabream (Sparus aurata L.) (Teleostei: Sparidae): light and electron microscopic description. J Eukaryot Microbiol 42: 529-539.
26. Cho JB, Kwon SR, Kim SK, Nam YK, Kim KH, (2004) Ultrastructure and development of Ceratomyxa protopsettae Fujita, 1923 (Myxosporea) in the gallbladder of cultured olive flounder, Paralichthys olivaceus. Acta Protozool 43: 241-250.
27. Grabner DS, El-Matbouli M, (2010) Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) portal of entry into the fish host. Dis Aquat Organ 90: 197-206.
28. Eszterbauer E, Kallert DM, Grabner D, El-Matbouli M, (2009) Differentially expressed parasite genes involved in host recognition and invasion of the triactinomyxon stage of Myxobolus cerebralis (Myxozoa). Parasitology 136: 367-377.
29. Kallert DM, Eszterbauer E, Grabner D, El-Matbouli M, (2009) In vivo exposure of susceptible and non-susceptible fish species to Myxobolus cerebralis actinospores reveals non-specific invasion behaviour. Dis Aquat Organ 84: 123-130.
30. McGurk C, Morris DJ, Bron JE, Adams A, (2005) The morphology of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) spores released from Fredericella sultana (Bryozoa: Phylactolaemata). J Fish Dis 28: 307-312.
31. Alama-Bermejo G, Raga JA, Holzer AS, (2011) Host-parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet parasitol 182: 181-192.
32. Georgévitch J, (1917) Recherches sur le développement de Ceratomyxa herouardi Georgévitch. Arch zool exp gen 56: 375-399 (in French).
33. Georgévitch J, (1929) Recherches sur Ceratomyxa maenae nov. sp. Arch Protistenkd 65: 106-123 (in French).
34. Morrison CM, Martell DJ, Leggiadro C, O'Neil D, (1996) Ceratomyxa drepanopsettae in the gallbladder of Atlantic halibut, Hippoglossus hippoglossus, from the northwest Atlantic Ocean. Folia Parasit 43: 20-36.
35. Maíllo-Bellón PA, Gracia-Royo MP, (2007) Vegetative stages, sporogenesis and spore morphology of Ceratomyxa appendiculata, Thélohan, 1892 (Myxozoa: Bibalvulida), from the gall bladder of Lophius budegassa, Spinola, 1807 (Teleostei: Lophiidae). Acta Protozool 46: 247-256.
36. Lom J, Dyková I, (1996) Notes on the ultrastructure of two myxosporean (Myxozoa) species, Zschokkella pleomorpha and Ortholinea fluviatilis. Folia Parasit 43: 189-202.
37. Sitjà-Bobadilla A, Alvarez-Pellitero P, (1993) Zschokkella mugilis n. sp. (Myxosporea: Bivalvulida) from mullets (Teleostei: Mugilidae) of Mediterranean waters: Light and electron microscopic description. J Eukaryot Microbiol 40: 755-764.
38. Sitjà-Bobadilla A, Alvarez-Pellitero P, (2001) Leptotheca sparidarum n. sp. (Myxosporea: Bivalvulida), a parasite from cultured common dentex (Dentex dentex L.) and gilthead sea bream (Sparus aurata L.) (Teleostei: Sparidae). J Eukaryot Microbiol 48: 627-639.
39. Cuadrado M, Albinyana G, Padrós F, Redondo MJ, Sitjà-Bobadilla A, et al. (2007) An unidentified epi-epithelial myxosporean in the intestine of gilthead sea bream Sparus aurata L. Parasitol Res 101: 403-411.
40. Morris DJ, Adams A, (2008) Sporogony of Tetracapsuloides bryosalmonae in the brown trout Salmo trutta and the role of the tertiary cell during the vertebrate phase of myxozoan life cycles. Parasitology 135: 1075-1092.
41. Uspenskaya AV, Raikova OI, (2004) F-actin and beta-tubulin localization in the myxospore stinging apparatus of Myxobolus pseudodispar Gorbunova, 1936 (Myxozoa, Myxosporea). Tsitologiia 46: 748-754.
42. Alvarez-Pellitero P, Sitjà-Bobadilla A, (1993) Ceratomyxa spp. (Protozoa: Myxosporea) infections in wild and cultured sea bass (Dicentrarchus labrax) from the Spanish Mediterranean area. J Fish Biol 42: 889-901.
43. Palenzuela O, Sitjà-Bobadilla A, Alvarez-Pellitero P, (1997) Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead sea bream Sparus aurata (Pisces: Teleostei) from Spain: aspects of the host-parasite relationship. Parasitol Res 83: 539-548.
44. Reed CC, Basson L, Van As LL, Dyková I, (2007) Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol 54: 283-292.
45. Jiménez-Guri E, Philippe H, Okamura B, Holland PWH, (2007) Buddenbrockia is a cnidarian worm. Science 317: 116-118.
46. Jiménez-Guri E, Okamura B, Holland PWH, (2007) Origin and evolution of a myxozoan worm. Integr Comp Biol 47: 752-758.
47. Holland JW, Okamura B, Hartikainen H, Secombes CJ, (2010) A novel minicollagen gene links cnidarians and myxozoans. Proc R Soc B 278: 546-553.
48. Diamant A, Whipps CM, Kent ML, (2004) A new species of Spaheromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern red sea: morphology, ultrastructure, and phylogeny. J Parasitol 90: 1434-1442.
49. Ter Höfte BB, Körting W, Lehmann J, (1984) "C- und K- Protozoen", Endoparasiten unsicherer systematischer Zuordnung bei jungen Karpfen (Cyprinus carpio L.). Derzeitiger Wissensstand und bildliche Dokumentation. Fisch und Umwelt 13: 89-99.
50. Morris DJ, (2010) Cell formation by myxozoan species is not explained by dogma. Proc R Soc B 277: 2565-2570.
51. Cuadrado M, Marques A, Diamant A, Sitjà-Bobadilla A, Palenzuela O, Alvarez-Pellitero P, Padrós F, Crespo S, (2008) Ultrastructure of Enteromyxum leei (Diamant, Lom, and Dyková, 1994) (Myxozoa), an enteric parasite infecting gilthead sea bream (Sparus aurata) and sharpsnout sea bream (Diplodus puntazzo). J Eukaryot Microbiol 55: 178-184.
52. Adriano EA, Arana S, Cordeiro NS, (2005) Histology, ultrastructure and prevalence of Henneguya piaractus (Myxosporea) infecting the gills of Piaractus mesopotamicus (Characidae) cultivated in Brazil. Dis Aquat Organ 64: 229-235.
53. Sitjà-Bobadilla A, Alvarez-Pellitero P, (1993) Ultrastructural and cytochemical observations on the sporogenesis of Sphaerospora testicularis (Protozoa: Myxosporea) from Mediterranean sea bass, Dicentrarchus labrax (L.). Eur J Protistol 29: 219-229.
54. Sitjà-Bobadilla A, Alvarez-Pellitero P, (1992) Light and electron microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea: Sphaerosporidae) from wild and cultured sea bass, Dicentrarchus labrax L. J Protozool 39: 273-281.
55. Sitjà-Bobadilla A, Alvarez-Pellitero P, (1995) Light and electron microscopic description of Polysporoplasma n. g. (Myxosporea: Bivalvulida), Polysporoplasma sparis n. sp. from Sparus aurata (L.), and Polysporoplasma mugilis n. sp. from Liza aurata L. Eur J Protistol 31: 77-89.
56. Kudo RR, (1021) On the effect of some fixatives upon Myxosporidian spores. Trans Am Micr Soc 40: 161-167.
57. Parker JD, Warner MC, (1970) Effects of fixation, dehydration and staining on dimensions of myxosporidan. J wildlife dis 6: 448-456.
58. Casal G, Costa G, Azevedo C, (2007) Ultrastructural description of Ceratomyxa tenuispora (Myxozoa), a parasite of the marine fish Aphanopus carbo (Trichiuridae), from the Atlantic coast of Madeira Island (Portugal). Folia Parasitol 54: 165-171.
59. Sitjà-Bobadilla A, Alvarez-Pellitero P, (1996) Virus-like particles in Polysporoplasma mugilis (Protozoa: Myxosporea), parasitic in a marine fish (Liza aurata L.). Int J Parasitol 26: 457-459.
60. Alama-Bermejo G, Cuadrado M, Raga JA, Holzer AS, (2009) Morphological and molecular redescription of the myxozoan Unicapsula pflugfelderi Schubert, Sprague and Reinboth 1975 from two teleost hosts in the Mediterranean. A review of the genus Unicapsula Davis 1924. J Fish Dis 32: 335-350.
61. Fenteany G, Zhu S, (2003) Small-molecule inhibitors of actin dynamics and cell motility. Curr Top Med Chem 3: 593-616.