Salmonid alphavirus-based replicon vaccine against infectious salmon anemia (ISA): Impact of immunization route and interactions of the replicon vector

Fish and Shellfish Immunology

Volumn 36, Issue 2, 2014, Pages 383-392

  Wolf, Astrid ^a   Hodneland, Kjartan ^b   Frost, Petter ^b   Hoeijmakers, Mathieu ^c   Rimstad, Espen ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b MERCK ANIMAL HEALTH   (United States)

^c INTERVET INTERNATIONAL BV   (Netherlands)

Author keywords

Immunization against infectious salmon anemia; Immunization route of DNA vaccines in fish; Replicon induced immune responses in Atlantic salmon; Salmonid alphavirus based replicon vaccine

Indexed keywords

HEMAGGLUTININ ESTERASE; VIRUS FUSION PROTEIN; VIRUS HEMAGGLUTININ; VIRUS VACCINE;

ALPHA VIRUS; ANIMAL; ANIMAL DISEASE; ARTICLE; ATLANTIC SALMON; FISH DISEASE; GENETICS; IMMUNIZATION AGAINST INFECTIOUS SALMON ANEMIA; IMMUNIZATION ROUTE OF DNA VACCINES IN FISH; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; ORTHOMYXOVIRUS; ORTHOMYXOVIRUS INFECTION; REPLICON; REPLICON-INDUCED IMMUNE RESPONSES IN ATLANTIC SALMON; SALMONID ALPHAVIRUS-BASED REPLICON VACCINE; VIROLOGY;

IMMUNIZATION AGAINST INFECTIOUS SALMON ANEMIA; IMMUNIZATION ROUTE OF DNA VACCINES IN FISH; REPLICON-INDUCED IMMUNE RESPONSES IN ATLANTIC SALMON; SALMONID ALPHAVIRUS-BASED REPLICON VACCINE;

ALPHAVIRUS; ANIMALS; FISH DISEASES; HEMAGGLUTININS, VIRAL; INJECTIONS, INTRAMUSCULAR; INJECTIONS, INTRAPERITONEAL; ISAVIRUS; ORTHOMYXOVIRIDAE INFECTIONS; REPLICON; SALMO SALAR; VIRAL FUSION PROTEINS; VIRAL VACCINES;

EID: 84893184280     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.12.018     Document Type: Article

References (64)

1. Biering E., Villoing S., Sommerset I., Christie K.E. Update on viral vaccines for fish. Dev Biol (Basel) 2005, 121:97-113.
2. Gomez-Casado E., Estepa A., Coll J.M. Acomparative review on European-farmed finfish RNA viruses and their vaccines. Vaccine 2011 Mar 24, 29(15):2657-2671.
3. Sommerset I., Krossøy B., Biering E., Frost P. Vaccines for fish in aquaculture. Expert Rev Vaccines 2005 Feb, 4(1):89-101.
4. Asche F.H., Tveteras R., Tveteras S. The salmon disease crisis in Chile. Marine Res Econ 2010, 24:405-411.
5. Kibenge F.S.B., Kibenge M.J.T., Joseph T., McDougall J. The development of infectious salmon anemia virus vaccines in Canada. International response to infectious salmon anemia: prevention, control, and eradication: proceedings of a symposium; 3-4 September 2002 2002, 39-50. Tech. Bull. 1902. edn. O. Miller, R.C. Cipriano (Eds.).
6. Mardones F.O., Perez A.M., Valdes-Donoso P., Carpenter T.E. Farm-level reproduction number during an epidemic of infectious salmon anemia virus in southern Chile in 2007-2009. Prev Vet Med 2011 Dec 1, 102(3):175-184.
7. Olsen A.B., Hellberg H. Helsesituasjon hos laksefisk. Fiskehelserapporten 2011 2012, 3-32. Veterinærinstituttet edn.
8. Wolf A., Hodneland K., Frost P., Braaen S., Rimstad E. Ahemagglutinin-esterase-expressing salmonid alphavirus replicon protects Atlantic salmon (Salmo salar) against infectious salmon anemia (ISA). Vaccine 2013 Jan 11, 31(4):661-669.
9. Hariharan M.J., Driver D.A., Townsend K., Brumm D., Polo J.M., Belli B.A., et al. DNA immunization against herpes simplex virus: enhanced efficacy using a Sindbis virus-based vector. JVirol 1998 Feb, 72(2):950-958.
10. Ljungberg K., Whitmore A.C., Fluet M.E., Moran T.P., Shabman R.S., Collier M.L., et al. Increased immunogenicity of a DNA-launched Venezuelan equine encephalitis virus-based replicon DNA vaccine. JVirol 2007 Dec, 81(24):13412-13423.
11. Nordstroem E.K., Forsell M.N., Barnfield C., Bonin E., Hanke T., Sundstrom M., et al. Enhanced immunogenicity using an alphavirus replicon DNA vaccine against human immunodeficiency virus type 1. JGen Virol 2005 Feb, 86(Pt 2):349-354.
12. Leitner W.W., Ying H., Restifo N.P. DNA and RNA-based vaccines: principles, progress and prospects. Vaccine 1999 Dec 10, 18(9-10):765-777.
13. Näslund T.I., Kostic L., Nordstrom E.K., Chen M., Liljeström P. Role of innate signalling pathways in the immunogenicity of alphaviral replicon-based vaccines. Virol J 2011, 8:36.
14. Avogadri F., Merghoub T., Maughan M.F., Hirschhorn-Cymerman D., Morris J., Ritter E., et al. Alphavirus replicon particles expressing TRP-2 provide potent therapeutic effect on melanoma through activation of humoral and cellular immunity. PLoS One 2010, 5(9).
15. Berglund P., Fleeton M.N., Smerdou C., Liljeström P. Immunization with recombinant Semliki Forest virus induces protection against influenza challenge in mice. Vaccine 1999 Feb 5, 17(5):497-507.
16. Colmenero P., Liljestrom P., Jondal M. Induction of P815 tumor immunity by recombinant Semliki Forest virus expressing the P1A gene. Gene Ther 1999 Oct, 6(10):1728-1733.
17. Hubby B., Talarico T., Maughan M., Reap E.A., Berglund P., Kamrud K.I., et al. Development and preclinical evaluation of an alphavirus replicon vaccine for influenza. Vaccine 2007 Nov 23, 25(48):8180-8189.
18. Reddy J.R., Kwang J., Varthakavi V., Lechtenberg K.F., Minocha H.C. Semiliki forest virus vector carrying the bovine viral diarrhea virus NS3 (p80) cDNA induced immune responses in mice and expressed BVDV protein in mammalian cells. Comp Immunol Microbiol Infect Dis 1999 Oct, 22(4):231-246.
19. Boudinot P., Blanco M., de K.P., Benmansour A. Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology 1998 Sep 30, 249(2):297-306.
20. Garver K.A., Conway C.M., Elliott D.G., Kurath G. Analysis of DNA-vaccinated fish reveals viral antigen in muscle, kidney and thymus, and transient histopathologic changes. Mar Biotechnol 2005, 7:540-553.
21. Heppell J., Lorenzen N., Armstrong N.K., Wu T., Lorenzen E., Einer-Jensen K., et al. Development of DNA vaccines for fish: vector design, intramuscular injection and antigen expression using viral haemorrhagic septicaemia virus genes as model. Fish Shellfish Immunol 1998, 8:271-286.
22. Seternes T., Tonheim T.C., Lovoll M., Bogwald J., Dalmo R.A. Specific endocytosis and degradation of naked DNA in the endocardial cells of cod (Gadus morhua L.). JExp Biol 2007 Jun, 210(Pt 12):2091-2103.
23. Tonheim T.C., Dalmo R.A., Bogwald J., Seternes T. Specific uptake of plasmid DNA without reporter gene expression in Atlantic salmon (Salmo salar L.) kidney after intramuscular administration. Fish Shellfish Immunol 2008 Jan, 24(1):90-101.
24. Fynan E.F., Webster R.G., Fuller D.H., Haynes J.R., Santoro J.C., Robinson H.L. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc Natl Acad Sci U S A 1993 Dec 15, 90(24):11478-11482.
25. de las Heras A.I., Rodriguez Saint-Jean S., Perez-Prieto S.I. Immunogenic and protective effects of an oral DNA vaccine against infectious pancreatic necrosis virus in fish. Fish Shellfish Immunol 2010 Apr, 28(4):562-570.
26. Corbeil S., Kurath G., LaPatra S.E. Fish DNA vaccine against infectious hematopoietic necrosis virus: efficacy of various routes of immunization. Fish Shellfish Immunol 2000, 10:711-723.
27. McLauchlan P.E., Collet B., Ingerslev E., Secombes C.J., Lorenzen N., Ellis A.E. DNA vaccination against viral haemorrhagic septicaemia (VHS) in rainbow trout: size, dose, route of injection and duration of protection-early protection correlates with Mx expression. Fish Shellfish Immunol 2003 Jul, 15(1):39-50.
28. Carroll T.D., Matzinger S.R., Barro M., Fritts L., McChesney M.B., Miller C.J., et al. Alphavirus replicon-based adjuvants enhance the immunogenicity and effectiveness of Fluzone (R) in rhesus macaques. Vaccine 2011 Jan 29, 29(5):931-940.
29. Leitner W.W., Ying H., Driver D.A., Dubensky T.W., Restifo N.P. Enhancement of tumor-specific immune response with plasmid DNA replicon vectors. Cancer Res 2000 Jan 1, 60(1):51-55.
30. Leitner W.W., Hwang L.N., deVeer M.J., Zhou A., Silverman R.H., Williams B.R., et al. Alphavirus-based DNA vaccine breaks immunological tolerance by activating innate antiviral pathways. Nat Med 2003 Jan, 9(1):33-39.
31. Leitner W.W., Bergmann-Leitner E.S., Hwang L.N., Restifo N.P. Type I interferons are essential for the efficacy of replicase-based DNA vaccines. Vaccine 2006 Jun 12, 24(24):5110-5118.
32. Smith, Hubby B., Copp L. Alphavirus replicon particles matched to protein antigens as immunological adjuvants 2011, AlphaVax, assignee, 20110086062.
33. Jimenez N., Coll J., Salguero F.J., Tafalla C. Co-injection of interleukin 8 with the glycoprotein gene from viral haemorrhagic septicemia virus (VHSV) modulates the cytokine response in rainbow trout (Oncorhynchus mykiss). Vaccine 2006 Jul 7, 24(27-28):5615-5626.
34. Sanchez E., Coll J., Tafalla C. Expression of inducible CC chemokines in rainbow trout (Oncorhynchus mykiss) in response to a viral haemorrhagic septicemia virus (VHSV) DNA vaccine and interleukin 8. Dev Comp Immunol 2007, 31(9):916-926.
35. Strandskog G., Skjaeveland I., Ellingsen T., Jørgensen J.B. Double-stranded RNA- and CpG DNA-induced immune responses in Atlantic salmon: comparison and synergies. Vaccine 2008 Aug 26, 26(36):4704-4715.
36. Strandskog G., Villoing S., Iliev D.B., Thim H.L., Christie K.E., Jørgensen J.B. Formulations combining CpG containing oliogonucleotides and poly I: C enhance the magnitude of immune responses and protection against pancreas disease in Atlantic salmon. Dev Comp Immunol 2011 Nov, 35(11):1116-1127.
37. Lorenzen N., Lorenzen E., Einer-Jensen K., LaPatra S.E. DNA vaccines as a tool for analysing the protective immune response against rhabdoviruses in rainbow trout. Fish Shellfish Immunol 2002 May, 12(5):439-453.
38. LaPatra S.E., Corbeil S., Jones G.R., Shewmaker W.D., Lorenzen N., Anderson E.D., et al. Protection of rainbow trout against infectious hematopoietic necrosis virus four days after specific or semi-specific DNA vaccination. Vaccine 2001 Jul 16, 19(28-29):4011-4019.
39. Lorenzen N., Lorenzen E., Einer-Jensen K., LaPatra S.E. Immunity induced shortly after DNA vaccination of rainbow trout against rhabdoviruses protects against heterologous virus but not against bacterial pathogens. Dev Comp Immunol 2002 Mar, 26(2):173-179.
40. Sommerset I., Lorenzen E., Lorenzen N., Bleie H., Nerland A.H. ADNA vaccine directed against a rainbow trout rhabdovirus induces early protection against a nodavirus challenge in turbot. Vaccine 2003 Dec 1, 21(32):4661-4667.
41. Karlsen M., Villoing S., Rimstad E., Nylund A. Characterization of untranslated regions of the salmonid alphavirus 3 (SAV3) genome and construction of a SAV3 based replicon. Virol J 2009, 6:173.
42. Øye A.K., Rimstad E. Inactivation of infectious salmon anaemia virus, viral haemorrhagic septicaemia virus and infectious pancreatic necrosis virus in water using UVC irradiation. Dis Aquat Organ 2001 Dec;20, 48(1):1-5.
43. Lauscher A., Krossøy B., Frost P., Grove S., Koenig M., Bohlin J., et al. Immune responses in Atlantic salmon (Salmo salar) following protective vaccination against infectious salmon anemia (ISA) and subsequent ISA virus infection. Vaccine 2011 Aug 26, 29(37):6392-6401.
44. Mourton C., Bearzotti M., Piechaczyk M., Paolucci F., Pau B., Bastide J.M., et al. Antigen-capture ELISA for viral haemorrhagic septicaemia virus serotype I. JVirol Methods 1990 Sep, 29(3):325-333.
45. Løvoll M., Austbø L., Jørgensen J.B., Rimstad E., Frost P. Transcription of reference genes used for quantitative RT-PCR in Atlantic salmon is affected by viral infection. Vet Res 2011 Jan, 42(1):8.
46. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001 Dec, 25(4):402-408.
47. Agresti A. Categorical data analysis 2002, John Wiley & Sons Inc, Hoboken, New Yersey, USA.
48. Usage note 23003: modeling a binary response and estimating a relative risk (prevalence ratio) 2012, http://support%20sas%20com/kb/23/003%20html.
49. Jones S.R.M., MacKinnon A.M., Salonius K. Vaccination of fresh-water-reared Atlantic salmon reduces mortality associated with infectious salmon anaemia virus. Bull Eur Assoc Fish Pathol 1999, 19(3):98-101.
50. Corr M., Lee D.J., Carson D.A., Tighe H. Gene vaccination with naked plasmid DNA: mechanism of CTL priming. JExp Med 1996 Oct 1, 184(4):1555-1560.
51. Fu T.M., Ulmer J.B., Caulfield M.J., Deck R.R., Friedman A., Wang S., et al. Priming of cytotoxic T lymphocytes by DNA vaccines: requirement for professional antigen presenting cells and evidence for antigen transfer from myocytes. Mol Med 1997 Jun, 3(6):362-371.
52. Vallejo A.N., Miller N.W., Harvey N.E., Cuchens M.A., Warr G.W., Clem L.W. Cellular pathway(s) of antigen processing and presentation in fish APC: endosomal involvement and cell-free antigen presentation. Dev Immunol 1992, 3(1):51-65.
53. Romøren K., Thu B.J., Evensen Ø. Expression of luciferase in selected organs following delivery of naked and formulated DNA to rainbow trout (Oncorhynchus mykiss) by different routes of administration. Fish Shellfish Immunol 2004 Feb, 16(2):251-264.
54. Kanellos T., Sylvester I.D., Howard C.R., Russell P.H. DNA is as effective as protein at inducing antibody in fish. Vaccine 1999, 26:965-972.
55. Leitner W.W., Hwang L.N., Bergmann-Leitner E.S., Finkelstein S.E., Frank S., Restifo N.P. Apoptosis is essential for the increased efficacy of alphaviral replicase-based DNA vaccines. Vaccine 2004 Mar 29, 22(11-12):1537-1544.
56. Ying H., Zaks T.Z., Wang R.F., Irvine K.R., Kammula U.S., Marincola F.M., et al. Cancer therapy using a self-replicating RNA vaccine. Nat Med 1999 Jul, 5(7):823-827.
57. Acosta F., Petrie A., Lockhart K., Lorenzen N., Ellis A.E. Kinetics of Mx expression in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar L.) parr in response to VHS-DNA vaccination. Fish Shellfish Immunol 2005 Jan, 18(1):81-89.
58. Lorenzen N., Lorenzen E., Einer-Jensen K., Heppell J., Wu T., Davis H. Protective immunity to VHS in rainbow trout (Oncorrhyncus mykiss, Walbaum) following DNA vaccination. Fish Shellfish Immunol 1998, 8(4):261-270.
59. Boudinot P., Bernard D., Boubekeur S., Thoulouze M.I., Bremont M., Benmansour A. The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout. JGen Virol 2004 Oct, 85(Pt 10):3099-3108.
60. Utke K., Kock H., Schuetze H., Bergmann S.M., Lorenzen N., Einer-Jensen K., et al. Cell-mediated immune responses in rainbow trout after DNA immunization against the viral hemorrhagic septicemia virus. Dev Comp Immunol 2008, 32(3):239-252.
61. Busch R.A. Polyvalent vaccines in fish: the interactive effects of multiple antigens. Dev Biol Stand 1997, 90:245-256.
62. Spickler A.R., Roth J.A. Adjuvants in veterinary vaccines: modes of action and adverse effects. JVet Intern Med 2003 May, 17(3):273-281.
63. Vogel F.R. Improving vaccine performance with adjuvants. Clin Infect Dis 2000 Jun, 30(Suppl.3):S266-S270.
64. Press C., Evensen Ø. The morphology of the immune system of teleost fishes. Fish Shellfish Immunol 1999, 9:309-318.