A soluble nonglycosylated recombinant infectious hematopoietic necrosis virus (IHNV) G-protein induces IFNs in rainbow trout (Oncorhynchus mykiss)

Fish and Shellfish Immunology

Volumn 25, Issue 1-2, 2008, Pages 170-180

  Verjan, Noel ^a   Ooi, Ei Lin ^a   Nochi, Tomonori ^a   Kondo, Hidehiro ^b   Hirono, Ikuo ^b   Aoki, Takashi ^b   Kiyono, Hiroshi ^a   Yuki, Yoshikazu ^a  

^a THE UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

IFN; IHNV; Innate immune response; Leukocyte activation; Recombinant G protein

Indexed keywords

INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; ONCORHYNCHUS MYKISS;

EID: 44749092713     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2008.04.004     Document Type: Article

References (74)

1. Roche S., Bressanelli S., Rey F.A., and Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313 (2006) 187-191
2. Coll J.M. The glycoprotein G of rhabdoviruses. Arch Virol 140 (1995) 827-851
3. Ito Y., Nishiyama Y., Shimokata K., Takeyama H., and Kunii A. Active component of HVJ (sendai virus) for interferon induction in mice. Nature 274 (1978) 801-802
4. Ito Y., and Hosaka Y. Component(s) of Sendai virus that can induce interferon in mouse spleen cells. Infect Immun 39 (1983) 1019-1023
5. Ito Y. Induction of interferon by virus glycoprotein(s) in lymphoid cells through interaction with the cellular receptors via lectin-like action: an alternative interferon induction mechanism. Arch Virol 138 (1994) 187-198
6. Charley B., and Laude H. Induction of alpha interferon by transmissible gastroenteritis coronavirus: role of transmembrane glycoprotein E1. J Virol 62 (1988) 8-11
7. Laude H., Gelfi J., Lavenant L., and Charley B. Single amino acid changes in the viral glycoprotein M affect induction of alpha interferon by the coronavirus transmissible gastroenteritis virus. J Virol 66 (1992) 743-749
8. Capobianchi M.R., Ankel H., Ameglio F., Paganelli R., Pizzoli P.M., and Dianzani F. Recombinant glycoprotein 120 of human immunodeficiency virus is a potent interferon inducer. AIDS Res Hum Retroviruses 8 (1992) 575-579
9. Bieback K., Lien E., Klagge I.M., Avota E., Schneider-Schaulies J., Duprex W.P., et al. Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J Virol 76 (2002) 8729-8736
10. Rassa J.C., Meyers J.L., Zhang Y., Kudaravalli R., and Ross S.R. Murine retroviruses activate B cells via interaction with toll-like receptor 4. Proc Natl Acad Sci U S A 99 (2002) 2281-2286
11. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T., et al. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 77 (2003) 4588-4596
12. Boehme K.W., Guerrero M., and Compton T. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J Immunol 177 (2006) 7094-7102
13. Georgel P., Jiang Z., Kunz S., Janssen E., Mols J., Hoebe K., et al. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362 (2007) 304-313
14. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
15. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303 (2004) 1526-1529
16. Lenoir G., and de Kinkelin P. Fish rhabdoviruses: comparative study of protein structure. J Virol 16 (1975) 259-262
17. McAllister P.E., and Wagner R.R. Structural proteins of two salmonid rhabdoviruses. J Virol 15 (1975) 733-738
18. Engelking H.M., and Leong J.C. The glycoprotein of infectious hematopoietic necrosis virus elicits neutralizing antibody and protective responses. Virus Res 13 (1989) 213-230
19. Anderson E.D., Mourich D.V., Fahrenkrug S.C., LaPatra S., Shepherd J., and Leong J.A. Genetic immunization of rainbow trout (Oncorhynchus mykiss) against infectious hematopoietic necrosis virus. Mol Mar Biol Biotechnol 5 (1996) 114-122
20. Lorenzen N., Lorenzen E., Einer-Jensen K., Heppell J., Wu T., and Davis H. Protective immunity to VHS in rainbow trout (Oncorhynchus mykiss, Walbaum) following DNA vaccination. Fish Shellfish Immunol 8 (1998) 261-270
21. Boudinot P., Blanco M., de Kinkelin P., and 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 non specific response in rainbow trout. Virology 249 (1998) 297-306
22. Lorenzen N., Lorenzen E., Einer-Jensen K., Heppell J., and Davis H.L. Genetic vaccination of rainbow trout against viral haemorrhagic septicaemia virus: small amounts of plasmid DNA protect against a heterologous serotype. Virus Res 63 (1999) 19-25
23. Corbeil S., Lapatra S.E., Anderson E.D., Jones J., Vincent B., Hsu Y.L., et al. Evaluation of the protective immunogenicity of the N, P, M, NV and G proteins of infectious hematopoietic necrosis virus in rainbow trout Oncorhynchus mykiss using DNA vaccines. Dis Aquat Org 39 (1999) 29-36
24. Corbeil S., LaPatra S.E., Anderson E.D., and Kurath G. Nanogram quantities of a DNA vaccine protect rainbow trout fry against heterologous strains of infectious hematopoietic necrosis virus. Vaccine 18 (2000) 2817-2824
25. Corbeil S., Kurath G., and LaPatra S.E. Fish DNA vaccine against infectious hematopoietic necrosis virus: efficacy of various routes of immunisation. Fish Shellfish Immunol 10 (2000) 711-723
26. 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 19 (2001) 4011-4019
27. Kurath G., Garver K.A., Corbeil S., Elliott D.G., Anderson E.D., and LaPatra S.E. Protective immunity and lack of histopathological damage two years after DNA vaccination against infectious hematopoietic necrosis virus in trout. Vaccine 24 (2006) 345-354
28. Kim C.H., Johnson M.C., Drennan J.D., Simon B.E., Thomann E., and Leong J.A. DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. J Virol 74 (2000) 7048-7054
29. Lorenzen N., Lorenzen E., and Einer-Jensen K. Immunity to viral haemorrhagic septicaemia (VHS) following DNA vaccination of rainbow trout at an early life-stage. Fish Shellfish Immunol 11 (2001) 585-591
30. Purcell M.K., Kurath G., Garver K.A., Herwig R.P., and Winton J.R. Quantitative expression profiling of immune response genes in rainbow trout following infectious haematopoietic necrosis virus (IHNV) infection or DNA vaccination. Fish Shellfish Immunol 17 (2004) 447-462
31. Boudinot P., Bernard D., Boubekeur S., Thoulouze M.I., Bremont M., and Benmansour A. The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout. J Gen Virol 85 (2004) 3099-3108
32. Purcell M.K., Nichols K.M., Winton J.R., Kurath G., Thorgaard G.H., Wheeler P., et al. Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol Immunol 43 (2006) 2089-2106
33. 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 32 (2008) 239-252
34. Lorenzen N., Olesen N.J., Jorgensen P.E., Etzerodt M., Holtet T.L., and Thogersen H.C. Molecular cloning and expression in Escherichia coli of the glycoprotein gene of VHS virus, and immunization of rainbow trout with the recombinant protein. J Gen Virol 74 Pt 4 (1993) 623-630
35. Lecocq-Xhonneux F., Thiry M., Dheur I., Rossius M., Vanderheijden N., Martial J., et al. A recombinant viral haemorrhagic septicaemia virus glycoprotein expressed in insect cells induces protective immunity in rainbow trout. J Gen Virol 75 Pt 7 (1994) 1579-1587
36. Mitra N., Sinha S., Ramya T.N., and Surolia A. N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31 (2006) 156-163
37. + T lymphocytes. J Immunol 173 (2004) 7150-7160
38. Ooi EL, Verjan N, Hirono I, Nochi T, Kondo H, Aoki T, et al. Biological characterisation of a recombinant Atlantic salmon type I interferon synthesized in Escherichia coli. Fish Shellfish Immunol 2008;24:506-513.
39. Reed L., and Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg 27 (1938) 493-497
40. Oshima S, Imajoh, M., Fukuda, H., Goto, T. Ando, A. IHNV strain HV7601 G gene. Published only in the NCBI Database; 2005.
41. Yanagida M., Miura Y., Yagasaki K., Taoka M., Isobe T., and Takahashi N. Matrix assisted laser desorption/ionization-time of flight-mass spectrometry analysis of proteins detected by anti-phosphotyrosine antibody on two-dimensional-gels of fibroblast cell lysates after tumor necrosis factor-alpha stimulation. Electrophoresis 21 (2000) 1890-1898
42. Zou J., Carrington A., Collet B., Dijkstra J.M., Yoshiura Y., Bols N., et al. Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175 (2005) 2484-2494
43. Zou J., Tafalla C., Truckle J., and Secombes C.J. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179 (2007) 3859-3871
44. Boehme K.W., and Compton T. Innate sensing of viruses by toll-like receptors. J Virol 78 (2004) 7867-7873
45. Gilmore R.D., Engelking H.M., Manning D.S., and Leong J.C. Expression in Escherichia coli of an epitope of the glycoprotein of infectious hematopoietic necrosis virus protects against viral challenge. Bio/Technology 6 (1988) 295-300
46. Oberg L.A., Wirkkula J., Mourich D., and Leong J.C. Bacterially expressed nucleoprotein of infectious hematopoietic necrosis virus augments protective immunity induced by the glycoprotein vaccine in fish. J Virol 65 (1991) 4486-4489
47. Xu L., Mourich D.V., Engelking H.M., Ristow S., Arnzen J., and Leong J.C. Epitope mapping and characterization of the infectious hematopoietic necrosis virus glycoprotein, using fusion proteins synthesized in Escherichia coli. J Virol 65 (1991) 1611-1615
48. Sato M., Taniguchi T., and Tanaka N. The interferon system and interferon regulatory factor transcription factors - studies from gene knockout mice. Cytokine Growth Factor Rev 12 (2001) 133-142
49. Collet B., Hovens G.C., Mazzoni D., Hirono I., Aoki T., and Secombes C.J. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2). Dev Comp Immunol 27 (2003) 111-126
50. Boyle K.A., Pietropaolo R.L., and Compton T. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol Cell Biol 19 (1999) 3607-3613
51. Sato A., Linehan M.M., and Iwasaki A. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci U S A 103 (2006) 17343-17348
52. Kurt-Jones E.A., Chan M., Zhou S., Wang J., Reed G., Bronson R., et al. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc Natl Acad Sci U S A 101 (2004) 1315-1320
53. Boudinot P., Massin P., Blanco M., Riffault S., and Benmansour A. vig-1, a new fish gene induced by the rhabdovirus glycoprotein, has a virus-induced homologue in humans and shares conserved motifs with the MoaA family. J Virol 73 (1999) 1846-1852
54. Iliev D.B., Roach J.C., Mackenzie S., Planas J.V., and Goetz F.W. Endotoxin recognition: in fish or not in fish?. FEBS Lett 579 (2005) 6519-6528
55. Purcell M.K., Smith K.D., Hood L., Winton J.R., and Roach J.C. Conservation of Toll-like receptor signaling pathways in teleost fish. Comp Biochem Physiol Part D Genomics Proteomics 1 (2006) 77-88
56. Iliev D.B., Liarte C.Q., MacKenzie S., and Goetz F.W. Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular pattern (PAMP) bearing agents. Mol Immunol 42 (2005) 1215-1223
57. Amend D.F., and Smith L. Pathophysiology of infectious hematopoietic necrosis virus disease in rainbow trout: hematological and blood chemical changes in moribund fish. Infect Immun 11 (1975) 171-179
58. Lampert P.W. Antibody-induced capping of measles virus antigens on plasma membrane studied by electron microscopy. J Virol 15 (1975) 1248-1255
59. Persson R., Svensson U., and Everitt E. Virus receptor interaction in the adenovirus system. II. Capping and cooperative binding of virions on HeLa cells. J Virol 46 (1983) 956-963
60. Lydy S.L., and Compans R.W. Role of the cytoplasmic domains of viral glycoproteins in antibody-induced cell surface mobility. J Virol 67 (1993) 6289-6294
61. Favoreel H.W., Nauwynck H.J., Van Oostveldt P., Mettenleiter T.C., and Pensaert M.B. Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J Virol 71 (1997) 8254-8261
62. Storrie B., and Edelson P.J. Distribution of concanavalin A in fibroblasts: direct endocytosis versus surface capping. Cell 11 (1977) 707-717
63. Burnett K. Signal transduction mediated by antigen receptors on teleost lymphocytes. Annu Rev Fish Dis 6 (1996) 193-206
64. MacDougal K.C., Mericko P.A., and Burnett K.G. Antigen receptor-mediated activation of extracellular related kinase (ERK) in B lymphocytes of teleost fishes. Dev Comp Immunol 23 (1999) 221-230
65. van Ginkel F.W., Miller N.W., Cuchens M.A., and Clem L.W. Activation of channel catfish B cells by membrane immunoglobulin cross-linking. Dev Comp Immunol 18 (1994) 97-107
66. Reth M. Antigen receptors on B lymphocytes. Annu Rev Immunol 10 (1992) 97-121
67. Campbell K.S. Signal transduction from the B cell antigen-receptor. Curr Opin Immunol 11 (1999) 256-264
68. Ma H., Yankee T.M., Hu J., Asai D.J., Harrison M.L., and Geahlen R.L. Visualization of Syk-antigen receptor interactions using green fluorescent protein: differential roles for Syk and Lyn in the regulation of receptor capping and internalization. J Immunol 166 (2001) 1507-1516
69. Liu X., and Collodi P. Novel form of fibronectin from zebrafish mediates infectious hematopoietic necrosis virus infection. J Virol 76 (2002) 492-498
70. Bearzotti M., Delmas B., Lamoureux A., Loustau A.M., Chilmonczyk S., and Bremont M. Fish rhabdovirus cell entry is mediated by fibronectin. J Virol 73 (1999) 7703-7709
71. Smith A.E., and Helenius A. How viruses enter animal cells. Science 304 (2004) 237-242
72. Okada N., Watarai M., Ozeri V., Hanski E., Caparon M., and Sasakawa C. A matrix form of fibronectin mediates enhanced binding of Streptococcus pyogenes to host tissue. J Biol Chem 272 (1997) 26978-26984
73. + T lymphocytes. J Immunol 164 (2000) 3236-3245
74. Greco G., Pal S., Pasqualini R., and Schnapp L.M. Matrix fibronectin increases HIV stability and infectivity. J Immunol 168 (2002) 5722-5729