Effects of Enteromyxum leei (Myxozoa) infection on gilthead sea bream (Sparus aurata) (Teleostei) intestinal mucus: Glycoprotein profile and bacterial adhesion

Parasitology Research

Volumn 112, Issue 2, 2013, Pages 567-576

  Estensoro, Itziar ^a   Jung Schroers, Verena ^b   Álvarez Pellitero, Pilar ^a   Steinhagen, Dieter ^b   Sitjà Bobadilla, Ariadna ^a  

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

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSAMINE; BETA GALACTOSAMINE; FUCOSE; GALACTOSAMINE; GLUCOSE; GLYCOPROTEIN; LECTIN; MANNOSE; MUCIN; NEURAMINIC ACID; UNCLASSIFIED DRUG;

AEROMONAS HYDROPHILA; ANIMAL TISSUE; ARTICLE; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ENTEROMYXUM LEEI; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL CHROMATOGRAPHY; GLYCOSYLATION; INTESTINAL MUCUS; MUCUS; MUCUS SECRETION; MYXOZOA; MYXOZOAN INFECTION; NONHUMAN; PARASITE ISOLATION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DETERMINATION; SPARUS AURATA; VIBRIO ALGINOLYTICUS;

AEROMONAS HYDROPHILA; ANIMALS; BACTERIAL ADHESION; CHROMATOGRAPHY, GEL; FISH DISEASES; GLYCOPROTEINS; MUCUS; MYXOZOA; PARASITIC DISEASES, ANIMAL; SEA BREAM; VIBRIO ALGINOLYTICUS;

AEROMONAS HYDROPHILA; ARCHOSARGUS RHOMBOIDALIS; BACTERIA (MICROORGANISMS); ENTEROMYXUM LEEI; MYXOSPOREA; MYXOZOA; SPARUS AURATA; TELEOSTEI; VERTEBRATA; VIBRIO ALGINOLYTICUS;

EID: 84878372441     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-012-3168-3     Document Type: Article

References (51)

1. Álvarez-Pellitero P (2011) Mucosal intestinal immunity and response to parasite infections in ectothermic vertebrates. Immunology and immune system disorders. Nova Science Publishers, Inc, New York
2. Álvarez-Pellitero P, Palenzuela O, Sitjà-Bobadilla A (2008) Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol Int 57:110-120
3. Ascencio F, Martínez-Arias W, Romero MJ, Wadstrom T (1998) Analysis of the interaction of Aeromonas caviae, A. hydrophila and A. sobria with mucins. FEMS Immunol Med Microbiol 20:219-229. doi: 10.1111/j.1574-695X. 1998.tb01130.x
4. Balebona MC, Moriñigo MA, Faris A, Krovacek K, Mansson I, Bordas MA, Borrego JJ (1995) Influence of salinity and Ph on the adhesion of pathogenic Vibrio strains to Sparus aurata skin mucus. Aquaculture 132:113-120
5. Bansil R, Turner BS (2006) Mucin structure, aggregation, physiological functions and biomedical applications. Curr Opin Colloid Interface Sci 11:164-170. doi: 10.1016/j.cocis.2005.11.001
6. Bergstrom KSB, Guttman JA, Rumi M, Ma CX, Bouzari S, Khan MA, Gibson DL, Vogl AW, Vallance BA (2008) Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun 76:796-811
7. Bergstrom KSB, Kissoon-Singh V, Gibson DL, Ma CX, Montero M, Sham HP, Ryz N, Huang TN, Velcich A, Finlay BB, Chadee K, Vallance BA (2010) Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog 6. doi: 10.1371/journal.ppat. 1000902
8. Bordas MA, Balebona MC, Chabrillon M, Rodriguez-Maroto JM, Morinigo MA (2003) Influence of temperature and salinity on the adhesion to mucous surfaces of gilt-head seabream (Sparus aurata L.) of pathogenic strains of Vibrio alginolyticus and Listonella anguillarum. Bull Eur Assoc Fish Pathol 23:273-280
9. Carrasson M, Grau A, Dopazo LR, Crespo S (2006) A histological, histochemical and ultrastructural study of the digestive tract of Dentex dentex (Pisces, Sparidae). Histol Histopathol 21:579-593
10. Cheng YF, Li MY, Wang SR, Peng HJ, Reid S, Ni NT, Fang H, Xu WF, Wang BH (2010) Carbohydrate biomarkers for future disease detection and treatment. Sci China Chem 53:3-20
11. Cuadrado M (2009) Enteromixosi produïda per Enteromyxum leei (Diamant, Lom i Dyková, 1994) en espàrids d'interès comercial del Mediterrani. Ph. D. Thesis, Universitat Autònoma de Barcelona, Barcelona
12. Dezfuli BS, Pironi F, Campisi M, Shinn AP, Giari L (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. J Fish Dis 33:481-488. doi: 10.1111/j.1365-2761.2010.01146.x
13. Diamant A (1997) Fish-to-fish transmission of a marine myxosporean. Dis Aquat Org 30(2):99-105
14. Domeneghini C, Straini RP, Veggetti A (1998) Gut glycoconjugates in Sparus aurata L. (Pisces, Teleostei). A comparative histochemical study in larval and adult ages. Histol Histopathol 13:359-372
15. Enss ML, Schmidtwittig U, Heim HK, Sewing KF (1995) Prostaglandin E(2) alters terminal glycosylation of high-molecular-weight glycoproteins released by pig gastric mucous cells in-vitro. Prostag Leukot Ess Fat Acids 52:333-340
16. Estensoro I, Bermúdez R, Losada AP, Quiroga MI, Álvarez-Pellitero P, Sitjà-Bobadilla A (2009) Effect of Enteromyxum leei (Myxozoa) on gastrointestinal neuromodulators and cell apoptosis of gilthead sea bream (Sparus aurata). In: Book of abstracts of the 14th European Association of Fish Pathologists International Conference, Prague, Czech Republic, p 264
17. Estensoro I, Redondo MJ, Álvarez-Pellitero P, Sitjà- Bobadilla A (2010) Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis Aquat Org 92:51-58
18. Estensoro I, Benedito-Palos L, Palenzuela O, Kaushik S, Sitjà-Bobadilla A, Pérez-Sánchez J (2011) The nutritional background of the host alters the disease course in a fish-myxosporean system. Vet Parasitol 175:141-150. doi: 10.1016/j.vetpar.2010.09.015
19. Estensoro I, Redondo MJ, Salesa B, Kaushik S, Pérez-Sánchez J, Sitjà-Bobadilla A (2012a) 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). Dis Aquat Org. doi: 10.3354/dao02486
20. Estensoro I, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J, Sitjà-Bobadilla A (2012b) 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 Shellfish Immunol 33:401-410. doi: 10.1016/j.fsi.2012.05.029
21. Fleurance R, Sauvegrain C, Marques A, Le Breton A, Guereaud C, Cherel Y, Wyers M (2008) Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis Aquat Org 79:219-228
22. Hicks SJ, Theodoropoulos G, Carrington SD, Corfield AP (2000) The role of mucins in host-parasite interactions. Part I - protozoan parasites. Parasitol Today 16(11):476-481
23. Huang ZH, Ma AJ, Wang XA (2011) The immune response of turbot, Scophthalmus maximus (L.), skin to high water temperature. J Fish Dis 34:619-627
24. Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319-330
25. Leknes IL (2010) Histochemical study on the intestine goblet cells in cichlid and poecilid species (Teleostei). Tissue Cell 42:61-64. doi: 10.1016/j.tice.2009.09.001
26. Lodemel JB, Mayhew TM, Myklebust R, Olsen RE, Espelid S, Ringo E (2001) Effect of three dietary oils on disease susceptibility in Arctic charr (Salvelinus alpinus L.) during cohabitant challenge with Aeromonas salmonicida ssp salmonicida. Aquac Res 32:935-945. doi: 10.1046/j.1365-2109.2001.00621.x
27. Losada AP, Bermúdez R, Faílde LD, Quiroga MI (2012) Quantitative and qualitative evaluation of iNOS expression in turbot (Psetta maxima) infected with Enteromyxum scophthalmi. Fish Shellfish Immunol 32:243-248. doi: 10.1016/j.fsi.2011.11.007
28. Magnadottir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137-151. doi: 10.1016/j.fsi.2004.09.006
29. Neuhaus H, van der Marel M, Caspari N, Meyer W, Enss M-L, Steinhagen D (2007a) Biochemical and histochemical effects of perorally applied endotoxin on intestinal mucin glycoproteins of the common carp Cyprinus carpio. Dis Aquat Org 77:17-27. doi: 10.3354/dao01836
30. Neuhaus H, van der Marel M, Caspari N, Meyer W, Enss ML, Steinhagen D (2007b) Biochemical and histochemical study on the intestinal mucosa of the common carp Cyprinus carpio L., with special consideration of mucin glycoproteins. J Fish Biol 70:1523-1534
31. Palenzuela O (2006) Myxozoan infections in Mediterranean mariculture. Parassitologia 48(1-2):27-29
32. Pedini V, Scocco P, Gargiulo AM, Ceccarelli P, Lorvik S (2002) Glycoconjugate characterization in the intestine of Umbrina cirrosa by means of lectin histochemistry. J Fish Biol 61:1363-1372. doi: 10.1111/j.1095-8649.2002. tb02482.x
33. Redondo MJ, Álvarez-Pellitero P (2009) Lectin histochemical 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 56:259-267
34. Redondo MJ, Álvarez-Pellitero P (2010) 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 59:445-453
35. Rigos G, Katharios P (2010) Pathological obstacles of newly-introduced fish species in Mediterranean mariculture: a review. Rev Fish Biol Fisher 20:47-70
36. Roberts SD, Powell MD (2005) The viscosity and glycoprotein biochemistry of salmonid mucus varies with species, salinity and the presence of amoebic gill disease. J Comp Physiol B-Biochem Syst Environ Physiol 175:1-11. doi: 10.1007/s00360-004-0453-1
37. Rodríguez I, Novoa B, Figueras A (2008) Immune response of zebrafish (Danio rerio) against a newly isolated bacterial pathogen Aeromonas hydrophila. Fish Shellfish Immunol 25:239-249. doi: 10.1016/j.fsi.2008.05.002
38. Roussel P, Delmotte P (2004) The diversity of epithelial secreted mucins. Curr Org Chem 8:413-437. doi: 10.2174/1385272043485846
39. Sahoo PK, Das Mahapatra K, Saha JN, Barat A, Sahoo M, Mohanty BR, Gjerde B, Odegard J, Rye M, Salte R (2008) Family association between immune parameters and resistance to Aeromonas hydrophila infection in the Indian major carp, Labeo rohita. Fish Shellfish Immunol 25:163-169. doi: 10.1016/j.fsi.2008.04.003
40. Sarasquete C, Gisbert E, Ribeiro L, Vieira L, Dinis MT (2001) Glyconjugates in epidermal, branchial and digestive mucous cells and gastric glands of gilthead sea bream, Sparus aurata, Senegal sole, Solea senegalensis and Siberian sturgeon, Acipenser baeri development. Eur J Histochem 45:267-278
41. Schroers V, Van der Marel M, Steinhagen D (2008) Influence of carp intestinal mucus molecular size and glycosylation on bacterial adhesion. Dis Aquat Org 81:135-142. doi: 10.3354/dao01947
42. Schroers V, Van der Marel M, Neuhaus H, Steinhagen D (2009) Changes of intestinal mucus glycoproteins after peroral application of Aeromonas hydrophila to common carp (Cyprinus carpio). Aquaculture 288:184-189
43. Sitjà-Bobadilla A, Palenzuela O (2012) Enteromyxum species. In: Woo PTK, Buchmann K (eds) Fish parasites: pathology and protection. CAB International, Oxfordshire, pp 163-176
44. Sitjà-Bobadilla A, Diamant A, Palenzuela O, 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.). J Fish Dis 30:243-250
45. Sitjà-Bobadilla A, Calduch-Giner J, Saera-Vila A, Palenzuela O, Álvarez-Pellitero P, 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 Shellfish Immunol 24:610-619
46. Theodoropoulos G, Hicks SJ, Corfield AP, Miller BG, Carrington SD (2001) The role of mucins in host-parasite interactions: part II - helminth parasites. Trends Parasitol 17:130-135
47. Torrecillas S, Makol A, Caballero MJ, Montero D, Gines R, Sweetman J, Izquierdo M (2011) Improved feed utilization, intestinal mucus production and immune parameters in sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Aquac Nutr 17:223-233. doi: 10.1111/j.1365-2095.2009.00730.x
48. Tse SK, Chadee K (1991) The interaction between intestinal mucus glycoproteins and enetric infections. Parasitol Today 7:163-172. doi: 10.1016/0169-4758(91)90121-4
49. Van der Marel M, Schroers V, Neuhaus H, Steinhagen D (2008) Chemotaxis towards, adhesion to, and growth in carp gut mucus of two Aeromonas hydrophila strains with different pathogenicity for common carp, Cyprinus carpio L. J Fish Dis 31:321-330
50. Van der Marel M, Caspari N, Neuhaus H, Meyer W, Enss ML, Steinhagen D (2010) Changes in skin mucus of common carp, Cyprinus carpio L., after exposure to water with a high bacterial load. J Fish Dis 33:431-439
51. Vesterlund S, Paltta J, Karp M, Ouwehand AC (2005) Adhesion of bacteria to resected human colonic tissue: quantitative analysis of bacterial adhesion and viability. Res Microbiol 156:238-244. doi: 10.1016/j.resmic.2004.08.012