Effect of immunization route on mucosal and systemic immune response in Atlantic salmon (Salmo salar)

Veterinary Immunology and Immunopathology

Volumn 151, Issue 1-2, 2013, Pages 113-123

  Valdenegro Vega, Victoria A ^a   Crosbie, Philip ^a   Vincent, Benita ^a   Cain, Kenneth D ^a,b   Nowak, Barbara F ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

Atlantic salmon; Hapten antigens; Immunization; Mucosal immunity

Indexed keywords

2,4 DINITROPHENOL; ANTIBODY; ANTIGEN; FLUORESCEIN ISOTHIOCYANATE; FLUOROTAG; KEYHOLE LIMPET HEMOCYANIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; ATLANTIC SALMON; CONTROLLED STUDY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPLANT; IMMUNITY; IMMUNIZATION; MUCOSAL IMMUNITY; NONHUMAN; SERUM; SKIN EXPLANT; SUPERNATANT; SYSTEMIC IMMUNITY; WESTERN BLOTTING;

ANIMALS; ANTIBODY FORMATION; BLOTTING, WESTERN; DINITROPHENOLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCEIN-5-ISOTHIOCYANATE; HAPTENS; HEMOCYANIN; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNIZATION, SECONDARY; INJECTIONS, INTRAPERITONEAL; SALMO SALAR;

SALMO SALAR;

EID: 84871708993     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2012.10.010     Document Type: Article

References (47)

1. Adams M.B., Nowak B.F. Amoebic gill disease: sequential pathology in cultured Atlantic salmon, Salmo salar L. J. Fish Dis. 2003, 26:601-614.
2. Aoki K., Sato K., Nagaoka S., Kamada M., Hiramatsu K. Heat denaturation of bovine serum albumin in alkaline pH region. Biochim. Biophys. Acta (BBA) 1973, 328:323-333.
3. Bandin I., Dopazo C.P., van Muiswinkel W.B., Wiegertjes G.F. Quantitation of antibody secreting cells in high and low antibody responder inbred carp (Cyprinus carpio L.) strains. Fish Shellfish Immunol. 1997, 7:487-501.
4. Bean E.S. Polyclonal antibodies. Basic Methods in Antibody Production and Characterization 2001, 272. CRC Press LLC, Boca Raton, USA. G.C. Howard, D.R. Bethell (Eds.).
5. Bernard D., Six A., Rigottier-Gois L., Messiaen S., Chilmonczyk S., Quillet E., Boudinot P., Benmansour A. Phenotypic and functional similarity of gut intraepithelial and systemic T cells in a teleost fish. J. Immunol. 2006, 176:3942-3949.
6. Bøgwald J., Stensvåg K., Stuge T.B., Jørgensen T.Ø. Tissue localisation and immune responses in Atlantic salmon, Salmo salar L., after oral administration of Aeromonas salmonicida, Vibrio anguillarum and Vibrio salmonicida antigens. Fish Shellfish Immunol. 1994, 4:353-368.
7. Cain K.D., Jones D.R., Raison R.L. Characterisation of mucosal and systemic immune responses in rainbow trout (Oncorhynchus mykiss) using surface plasmon resonance. Fish Shellfish Immunol. 2000, 10:651-666.
8. Cain K.D., Jones D.R., Raison R.L. Antibody-antigen kinetics following immunization of rainbow trout (Oncorhynchus mykiss) with a T-cell dependent antigen. Dev. Comp. Immunol. 2002, 26:181-190.
9. Delamare-Deboutteville J., Wood D., Barnes A.C. Response and function of cutaneous mucosal and serum antibodies in barramundi (Lates calcarifer) acclimated in seawater and freshwater. Fish Shellfish Immunol. 2006, 21:92-101.
10. dos Santos N.M.S., Taverne-Thiele J.J., Barnes A.C., Ellis A.E., Rombout H.W.M. Kinetics of juvenile sea bass (Dicentrarchus labrax, L.) systemic and mucosal antibody secreting cell response to different antigens (Photobacterium damselae spp. piscicida Vibrio anguillarum and DNP). Fish Shellfish Immunol. 2001, 11:317-331.
11. dos Santos N.M.S., Taverne-Thiele J.J., Barnes A.C., van Muiswinkel W.B., Ellis A.E., Rombout J.H.W.M. The gill is a major organ for antibody secreting cell production following direct immersion of sea bass (Dicentrarchus labrax L.) in a Photobacterium damselae ssp. piscicida bacterin: an ontogenetic study. Fish Shellfish Immunol. 2001, 11:65-74.
12. Drennan J.D., LaPatra S.E., Swan C.M., Ireland S., Cain K.D. Characterization of serum and mucosal antibody responses in white sturgeon (Acipenser transmontanus Richardson) following immunization with WSIV and a protein hapten antigen. Fish Shellfish Immunol. 2007, 23:657-669.
13. Dussault C., Rodriguez M.A. Field trials of marking stream salmonids by dye injection and coded-wire-tagging. N. Am. J. Fish. Manage. 1997, 17:451-456.
14. Esteve-Gassent M.D., Fouz B., Amaro C. Efficacy of a bivalent vaccine against eel diseases caused by Vibrio vulnificus after its administration by four different routes. Fish Shellfish Immunol. 2004, 16:93-105.
15. Fast M.D., Sims D.E., Burka J.F., Mustafa A., Ross N.W. Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2002, 132:645-657.
16. Findlay C., Tatner M. The effect of reconstitution with cryopreserved thymocytes on the in vivo antibody response to sheep red blood cells, Aeromonas salmonicida, and DNP-KLH, in adult long term thymectomised rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 1996, 6:371-381.
17. Grabowski L.D., LaPatra S.E., Cain K.D. Systemic and mucosal antibody response in tilapia, Oreochromis niloticus (L.), following immunization with Flavobacterium columnare. J. Fish Dis. 2004, 27:573-581.
18. Hamuro K., Suetake H., Saha N.R., Kikuchi K., Suzuki Y. A Teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin. J. Immunol. 2007, 178:5682-5689.
19. Hatten F., Fredriksen å., Hordvik I., Endresen C. Presence of IgM in cutaneous mucus, but not in gut mucus of Atlantic salmon, Salmo salar. Serum IgM is rapidly degraded when added to gut mucus. Fish Shellfish Immunol. 2001, 11:257-268.
20. Hedfors I.A., Bakke H., Skjødt K., Grimholt U. Antibodies recognizing both IgM isotypes in Atlantic salmon. Fish Shellfish Immunol. 2012, 33:1199-1206.
21. Jones D.R., Hannan C.M., Russell-Jones G.J., Raison R.L. Selective B cell non-responsiveness in the gut of the rainbow trout (Oncorhynchus mykiss). Aquaculture 1999, 172:29-39.
22. Joosten P.H.M., Kruijer W.J., Rombout J.H.W.M. Anal immunisation of carp and rainbow trout with different fractions of a Vibrio anguillarum bacterin. Fish Shellfish Immunol. 1996, 6:541-551.
23. Joosten P.H.M., Tiemersma E., Threels A., Caumartin-Dhieux C., Rombout J.H.W.M. Oral vaccination of fish against Vibrio anguillarum using alginate microparticles. Fish Shellfish Immunol. 1997, 7:471-485.
24. LaFrentz B., LaPatra S.E., Jones G., Congleton J., Sun B., Cain K. Characterization of serum and mucosal antibody responses and relative per cent survival in rainbow trout, Oncorhynchus mykiss (Walbaum), following immunization and challenge with Flavobacterium psychrophilum. J. Fish Dis. 2002, 25:703-713.
25. Lin S.H., Davidson G., Secombes C., Ellis A. Use of a lipid-emulsion carrier for immunisation of dab (Limanda limanda) by bath and oral routes: an assessment of systemic and mucosal antibody responses. Aquaculture 2000, 181:11-24.
26. Lobb C. Secretory immunity induced in catfish, Ictalurus punctatus, following bath immunization. Dev. Comp. Immunol. 1987, 11:727-738.
27. Lobb C.J., Clem L.W. The metabolic relationships of the immunoglobulins in fish serum, cutaneous mucus, and bile. J. Immunol. 1981, 127:1525-1529.
28. Lumsden J., Ostland V., Byrne P., Ferguson H. Detection of a distinct gill-surface antibody response following horizontal infection and bath challenge of brook trout Salvelinus fontinalis with Flavobacterium branchiophilum, the causative agent of bacterial gill disease. Dis. Aquat. Org. 1993, 16:21-27.
29. Lumsden J.S., Ostland V.E., MacPhee D.D., Ferguson H.W. Production of gill-associated and serum antibody by rainbow trout (Oncorhynchus mykiss) following immersion immunization with acetone-killed Flavobacterium branchiophilum and the relationship to protection from experimental challenge. Fish Shellfish Immunol. 1995, 5:151-165.
30. Miura K., Orcutt A.C., Muratova O.V., Miller L.H., Saul A., Long C.A. Development and characterization of a standardized ELISA including a reference serum on each plate to detect antibodies induced by experimental malaria vaccines. Vaccine 2008, 26:193-200.
31. O'Donnell G.B., Smith P.R., Kilmartin J.J., Moran A.P. Uptake and fate of orally administered bacterial lipopolysaccharide in brown trout (Salmo trutta). Fish Shellfish Immunol. 1994, 4:285-299.
32. Plikaytis B.D.B., Turner S.H.S., Gheesling L.L.L., Carlone G.M.G. Comparisons of standard curve-fitting methods to quantitate Neisseria meningitidis group A polysaccharide antibody levels by enzyme-linked immunosorbent assay. J. Clin. Microbiol. 1991, 29:1439-1446.
33. Quinn G.P., Keough M.J. Experimental Design and Data Analysis for Biologists 2002, Cambridge University Press, Cambridge, p. 537.
34. Rombout J.W.H.M., Blok L.J., Lamers C.H.J., Egberts E. Immunization of carp (Cyprinus carpio) with a Vibrio anguillarum bacterin: indications for a common mucosal immune system. Dev. Comp. Immunol. 1986, 10:341-351.
35. Salinas I., Zhang Y.-A., Sunyer J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 2011, 35:1346-1365.
36. Shoemaker C.A., Xu D.-H., Shelby R.A., Klesius P.H. Detection of cutaneous antibodies against Flavobacterium columnare in channel catfish, Ictalurus punctatus (Rafinesque). Aquacult. Res. 2005, 36:813-818.
37. Swan C.M., Lindstrom N.M., Cain K.D. Identification of a localized mucosal immune response in rainbow trout, Oncorhynchus mykiss (Walbaum), following immunization with a protein-hapten antigen. J. Fish Dis. 2008, 31:383-393.
38. van Muiswinkel, W.B., Wiegertjes, G.F., 2997. Immune responses after injection vaccination of fish. In: Gudding, R., Lillehaug, A., Midtlyng, P.J., Brown, F. (Eds.), Fish Vaccinology. Dev. Biol. Stand. Karger, Basel, pp. 55-57.
39. Vervarcke S., Ollevier F., Kinget R., Michoel A. Mucosal response in African catfish after administration of Vibrio anguillarum O2 antigens via different routes. Fish Shellfish Immunol. 2005, 18:125-133.
40. Vinitantharat S., Gravningen K., Greger E. Fish vaccines. Adv. Vet. Med. 1999, 41:539-550.
41. Xu D.-H., Klesius P.H., Shoemaker C.A. Effect of immunization of channel catfish with inactivated trophonts on serum and cutaneous antibody titers and survival against Ichthyophthirius multifiliis. Fish Shellfish Immunol. 2009, 26:614-618.
42. Xu D.H., Klesius P.H. Protective effect of cutaneous antibody produced by channel catfish, Ictalurus punctatus (Rafinesque), immune to Ichthyophthirius multifiliis Fouquet on cohabited non-immune catfish. J. Fish Dis. 2003, 26:287-291.
43. Xu D.H., Klesius P.H., Shelby R.A. Cutaneous antibodies in excised skin from channel catfish, Ictalurus punctatus Rafinesque, immune to Ichthyophthirius multifiliis. J. Fish Dis. 2002, 25:45-52.
44. Xu Z., Chen C.F., Mao Z.J., Zhu W.Y. Detection of serum and mucosal antibody production and antibody secreting cells (ASCs) in large yellow croaker (Pseudosciaena crocea) following vaccination with Vibrio harveyi via different routes. Aquaculture 2009, 287:243-247.
45. Young N.D., Crosbie P.B.B., Adams M.B., Nowak B.F., Morrison R.N. Neoparamoeba perurans n. sp., an agent of amoebic gill disease of Atlantic salmon (Salmo salar). Int. J. Parasitol. 2007, 37:1469-1481.
46. Zhang Y.-A., Salinas I., Li J., Parra D., Bjork S., Xu Z., LaPatra S.E., Bartholomew J., Sunyer J.O. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 2010, 11:827-835.
47. Zilberg D., Klesius P.H. Quantification of immunoglobulin in the serum and mucus of channel catfish at different ages and following infection with Edwardsiella ictaluri. Vet. Immunol. Immunopathol. 1997, 58:171-180.