Folia Parasitologica, vol. 56 (2009), issue 4

Folia Parasitologica 56[4] 259-267 (2009) | DOI: 10.14411/fp.2009.030

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

María J. Redondo, Pilar Alvarez-Pellitero
Instituto de Acuicultura de Torre de la Sal, Consejo Superior de Investigaciones Científicas, 12595 Ribera de Cabanes, Castellón, Spain

The presence of terminal carbohydrate residues in Enteromyxum leei (Diamant, Lom et Dyková, 1994) Palenzuela, Redondo et Álvarez-Pellitero, 2002 stages in gilthead seabream intestines was studied at light microscopy (LM) and transmission electron microscopy (TEM) level using lectin histochemical techniques. Abundant mannose and/or glucose residues were demonstrated by the intense staining caused by binding of biotinylated concanavalin A (Con A), at both LM and TEM. A clear positivity was also obtained with Ulex europaeus (UEA I) agglutinin specific for fucose residues. Both lectins stained E. leei proliferative and sporogonic stages, though glycan patterns varied between these developmental stages. Wheat germ agglutinin (WGA) and Bandeiraea simplicifolia lectin I (BSL I) recognised only structures in the sporogonic stages. Faint labelling occurred with Glycine max (SBA) lectin. No staining was obtained with Sambucus nigra (SNA) agglutinin. The TEM studies demonstrated a restricted presence of N‑acetyl-D-galactosamine and α-D-galactose, whereas glucose/mannose and fucose, the dominant structures, were also present at the parasite membranes and host-parasite interface, suggesting a role in host-parasite interaction.

Keywords: Myxosporea, lectins, lectin-gold electron microscopy, histochemistry

Received: February 19, 2009; Accepted: July 21, 2009; Published: December 1, 2009


References

  1. Barbosa H.S., Nazareth M., Meirelles S.L. 1992: Ultrastructural detection in vitro of WGA-, RCAI-, and Con A-binding sites involved in the invasion of heart muscle cells by Trypanosoma cruzi. Parasitol. Res. 78: 404-409 Go to original source... Go to PubMed...
  2. Benchimol M., Bernardino M.V. 2002: Ultrastructural localization of glycoconjugates in Tritrichomonas foetus. Parasitol. Res. 88: 134-143 Go to original source... Go to PubMed...
  3. Cammarata M., Benenati G., Odom E.W., Salerno G., Vizzini A., Vasta G., Parrinello N. 2007: Isolation and characterization of a fish F-type lectin from a gilt head bream (Sparus aurata) serum. Biochim. Biophys. Acta 1770: 150-155 Go to original source... Go to PubMed...
  4. Casaravilla C., Malgor R., Carmona C. 2003: Characterization of carbohydrates of adult Echinococcus granulosus by lectinbinding analysis. J. Parasitol. 89: 57-61 Go to original source... Go to PubMed...
  5. Castagnaro M., Marin D e M ateo M., Ghittino C., Hedrick R.P. 1991: Lectin histochemistry and ultrastructure of rainbow trout Oncorhynchus mykiss kidneys affected by proliferative kidney disease. Dis. Aquat. Org. 10: 173-183 Go to original source...
  6. El-Matbouli M., Anders C., Hoffmann R.W., Kaltner K., Gabius H.-J. 2002: Detection of glycoconjugates and lectin-like activities in the causative agent of whirling disease. In: J.L. Bartholomew and J.C. Wilson (Eds.), Whirling Disease: Reviews and Current Topics. Symposium 29. American Fisheries Society, Bethesda, MD, pp. 55-60
  7. Fuchs N., Ingold K., Sonda S., Buetikofer P., Hemphill A. 1999: Detection of surface-associated and intracellular glycoconjugates and glycoproteins in Neospora caninum tachyzoites. Int. J. Parasitol. 29: 1597-1611 Go to original source... Go to PubMed...
  8. Fuller A.L., McDougald L.R. 2002: Lectin-binding by sporozoites of Eimeria tenella. Parasitol. Res. 88: 118-125 Go to original source... Go to PubMed...
  9. Ghittino C., Latini M., Agnetti F., Panzieri C., Lauro L., Ciappelloni R. 2003: Emerging pathologies in aquaculture: effects on production and food safety. Vet. Res. Commun. 27: 471-479 Go to original source... Go to PubMed...
  10. Golomazou E., Athanassopoulou F., Karagouni E., Tsagozis P., Tsantilas H., Vagianou S.T. 2006: 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 260: 44-53 Go to original source...
  11. Griffiths G. 1993: Fine Structure Immunocytochemistry. Springer-Verlag, New York, 459 pp
  12. Gruden-Movsesijan A., Milosavljevic L.J.S. 2006: The involvement of the macrophage mannose receptor in the innate immune response to infection with parasite Trichinella spiralis. Vet. Immunol. Immunopathol. 109: 57-67 Go to original source... Go to PubMed...
  13. Hammerschmidt K., Kurtz J. 2005: Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. Int. J. Parasitol. 35: 1499-1507 Go to original source... Go to PubMed...
  14. Hart G.W., West C.M. 2009: Nucleocytoplasmic glycosylation. In: A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart and M.E. Etzler (Eds.), Essentials of Glycobiology. Second Edition. Cold Spring Harbor, New York, pp. 17-1, 17-13
  15. Hokke C.H., Yazdanbakhsh M. 2005: Schistosome glycans and innate immunity. Parasite Immunol. 27: 257-264 Go to original source... Go to PubMed...
  16. Horak P. 1995: Developmentally regulated expression of surface carbohydrate residues on larval stages of the avian schistosome Trichobilharzia szidati. Folia Parasitol. 42: 255-265 Go to PubMed...
  17. Imberty A., Varrot A. 2008: Microbial recognition of human cell surface glycoconjugates. Curr. Opin. Struct. Biol. 18: 567-576. Go to original source... Go to PubMed...
  18. Iyer S.N., Hart G.W. 2003: Dynamic nuclear and cytoplasmic glycosylation: enzymes of O-GlcNAc cycling. Biochemistry 42: 2493-2499 Go to original source... Go to PubMed...
  19. Jacobson R.J., Doyle R.L. 1996: Lectin-parasite interactions. Parasitol. Today 12: 55-61 Go to original source... Go to PubMed...
  20. John N.M., Zea M.E., Kawano T., Omata Y., Saito A., Toyoda Y., Mikami T. 1999: Identification of carbohydrates on Eimeria stiedai sporozoites and their role in the invasion of cultured cells. Vet. Parasitol. 81: 99-105 Go to original source... Go to PubMed...
  21. Kaltner H., Stippi M., Knaus M., El-Matbouli M. 2007: Characterization of glycans in the development stages of Myxobolus cerebralis (Myxozoa), the causative agent of whirling disease. J. Fish Dis. 30: 637-647 Go to original source... Go to PubMed...
  22. Kim J.H., Ogawa K., Wakabayashi H. 1999: Lectin-reactive components of the microsporidian Glugea plecoglossi and their relation to spore phagocytosis by head kidney macrophages of ayu Plecoglossus altivelis. Dis. Aquat. Org. 39: 59-63 Go to original source... Go to PubMed...
  23. Klabunde J., Berger J., Jensenius J.C., Klinkert M.Q., Zelck U.E., Kremsner P.G., Kun J.F.J. 2000: Schistosoma mansoni: adhesion of mannan-binding lectin to surface glycoproteins of cercariae and adult worms. Exp. Parasitol. 95: 231-239 Go to original source... Go to PubMed...
  24. Knaus M., El-Matbouli M. 2005: Characterisation of carbohydrate-binding sites in developmental stages of Myxobolus cerebralis. Parasitol. Res. 97: 505-514 Go to original source... Go to PubMed...
  25. Lom J., Dykova I. 2006: Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 53: 1-36 Go to original source... Go to PubMed...
  26. Lukes J., Volf P., Lom J. 1993: Detection of chitin in spores of Myxobolus muelleri and M. subepithelialis (Myxosporea, Myxozoa). Parasitol. Res. 79: 439-440 Go to original source... Go to PubMed...
  27. Ma B., Simala-Grant J.L., Taylor D.E. 2006: Fucosylation in prokaryotes and eukaryotes. Glycobiology 16: 158R-184R Go to original source... Go to PubMed...
  28. Marin de M ateo M., Bovo G., Comuzzi M., Adams A. 1997: Lectin histochemical studies on Sphaerospora sp. (Myxosporea) from Italian brown trout, Salmo trutta L. J. Fish Dis. 20: 51-58 Go to original source...
  29. Marin de Mateo M., McGeorge J., Morris D., Kent M.L. 1996: Comparative studies of PKX and Sphaerospora spp. from salmonids using lectin and monoclonal antibody staining techniques. J. Fish Dis. 19: 55-63 Go to original source...
  30. Morris D.J., Adams A. 2004: Localization of carbohydrate terminals on Tetracapsuloides bryosalmonae using lectin histochemistry and immunogold electron microscopy. J. Fish Dis. 27: 37-45 Go to original source... Go to PubMed...
  31. Munoz P., Palenzuela O., Alvarez-Pellitero P., Sitja-Boba dilla A. 1999: Comparative studies on carbohydrates of several myxosporean parasites of fish using lectin histochemical methods. Folia Parasitol. 46: 241-247 Go to PubMed...
  32. Munoz P., Sitja-Bobadilla A., Alvarez-Pellitero P. 2000: Ultrastructural localisation of carbohydrates in several myxosporean parasites. Parasite 7: 185-191 Go to original source... Go to PubMed...
  33. Padros P., Palenzuela O., Hispano C., Tosas O., Zarza C., Crespo S., Alvarez-Pellitero P. 2001: Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Dis. Aquat. Org. 47: 57-62 Go to original source... Go to PubMed...
  34. Palenzuela O. 2006: Myxozoan infections in Mediterranean mariculture. Parassitologia 48: 27-29 Go to PubMed...
  35. Quiroga M.I., Redondo M.J., Sitja-Bobadilla A., Palenzuela O., Riaza A., Macias A., Vazquez S., Perez A., Nieto J.M., Alvarez-Pellitero P. 2006: Risk factors associated with Enteromyxum scophthalmi (Myxozoa) infection in cultured turbot, Scophthalmus maximus (L.). Parasitology 133: 433-442 Go to original source... Go to PubMed...
  36. Redondo M.J., Cortadellas N., Palenzuela O., Alvarez-Pellitero P. 2008: Detection of carbohydrate terminals in the enteric parasite Enteromyxum scophthalmi (Myxozoa) and possible interactions with its fish host Psetta maxima. Parasitol. Res. 102: 1257-1267 Go to original source... Go to PubMed...
  37. Rodriguez A., Esteban M.A., Meseguer J. 2003: A mannose-receptor is possibly involved in the phagocytosis of Saccharomyces cerevisiae by seabream (Sparus aurata L.) leucocytes. Fish Shellfish Immunol. 14: 375-388 Go to original source... Go to PubMed...
  38. Schabussova I., Schabuss M., Gelnar M., Horak P. 2003: Use of lectins in characterizing developmentally regulated changes on the surface of Paradiplozoon megan (Monogenea: Diplozoidae). Helminthologia 40: 135-140
  39. Sharon N. 2006: Carbohydrates as future anti-adhesion drugs for infectious diseases. Biochim. Biophys. Acta 1760: 527-537 Go to original source... Go to PubMed...
  40. Sitja-Bobadilla A., Diamant A., Palenzuela O., AlvarezP ellitero 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 Go to original source... Go to PubMed...
  41. Soeiro M.N.C., Paiva M.M., Barbossa H.S., Meirelles M.N.L., Araujo -Jorge T.C. 1999: A cardiomyocyte mannose receptor system is involved in Trypanosoma cruzi invasion and is downmodulated after infection. Cell Struct. Funct. 24: 139-149 Go to original source... Go to PubMed...
  42. Taupin V., Garenaux E., Mazet M., Maes E., Denise H., Prensier G., Vivares C.P., Guerardel Y., Metenier G. 2006: Major O-glycans in the spores of two microsporidian parasites are represented by unbranched manno-oligosaccharides containing α-1,2 linkages. Glycobiology 17: 56-67 Go to original source... Go to PubMed...
  43. Taylor D.W., Goddard J.M., McMahon J.E. 1986: Surface component on Onchocerca volvulus. Mol. Biochem. Parasitol. 18: 283-300 Go to original source... Go to PubMed...
  44. Wisnewski N., McNeil M., Grieve R.B., Wassom D.L. 1993: Characterization of a novel fucosyl- and tylevosyl-containing glycoconjugates from Trichinella spiralis muscle stage larvae. Mol. Biochem. Parasitol. 61: 25-36 Go to original source... Go to PubMed...
  45. Yaganida T., Nomura Y., Kimura T., Fukuda Y., Yokoyama H., Ogawa K. 2004: Molecular and morphological redescriptions of enteric myxozoans, Enteromyxum leei (formerly Myxidium sp. TP) and Enteromyxum fugu comb. n. (syn. Myxidium fugu) from cultured tiger puffer. Fish Pathol. 39: 137-143 Go to original source...
  46. Xu D.-H., Klesius P.H., Shoemaker C.A. 2001: Effect of lectins on the invasion of Ichthyophthirius theront to channel catfish tissue. Dis. Aquat. Org. 45: 115-120 Go to original source... Go to PubMed...