Immunomodulatory effects of dietary β-1,3-glucan from Euglena gracilis in rainbow trout (Oncorhynchus mykiss) immersion vaccinated against Yersinia ruckeri

Fish and Shellfish Immunology

Volumn 33, Issue 1, 2012, Pages 111-120

  Skov, Jakob ^a   Kania, Per Walter ^a   Holten Andersen, Lars ^a   Fouz, Belén ^b   Buchmann, Kurt ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Head kidney; Paramylon; Vaccination; Yersinia ruckeri; Glucan

Indexed keywords

ALGAE; EUGLENA GRACILIS; ONCORHYNCHUS MYKISS; YERSINIA RUCKERI;

EID: 84861482433     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2012.04.009     Document Type: Article

References (57)

1. Stone B.A. Chemistry of β-glucans. Chemistry, biochemistry and biology of (1-3)-β-glucans and related polysaccharides 2009, 5-46. Academic Press, Burlington. A. Bacic, G.B. Fincher, B.A. Stone (Eds.).
2. Novak M., Vetvicka V. Glucans as biological response modifiers. Endocr Metab Immune Disord Drug Targets 2009, 9:67-75.
3. Soltanian S., Stuyven E., Cox E., Sorgeloos P., Bossier P. Beta-glucans as immunostimulant in vertebrates and invertebrates. Crit Rev Microbiol 2009, 35:109-138.
4. Misra C.K., Das B.K., Mukherjee S.C., Pattnaik P. Effect of long term administration of dietary β-glucan on immunity, growth and survival of Labeo rohita fingerlings. Aquaculture 2006, 255:82-94.
5. Ai Q.H., Mai K.S., Zhang L., Tan B.P., Zhang W.B., Xu W., et al. Effects of dietary β-1,3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol 2007, 22:394-402.
6. Li P., Wen Q., Gatlin D.M. Dose-dependent influences of dietary β-1,3-glucan on innate immunity and disease resistance of hybrid striped bass Morone chrysops × Morone saxatilis. Aquac Res 2009, 40:1578-1584.
7. Sahoo P.K., Mukherjee S.C. The effect of dietary immunomodulation upon Edwardsiella tarda vaccination in healthy and immunocompromised Indian major carp (Labeo rohita). Fish Shellfish Immunol 2002, 12:1-16.
8. Dalmo R.A., Bøgwald J. β-Glucans as conductors of immune symphonies. Fish Shellfish Immunol 2008, 25:384-396.
9. Siwicki A.K., Kazun K., Glabski E., Terech-Majewska E., Baranowski P., Trapkowska S. The effect of beta-1.3/1.6-glucan in diets on the effectiveness of anti-Yersinia ruckeri vaccine - an experimental study in rainbow trout (Oncorhynchus mykiss). Pol J Food Nutr Sci 2004, 13:59-61.
10. Jaafar R.M., Skov J., Kania P.W., Buchmann K. Dose dependent effects of dietary immunostimulants on rainbow trout immune parameters and susceptibility to the parasite Ichthyophthirius multifiliis. J Aquac Res Dev 2011, S3:001.
11. 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 Aquacult 2002, 64:1-9.
12. Welker T.L., Lim C., Yildirim-Aksoy M., Shelby R., Klesius P.H. Immune response and resistance to stress and Edwardsiella ictaluri challenge in channel catfish, Ictalurus punctatus, fed diets containing commercial whole-cell yeast or yeast subcomponents. J World Aquacult Soc 2007, 38:24-35.
13. Whittington R., Lim C., Klesius P.H. Effect of dietary β-glucan levels on the growth response and efficacy of Streptococcus iniae vaccine in Nile tilapia, Oreochromis niloticus. Aquaculture 2005, 248:217-225.
14. Bohn J.A., BeMiller J.N. (1→3)-β-d-Glucans as biological response modifiers: a review of structure-functional activity relationships. Carbohyd Polym 1995, 28:3-14.
15. Sletmoen M., Stokke B.T. Higher order structure of (1,3)-β-d-glucans and its influence on their biological activities and complexation abilities. Biopolymers 2008, 89:310-321.
16. Wismar R., Brix S., Frøkiær H., Lærke H.N. Dietary fibers as immunoregulatory compounds in health and disease. Ann N Y Acad Sci 2010, 1190:70-85.
17. Chen J., Seviour R. Medicinal importance of fungal β-(1→3), (1→6)-glucans. Mycol Res 2007, 111:635-652.
18. Brown G.D., Gordon S. Immune recognition of fungal β-glucans. Cell Microbiol 2005, 7:471-479.
19. Barsanti L., Vismara R., Passarelli V., Gualtieri P. Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions. J Appl Phycol 2001, 13:59-65.
20. Vismara R., Vestri S., Frassanito A.M., Barsanti L., Gualtieri P. Stress resistance induced by paramylon treatment in Artemia sp. J Appl Phycol 2004, 16:61-67.
21. Sugiyama A., Hata S., Suzuki K., Yoshida E., Nakano R., Mitra S., et al. Oral administration of paramylon, a β-1,3-d-glucan isolated from Euglena gracilis Z inhibits development of atopic dermatitis-like skin lesions in NC/Nga mice. J Vet Med Sci 2010, 72:755-763.
22. Sugiyama A., Suzuki K., Mitra S., Arashida R., Yoshida E., Nakano R., et al. Hepatoprotective effects of paramylon, a β-1,3-d-glucan isolated from Euglena gracilis Z, on acute liver injury induced by carbon tetrachloride in rats. J Vet Med Sci 2009, 71:885-890.
23. Kudrenko B., Snape N., Barnes A.C. Linear and branched β(1-3)-d-glucans activate but do not prime teleost macrophages in vitro and are inactivated by dilute acid: implications for dietary immunostimulation. Fish Shellfish Immunol 2009, 26:443-450.
24. Hong F., Yan J., Baran J.T., Allendorf D.J., Hansen R.D., Ostroff G.R., et al. Mechanism by which orally administered β-1,3-glucans enhance the tumoricidal activity of antitumor monoclonal antibodies in murine tumor models. J Immunol 2004, 173:797-806.
25. Dalmo R.A., Bogwald J., Ingebrigtsen K., Seljelid R. The immunomodulatory effect of laminaran [β(1,3)-d-glucan] on Atlantic salmon, Salmo salar L, anterior kidney leucocytes after intraperitoneal, peroral and peranal administration. J Fish Dis 1996, 19:449-457.
26. Press C.M., Evensen Ø. The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 1999, 9:309-318.
27. Meseguer J., Lopez-Ruiz A., Garcia-Ayala A. Reticulo-endothelial stroma of the head-kidney from the seawater teleost gilthead seabream (Sparus aurata L.): an ultrastructural and cytochemical study. Anat Rec 1995, 241:303-309.
28. Ortuno J., Cuesta A., Esteban M.A., Meseguer J. Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Sparus aurata L.) innate immune system. Vet Immunol Immunopathol 2001, 79:167-180.
29. Fouz B., Zarza C., Amaro C. First description of non-motile Yersinia ruckeri serovar I strains causing disease in rainbow trout, Oncorhynchus mykiss (Walbaum), cultured in Spain. J Fish Dis 2006, 29:339-346.
30. Parry R.M., Chandan R.C., Shahani K.M. A rapid sensitive assay of muramidase. Proc Soc Exp Biol Med 1965, 119:384-386.
31. Ellis A.E. Lysozyme assays. Techniques in fish immunology 1990, 101-103. SOS Publications, Fair Haven. J.S. Stolen, T.C. Fletcher, D.P. Anderson, B.S. Roberson, W.B. van Muiswinkel (Eds.).
32. Raida M.K., Buchmann K. Development of adaptive immunity in rainbow trout, Oncorhynchus mykiss (Walbaum) surviving an infection with Yersinia ruckeri. Fish Shellfish Immunol 2008, 25:533-541.
33. Gibello A., Blanco M.M., Moreno M.A., Cutuli M.T., Domenech A., Dominguez L., et al. Development of a PCR assay for detection of Yersinia ruckeri in tissues of inoculated and naturally infected trout. Appl Environ Microbiol 1999, 65:346-350.
34. Amend D.F. Potency testing of fish vaccines. Dev Biol Stand 1981, 49:447-454.
35. -ΔΔCT method. Methods 2001, 25:402-408.
36. Raida M.K., Buchmann K. Bath vaccination of rainbow trout (Oncorhynchus mykiss Walbaum) against Yersinia ruckeri: effects of temperature on protection and gene expression. Vaccine 2008, 26:1050-1062.
37. Johnson K.A., Amend D.F. Comparison of efficacy of several delivery methods using Yersinia ruckeri bacterin on rainbow trout, Salmo gairdneri Richardson. J Fish Dis 1983, 6:331-336.
38. Johnson K.A., Flynn J.K., Amend D.F. Duration of immunity in salmonids vaccinated by direct immersion with Yersinia ruckeri and Vibrio anguillarum bacterins. J Fish Dis 1982, 5:207-213.
39. Ashida T., Okimasu E., Ui M., Heguri M., Oyama Y., Amemura A. Protection of Japanese flounder Paralichthys olivaceus against experimental edwardsiellosis by formalin-killed Edwardsiella tarda in combination with oral administration of immunostimulants. Fisheries Sci 1999, 65:527-530.
40. deBaulny M.O., Quentel C., Fournier V., Lamour F., LeGouvello R. Effect of long-term oral administration of β-glucan as an immunostimulant or an adjuvant on some non-specific parameters of the immune response of turbot Scophthalmus maximus. Dis Aquat Organ 1996, 26:139-147.
41. Scapigliati G., Meloni S., Buonocore F., Bossu P., Prugnoli D., Secombes C.J. Immunopurification of B lymphocytes from sea bass Dicentrarchus labrax (L.). Mar Biotechnol 2003, 5:214-221.
42. Janeway's immunobiology 2008, Garland Science, Taylor & Francis Group, New York. 7th ed. K. Murphy, P. Travers, M. Walport (Eds.).
43. Zhang Y.A., Salinas I., Li J., Parra D., Bjork S., Xu Z., et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 2010, 11:827-835.
44. Cossarini-Dunier M. Protection against enteric redmouth disease in rainbow trout, Salmo gairdneri Richardson, after vaccination with Yersinia ruckeri bacterin. J Fish Dis 1986, 9:27-33.
45. Cipriano R.C., Ruppenthal T. Immunization of salmonids against Yersinia ruckeri: significance of humoral immunity and cross protection between serotypes. J Wildl Dis 1987, 23:545-550.
46. Boschi I., Randelli E., Buonocore F., Casani D., Bernini C., Fausto A.M., et al. Transcription of T cell-related genes in teleost fish, and the European sea bass (Dicentrarchus labrax) as a model. Fish Shellfish Immunol 2011, 31:655-662.
47. Harun N.O., Wang T.H., Secombes C.J. Gene expression profiling in naive and vaccinated rainbow trout after Yersinia ruckeri infection: insights into the mechanisms of protection seen in vaccinated fish. Vaccine 2011, 29:4388-4399.
48. Paulsen S.M., Engstad R.E., Robertsen B. Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast β-glucan and bacterial lipopolysaccharide. Fish Shellfish Immunol 2001, 11:23-37.
49. Grinde B. Lysozyme from rainbow trout, Salmo gairdneri Richardson, as an antibacterial agent against fish pathogens. J Fish Dis 1989, 12:95-104.
50. Marsh M.B., Rice C.D. Development, characterization, and technical applications of a fish lysozyme-specific monoclonal antibody (mAb M24-2). Comp Immunol Microbiol Infect Dis 2010, 33:e15-e23.
51. Liu F., Wen Z.L. Cloning and expression pattern of the lysozyme C gene in zebrafish. Mech Dev 2002, 113:69-72.
52. Faust N., Varas F., Kelly L.M., Heck S., Graf T. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 2000, 96:719-726.
53. Keshav S., Chung P., Milon G., Gordon S. Lysozyme is an inducible marker of macrophage activation in murine tissues as demonstrated by in situ hybridization. J Exp Med 1991, 174:1049-1058.
54. Lie O., Evensen O., Sørensen A., Frøysadal E. Study on isozyme activity in some fish species. Dis Aquat Organ 1989, 6:1-5.
55. Bayne C.J., Gerwick L. The acute phase response and innate immunity of fish. Dev Comp Immunol 2001, 25:725-743.
56. Raida M.K., Buchmann K. Innate immune response in rainbow trout (Oncorhynchus mykiss) against primary and secondary infections with Yersinia ruckeri O1. Dev Comp Immunol 2009, 33:35-45.
57. Gonzalez S.F., Buchmann K., Nielsen M.E. Ichthyophthirius multifiliis infection induces massive up-regulation of serum amyloid A in carp (Cyprinus carpio). Vet Immunol Immunopathol 2007, 115:172-178.