Analysis of rainbow trout Oncorhynchus mykiss epidermal mucus and evaluation of semiochemical activity for polar filament discharge in Myxobolus cerebralis actinospores

Journal of Fish Biology

Volumn 77, Issue 7, 2010, Pages 1579-1598

  Kallert, D M ^a   Ponader, S ^b   Adelt, S ^c   Kaese, P ^d   Geyer, R ^d   Haas, W ^b   El Matbouli, M ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF WUPPERTAL   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Attachment; Biochemical separation; Chemostimuli; Chromatography; Host finding; Myxozoa

Indexed keywords

ANIMAL; ANIMAL PARASITOSIS; ARTICLE; CHEMISTRY; CYTOLOGY; EPIDERMIS; FISH DISEASE; FRACTIONATION; HOST PARASITE INTERACTION; MUCUS; MYXOBOLUS; PARASITOLOGY; PHYSIOLOGY; RAINBOW TROUT;

ANIMALS; CHEMICAL FRACTIONATION; EPIDERMIS; FISH DISEASES; HOST-PARASITE INTERACTIONS; MUCUS; MYXOBOLUS; ONCORHYNCHUS MYKISS; PARASITIC DISEASES, ANIMAL;

MYXOBOLUS CEREBRALIS; MYXOZOA; ONCORHYNCHUS MYKISS;

EID: 78449313630     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2010.02785.x     Document Type: Article

References (46)

1. Adelt, S., Plettenburg, O., Stricker, R., Reiser, G., Altenbach, H. J. & Vogel, G. (1999). Enzyme-assisted total synthesis of the optical antipodes D-myo-inositol 3, 4, 5-trisphosphate and D-myo-inositol 1, 5, 6-trisphosphate: aspects of their structure-activity relationship to biologically active inositol phosphates. Journal of Medical Chemistry 42, 1262-1273.
2. Arsan, E. L. & Bartholomew, J. L. (2008). Potential for dissemination of the non-native salmonid parasite Myxobolus cerebralis in Alaska. Journal of Aquatic Animal Health 20, 136-149.
3. Asakawa, M. (1974). Sialic acid containing glycoprotein in the external mucus of eel, Anguilla japonica Temminck et Schlegel-II carbohydrate and amino acid composition. Bulletin of the Japanese Society for the Science of Fish 40, 303-308.
4. Barry, J. M. & O'Rourke, F. J. (1959). Species specificity of fish mucus. Nature 184, 2039.
5. Bernt, E. & Bergmeyer, H. U. (1970). Bestimmung von Harnstoff. In Methoden der Enzymatischen Analyse, 2nd edn (Bergmeyer, H. U., ed.), pp. 1659-1663. Weinheim: Chemie.
6. Bhavanandan, V. P. & Sheykhnazari, M. (1993). Adaptation of the periodate/resorcinol method for determination of sialic acids to a microassay using microtiter plate reader. Analytical Biochemistry 213, 438-440.
7. Bjork, S. J. & Bartholomew, J. L. (2009). Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon. Diseases of Aquatic Organisms 86, 29-37.
8. Bodennec, J., Koul, O., Aguado, I., Brichon, G., Zwingelstein, G. & Portoukalian, J. (2000). A procedure for fractionation of sphingolipid classes by solid-phase extraction on aminopropyl cartridges. Journal of Lipid Research 41, 1524-1531.
9. Cannon, Q. & Wagner, E. (2003). Comparison of discharge mechanisms of cnidarian cnidae and myxozoan polar capsules. Reviews in Fisheries Science 11, 185-219.
10. Carisano, A. (1985). Rapid and sensitive method for the determination of proline by reversed-phase high-performance liquid chromatography with automated pre-column fluorescence derivatization. Journal of Chromatography 318, 132-138.
11. Carlstedt, I., Sheehan, J., Corfield, A. & Galagher, J. (1985). Mucous glycoproteins: a gel of a problem. Essays in Biochemistry 20, 41-69.
12. Castell, J. V., Cervera, M. & Marco, R. (1979). A convenient micromethod for the assay of primary amines and proteins with fluorescamin. A reexamination of the conditions of reaction. Analytical Biochemistry 99, 379-391.
13. Clamp, J., Allen, A., Gibbons, R. A. & Roberts, G. (1978). Chemical aspects of mucus. British Medical Bulletin 34, 25-41.
14. Edge, A. S., Faltynek, C. R., Hof, L., Reichert, L. E. Jr. & Weber, P. (1981). Deglycosylation of glycoproteins by trifluoromethanesulfonic acid. Analytical Biochemistry 118, 131-137.
15. El-Matbouli, M., Hoffmann, R. W., Schoel, H., McDowell, T. S. & Hedrick, R. P. (1999). Whirling disease: host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 35, 1-12.
16. Eszterbauer, E., Kallert, D. M., 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.
17. Ferguson, H. W., Morrison, D., Ostland, V. E., Lumsden, J. & Byrne, P. (1992). Responses of mucus-producing cells in gill disease of rainbow trout (Oncorhynchus mykiss). Journal of Comparative Pathology 106, 255-265.
18. Fischbach, A., Adelt, S., Müller, A. & Vogel, G. (2006). Disruption of inositol biosynthesis through targeted mutagenesis in Dictyostelium discoideum: generation and characterization of inositol-auxotrophic mutants. The Biochemical Journal 397, 509-518.
19. Folch, J., Lees, M. & Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497-509.
20. Fürst, P., Pollack, L., Graser, T. A., Godel, H. & Stehle, P. (1990). Appraisal of four pre-column derivatization methods for the high-performance liquid chromatographic determination of free amino acids in biological materials. Journal of Chromatography 499, 557-569.
21. Geyer, R. & Geyer, H. (1994). Saccharide linkage analysis using methylation and other techniques. Methods in Enzymology 230, 86-108.
22. 2 und pH auf das Fixationsverhalten der Cercarie von Diplostomum spathaceum (Trematoda). Zeitschrift für Parasitenkunde 46, 53-60.
23. Haas, W. & Ostrowski de Núñez, M. (1988). Chemical signals of fish skin for the attachment response of Acanthostomum brauni cercariae. Parasitology Research 74, 552-557.
24. Haas, W., Granzer, M. & Garcia, E. G. (1987). Host identification by Schistosoma japonicum cercariae. Journal of Parasitology 73, 568-577.
25. Haas, W., Haberl, B., Hofmann, M., Kerschensteiner, M. & Ketzer, U. (1999). Ichthyophthirius multifiliis invasive stages find their fish hosts with complex behaviour patterns and in response to different chemical signals. European Journal of Protistology 35, 129-135.
26. Haas, W., Stiegeler, P., Keating, A., Kullmann, B., Rabenau, H., Schönamsgruber, E. & Haberl, B. (2002). Diplostomum spathaceum cercariae respond to a unique profile of cues during recognition of their fish host. International Journal for Parasitology 32, 1145-1154.
27. Hallett, S. L., Lorz, H. V., Atkinson, S. D., Rasmussen, C., Xue, L. & Bartholomew, J. L. (2009). Propagation of the myxozoan parasite Myxobolus cerebralis by different geographic and genetic populations of Tubifex tubifex: an Oregon perspective. Journal of Invertebrate Pathology 102, 57-68.
28. Handy, R. D. (1989). The ionic composition of rainbow trout body mucus. Comparative Biochemistry and Physiology A 93, 571-576.
29. Kallert, D. M. & El-Matbouli, M. (2008). Differences in viability and reactivity of actinospores of three myxozoan species upon ageing. Folia Parasitologica 55, 105-110.
30. Kallert, D. M., El-Matbouli, M. & Haas, W. (2005). Polar filament discharge of Myxobolus cerebralis actinospores is triggered by combined non-specific mechanical and chemical cues. Parasitology 131, 609-616.
31. Kallert, D. M., 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. Diseases of Aquatic Organisms 84, 123-130.
32. Klesius, P. H., Shoemaker, C. A. & Evans, J. J. (2008). Flavobacterium columnare chemotaxis to channel catfish mucus. FEMS Microbiolical Letters 288, 216-220.
33. Mawhinney, T. P. & Chance, D. L. (1994). Hydrolysis of sialic acids and O-acetylated sialic acids with propionic acid. Analytical Biochemistry 223, 164-167.
34. Monsigny, M., Petit, C. & Roche, A. C. (1988). Colorimetric determination of neutral sugars by a resorcinol sulfuric acid micromethod. Analytical Biochemistry 175, 525-530.
35. Nakagawa, H., Hama, Y., Sumi, T., Li, S. C. & Li, Y. T. (2001). KDN-containing glycoprotein from loach skin mucus. Advances in Experimental Medicine and Biology 491, 171-184.
36. Nakagawa, H., Asakawa, M. & Enomoto, N. (1988). Diversity in the carbohydrate moieties of mucous glycoproteins of various fishes. Nippon Suisan Gakkaishi 54, 1653-1658.
37. Ohashi, H., Umeda, N., Hirazawa, N., Ozaki, Y., Miura, C. & Miura, T. (2007). Purification and identification of a glycoprotein that induces the attachment of oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae). International Journal for Parasitology 37, 1483-1490.
38. Rahemtulla, F. & Løvtrup, S. (1974). The comparative biochemistry of invertebrate mucopolysaccharides II. Nematoda; Annelida. Comparative Biochemistry and Physiology B 49, 639-646.
39. Roberts, S. D. & Powell, M. D. (2005). The viscosity and glycoprotein biochemistry of salmonid mucus varies with species, salinity and the presence of amoebic gill disease. Journal of Comparative Biochemistry and Physiology B 175, 1-11.
40. Shirakashi, S. & El-Matbouli, M. (2009). Myxobolus cerebralis (Myxozoa), the causative agent of whirling disease, reduces fecundity and feeding activity of Tubifex tubifex (Oligochaeta). Parasitology 136, 603-613.
41. Siegenthaler, U. & Ritter, W. (1977). Eine rasche DC-Methode zum Nachweis von Mono- und Disacchariden in Milchmischgetränken und Joghurt. Mitteilungen aus dem Gebiete der Lebensmitteluntersuchung und Hygiene 68, 448-450.
42. Sitjà-Bobadilla, A. (2009). Can myxosporean parasites compromise fish and amphibian reproduction? Proceedings of the Royal Society B 22, 2861-2870.
43. Smith, M. (2001). Extrusion of polar filaments in Myxobolus cerebralis actinospores. The Ichthyogram 11, 3-5.
44. Starcher, B. (2001). A ninhydrin-based assay to quantitate the total protein content of tissue samples. Analytical Biochemistry 292, 125-129.
45. Stiegeler, P. (1997). Chemische Signale für das Verbleibeverhalten der Cercarien von Diplostomum pseudospathaceum am Fischwirt. Diploma Thesis, University of Erlangen-Nuremberg, Erlangen, Germany.
46. Yokoyama, H., Ogawa, K. & Wakabayashi, H. (1995). Chemoresponse of actinosporean spores of Myxobolus cultus to skin mucus of goldfish Carassius auratus. Diseases of Aquatic Organisms 21, 7-11.