Vaccination of calves using the BRSV nucleocapsid protein in a DNA prime-protein boost strategy stimulates cell-mediated immunity and protects the lungs against BRSV replication and pathology

Vaccine

Volumn 26, Issue 37, 2008, Pages 4840-4848

  Carine, Letellier ^a   Mathieu, Boxus ^b   Laurent, Rosar ^a   Jean François, Toussaint ^a   Karl, Walravens ^a   Stefan, Roels ^a   Gilles, Meyer ^c   Jean Jacques, Letesson ^d   Pierre, Kerkhofs ^a  

^a VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c CNRS   (France)

^d UNIVERSITY OF NAMUR   (Belgium)

Author keywords

BRSV; Nucleocapsid gene; Prime boost

Indexed keywords

GAMMA INTERFERON; GUANINE NUCLEOTIDE BINDING PROTEIN; NUCLEOCAPSID PROTEIN; PLASMID DNA; PRIMER DNA; VIRUS GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; BOVINE RESPIRATORY SYNCYTIAL PNEUMOVIRUS; CALF (BOVINE); CD8+ T LYMPHOCYTE; CELL CULTURE; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DNA IMMUNIZATION; HISTOPATHOLOGY; IMMUNOSTIMULATION; LUNG INFECTION; LUNG LAVAGE; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROLOGY; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CATTLE; CATTLE DISEASES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; IMMUNIZATION, SECONDARY; INTERFERON TYPE II; LUNG; NUCLEOCAPSID PROTEINS; PLASMIDS; PNEUMONIA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, BOVINE; VACCINES, DNA; VACCINES, SUBUNIT;

EID: 49549105098     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2008.06.100     Document Type: Article

References (74)

1. Brandenburg A.H., Neijens H.J., and Osterhaus A.D.M.E. Pathogenesis of RSV lower respiratory tract infection: implications for vaccine development. Vaccine 19 (2001) 2769-2782
2. Larsen L.E. Bovine respiratory syncytial virus (BRSV): a review. Acta Vet Scand 41 (2000) 1-24
3. Van der Poel W.H., Brand A., Kramps J.A., and Van Oirschot T.J. Respiratory syncytial virus infections in human beings and in cattle. J Infect 29 (1994) 215-228
4. Belknap E.B., Baker J.C., Patterson J.S., Walker R.D., Haines D.M., and Clark E.G. The role of passive immunity in bovine respiratory syncytial virus-infected calves. J Infect Dis 163 (1991) 470-476
5. Kimman T.G., Westenbrink F., Schreuder B.E.C., and Straver P.J. Local and systemic antibody response to bovine respiratory syncytial virus infection and reinfection in calves with and without maternal antibodies. J Clin Microbiol 25 (1987) 1097-1106
6. Kimman T.G., Zimmer G.M., Westenbrink F., Mars J., and van Leeuwen E. Epidemiological study of bovine respiratory syncytial virus infections in calves: Influence of maternal antibodies on the outcome of disease. Vet Rec 123 (1988) 104-109
7. Ellis J.A. The immunology of the bovine respiratory disease complex. Vet Clin North Am Food Anim Pract 17 (2001) 535-550
8. Peters A.R., Thevasagayam S.J., Wieseman A., and Salt J.S. Duration of immunity of a quadrivalent vaccine against respiratory diseases caused by BHV-1, PIV3, BVDV, and BRSV in experimentally infected calves. Prev Vet Med 66 (2004) 63-77
9. Patel J.R., and Didlick S.A. Evaluation of efficacy of an inactivated vaccine against BRSV in calves with maternal antibodies. Am J Vet Res 65 (2004) 417-421
10. Ellis J., Gow S., West K., Waldner C., Rhodes C., Mutwiri G., et al. Response of calves to challenge exposure with virulent BRSV following intranasal administration of vaccines formulated for parenteral administration. J Am Vet Med Assoc 15 (2007) 233-243
11. Kim H.W., Canchola J.G., Brandt C.D., Pyles G., Chanock R.M., Jensen K., et al. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 89 (1969) 422-434
12. Gershwin L.J., Schelegle E.S., Gunther R.A., Anderson M.L., Woolums A.R., Larochelle D.R., et al. A bovine model of vaccine enhanced respiratory syncytial virus pathophysiology. Vaccine 16 (1998) 1225-1236
13. Hussell T., Baldwin C.J., O'Garra A., and Openshaw P.J. CD8+ T cells control Th2-driven pathology during pulmonary respiratory syncytial virus infection. Eur J Immunol 27 (1997) 3341-3349
14. Varga S.M., Wang X., Welsh R.M., and Braciale T.J. Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4(+) T cells. Immunity 15 (2001) 637-646
15. Connors M., Giese N.A., Kulkarni A.B., Firestone C.Y., Morse III H.C., and Murphy B.R. Enhanced pulmonary histopathology induced by respiratory syncytial virus (RSV) challenge of formalin-inactivated RSV-immunized BALB/c mice is abrogated by depletion of interleukin-4 (IL-4) and IL-10. J Virol 68 (1994) 5321-5325
16. Antonis A.F.G., Schrijver R.S., Daus F., Steverink P.J.G.M., Stockhofe N., Hensen E.J., et al. Vaccine-induced immunopathology during bovine respiratory syncytial virus infection: exploring the parameters of pathogenesis. J Virol 77 (2003) 12067-12073
17. Gershwin L.J., Gunther R.A., Anderson M.L., Woolums A.R., McArthur- Vaughan K., Randel K.E., et al. Bovine respiratory syncytial virus-specific IgE is associated with interleukin-2 and -4, and interferon-gamma expression in pulmonary lymph of experimentally infected calves. Am J Vet Res 61 (2000) 291-298
18. Kalina W.V., Woolums A.R., Berghaus R.D., and Gershwin L.J. Formalin-inactivated bovine RSV vaccine enhances a Th2 mediated immune response in infected cattle. Vaccine 22 (2004) 1465-1474
19. Schreiber P., Matheise J.P., Dessy F., Heimann M., Letesson J.-J., Coppe P., et al. High mortality rate associated with bovine respiratory syncytial virus (BRSV) infection in Belgian white blue calves previously vaccinated with an inactivated BRSV vaccine. J Vet Med B Infect Dis Vet Public Health 47 (2000) 535-550
20. Larsen L.E., Tegtmeier C., and Pedersen E. Bovine respiratory syncytial virus (BRSV) pneumonia in beef calf herds despite vaccination. Acta Vet Scand 42 (2001) 113-121
21. Taylor G., Thomas L.H., Furze J.M., Cook R.S., Wyld S.G., Lerch R., et al. Recombinant vaccinia viruses expressing the F, G or N, but not the M2, protein of bovine respiratory syncytial virus (BRSV) induce resistance to BRSV challenge in the calf and protect against the development of pneumonic lesions. J Gen Virol 78 (1997) 3195-3206
22. Thomas L.H., Cook R.S., Wyld S.G., Furze J.M., and Taylor G. Passive protection of gnotobiotic caves using monoclonal antibodies directed at different epitopes on the fusion protein of bovine respiratory syncytial virus. J Infect Dis 177 (1998) 874-880
23. Taylor G., Thomas L.H., Wyld S.G., Furze J.M., Sopp P., and Howard C.J. Role of T-lymphocyte subsets in recovery from respiratory syncytial virus infection in calves. J Virol 69 (1995) 6658-6664
24. Braciale T.J. Respiratory Syncytial virus and T cells Interplay between the virus and the host adaptive immune system. Proc Am Thorac Soc 2 (2005) 141-146
25. Openshaw P.J., and Tregoning J.S. Immune responses and disease enhancement during respiratory syncytial virus infection. Clin Microbiol Rev 18 (2005) 541-555
26. Bangham C.R., Openshaw P.J., Ball L.A., King A.M., Wertz G.W., and Askonas B.A. Human and murine cytotoxic T cells specific to respiratory syncytial virus recognize the viral nucleoprotein (N), but not the major glycoprotein (G), expressed by vaccinia virus recombinants. J Immunol 137 (1986) 3973-3977
27. Connors M., Kulkarni A.B., Collins P.L., Firestone C.-Y., Holmes K.L., Morse H.C., et al. Resistance to respiratory syncytial virus (RSV) challenge induced by infection with a vaccinia virus recombinant expressing the RSV M2 protein is mediated by CD8+ T cells, while that induced by Vac-F or Vac-G recombinants is mediated by antibodies. J Virol 66 (1992) 1277-1281
28. Gaddum R.M., Cook R.S., Furze J.M., Ellis S.A., and Taylor G. Recognition of bovine respiratory syncytial virus proteins by bovine CD8+ T lymphocytes. Immunology 108 (2003) 220-229
29. Antonis A.F.G., Claassen E.A.W., Hensen E.J., de Groot R.J., de Groot-Mijnes J.D.F., Schrijver R.S., et al. Kinetics of antiviral CD8 T cell responses during primary and post-vaccination secondary bovine respiratory syncytial virus infection. Vaccine 24 (2006) 1551-1561
30. Gaddum R.M., Cook R.S., Thomas L.H., and Taylor G. Primary cytotoxic T-cell responses to bovine respiratory syncytial virus in calves. Immunology 88 (1996) 421-427
31. McInnes E., Sopp P., Howard C.J., and Taylor G. Phenotypic analysis of local cellular responses in calves infected with bovine respiratory syncytial virus. Immunology 96 (1999) 396-403
32. Rutigliano J.A., Johnson T.R., Hollinger T.N., Fischer J.E., Aung S., and Graham B.S. Treatment with anti-LFA-1 delays the CD8+ cytotoxic-T-lymphocyte response and viral clearance in mice with primary respiratory syncytial virus infection. J Virol 78 (2004) 3014-3023
33. Srikiatkhachorn A., and Braciale T.J. Virus-specific CD8+ T lymphocytes downregulate T helper cell type 2 cytokine secretion and pulmonary eosinophilia during experimental murine respiratory syncytial virus infection. J Exp Med 186 (1997) 421-432
34. Robinson H.L., and Pertmer T.M. DNA vaccines for viral infections: basic studies and applications. Adv Virus Res 55 (2000) 1-74
35. Bembridge G.P., Rodriguez N., Garcia-Beato R., Nicolson C., Melero J.A., and Taylor G. DNA encoding the attachment (G) or fusion (F) protein of respiratory syncytial virus induces protection in the absence of pulmonary inflammation. J Gen Virol 81 (2000) 2519-2523
36. Brady R.P., Topliff C.L., and Kelling C.L. In vitro expression of full-length and truncated bovine respiratory syncytial virus G proteins and their antibody responses in BALB/c mice. Vaccine 22 (2004) 3762-3768
37. Babiuk L.A., Pontarollo R., Babiuk S., Loehr B., and van Drunen Littel-van den Hurk S. Induction of immune response by DNA vaccines in large animals. Vaccine 21 (2003) 649-658
38. Toussaint J.F., Letellier C., Paquet D., Dispas M., and Kerkhofs P. Prime-boost strategies combining DNA and inactivated vaccines confer high immunity and protection in cattle against bovine herpesvirus-1. Vaccine 23 (2005) 5073-5081
39. Boxus M., Tignon M., Toussaint J.-F., Roels S., Benoit M.A., Walravens K., et al. DNA immunization against fusion and nucleocapsid proteins protects calves against BRSV. J Virol 81 (2007) 6879-6889
40. Martinez X., Li X., Kovarik J., Klein M., Lambert P.-H., and Siegrist C.-A. Combining DNA and protein vaccination for early life immunization against RSV in mice. Eur J Immunol 29 (1999) 3390-3400
41. Samal S.K., Zamora M., McPhillips T.H., and Mohanty S.B. Molecular cloning and sequence analysis of Bovine Respiratory Syncytial Virus mRNA encoding the major nucleocapsid protein. Virology 180 (1991) 453-456
42. Tjornehoj K., Uttenthal A., Viuff B., Larsen L.E., Rontved C., and Ronsholt L. An experimental infection model for reproduction of calf pneumonia with bovine respiratory syncytial virus (BRSV) based on one combined exposure of calves. Res Vet Sci 74 (2003) 55-65
43. Wellemans G., and Leunen J. La Rhino-trachéite infectieuse des bovins et sa sérologie. Ann Méd Vét 117 (1973) 507518
44. Uttenthal A., Larsen L.E., Philipsen J.S., Tjornehoj K., Viuff B., Nielsen K.H., et al. Antibidy dynamics in BRSV-infected Danish dairy herds as determined by isotype-specific immunoglobulins. Vet Microbiol 76 (2000) 329-341
45. Boxus M., Letellier C., and Kerkhofs P. Real Time RT-PCR for the detection and quantitation of bovine respiratory syncytial virus. J Virol Methods 125 (2005) 125-130
46. Gurunathan S., Klinman D.M., and Seder R.A. DNA vaccines: immunology, application, and optimization. Annu Rev Immunol 18 (2000) 927-974
47. Van Drunen Little-van den Hurk S., Braun R.P., Lewis P.J., Karvonen B.C., Babiuk L.A., and Griebel P.J. Immunization of neonates with DNA encoding a bovine herpesvirus glycoprotein is effective in the presence of maternal antibodies. Viral Immunol 12 (1999) 67-77
48. Martinez X., Brandt C., Saddallah F., Tougne C., Barrios C., Wild F., et al. DNA immunization circumvents deficient induction of TH1 and cytotoxic T cells lymphocyte responses in neonates and during early life. PNAS 94 (1997) 8726-8731
49. Morein B., Abusugra I., and Blomqvist G. Immunity in neonates. Vet Immunol Immunopathol 87 (2002) 207-213
50. Li X., Sambhara S., Li C.X., Ewasyshyn M., Parrington M., Caterini J., et al. Protection against respiratory syncytial virus infection by DNA immunization. J Exp Med 188 (1998) 681-688
51. Li X., Sambhara S., Li C.X., Ettorre L., Switzer I., Cates G., et al. Plasmid DNA encoding the respiratory syncytial virus G protein is a promising vaccine candidate. Virology 269 (2000) 54-65
52. Schrijver R.S., Langedijk J.P., Keil G.M., Middel W.G.J., Maris-Veldhuis M., Van Oirschot J.T., et al. Immunization of cattle with a BHV1 vector vaccine or a DNA vaccine both coding for the G protein of BRSV. Vaccine 15 (1997) 1908-1916
53. Schrijver R.S., Langedijk J.P., Keil G.M., Middel W.G.J., Maris-Veldhuis M., Van Oirschot J.T., et al. Comparison of DNA application methods to reduce BRSV shedding in cattle. Vaccine 16 (1998) 130-134
54. Taylor G., Bruce C., Barbet A.F., Wyld S.G., and Thomas L.H. DNA vaccination against respiratory syncytial virus in young calves. Vaccine 23 (2005) 1242-1250
55. Vaughan K., Rhodes G.H., and Gershwin L.J. DNA immunization against respiratory syncytial virus (RSV) in infant rhesus monkeys. Vaccine 23 (2005) 2928-2942
56. King A.M.Q., Stott E.J., Langer S.J., Young K.K.-Y., Ball L.A., and Wertz G.W. Recombinant vaccinia virus carrying the N gene of Human respiratory syncytial virus: studies of gene expression in cell culture and immune response in mice. J Virol 61 (1987) 2885-2890
57. Connors M., Collins P.L., Firestone C.-Y., and Murphy B. Respiratory syncytial virus (RSV) F, G, M2, and N proteins each induce resistance to RSV challenge, but resistance induced by M2 and N proteins is relatively short-lived. J Virol 65 (1991) 1634-1637
58. Grell S.N., Riber U., Tjornehoj K., Larsen L.E., and Heegaard P.M.H. Age-dependent differences in cytokine and antibody responses after experimental RSV infection in a bovine model. Vaccine 23 (2005) 3412-3423
59. Viuff B., Tjornehoj K., Larsen L.E., Rontved C., Uttenthal A., Ronsholt L., et al. Replication and clearance of respiratory syncytial virus apoptosis is an important pathway of virus clearance after experimental infection with BRSV. Am J Pathology 161 (2002) 2195-2207
60. Estes D.M., and Brown W.C. Type 1 and type 2 responses in regulation of Ig isotype expression in cattle. Vet Immunol Immunopathol 90 (2002) 1-10
61. Cannon M.J., Openshaw P.J., and Askonas B.A. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J Exp Med 168 (1988) 1163-1168
62. Ostler T., Davidson W., and Ehl S. Virus clearance and immunopathology by CD8(+) T cells during infection with respiratory syncytial virus are mediated by IFN-gamma. Eur J Immunol 32 (2002) 2117-2123
63. Aung S., Tang Y.W., and Graham B.S. Interleukin-4 diminishes CD8(+) respiratory syncytial virus-specific cytotoxic T lymphocyte activity in vivo. J Virol 73 (1999) 8944-8949
64. Woolums A.R., Singer R.S., Boyle G.A., and Gershwin L.J. Interferon gamma production during bovine respiratory syncytial virus (BRSV) infection is diminished in calves vaccinated with formalin-inactivated BRSV. Vaccine 17 (1999) 1293-1297
65. Oumouna M., Mapletoft J.W., Karvonen B.C., Babiuk L.A., and van Drunen Littel-van den Hurk S. Formulation with CpG oligodeoxynucleotides prevents induction of pulmonary immunopathology following priming with formalin-inactivated or commercial killed bovine respiratory syncytial virus vaccine. J Virol 79 (2005) 2024-2032
66. Mapletoft J.W., Oumouna M., Townsend H.G., Gomis S., Babiuk L.A., and van Drunen Littel-van den Hurk S. Formulation with CpG oligodeoxynucleotides increases cellular immunity and protection induced by vaccination of calves with formalin-inactivated bovine respiratory syncytial virus. Virology 353 (2006) 316-323
67. West K., Petrie L., Konoby C., Haines D.M., Cortese V., and Ellis J.A. The efficacy of modified-live bovine respiratory syncytial virus vaccines in experimentally infected calves. Vaccine 18 (2000) 907-919
68. Sharma A.K., Woldehiwet Z., Walravens K., and Letesson J. Immune response of lambs to the fusion glycoprotein of BRSV expressed on insect cells infected with a recombinant baculovirus. Vaccine 14 (1996) 773-779
69. Abe T., Takahashi H., Hamazaki H., Miyano-kurosaki N., Matsuura Y., and Takaku H. Baculovirus induces an innate immune response and confers protection from lethal Influenza virus infection in mice. J Immunol 171 (2003) 1133-1139
70. Liang R., van den Hurk J.V., Babiuk L.A., and van Drunen Littel-van den Hurk S. Priming with DNA encoding E2 and boosting with E2 protein formulated with CpG oligodeoxynucleotides induces strong immune responses and protection from Bovine viral diarrhea virus in cattle. J Gen Virol 87 (2006) 2971-2982
71. Estcourt M.J., Ramsay A.J., Brooks A., Thomson S.A., Medveckzy C.J., and Ramshaw I.A. Prime-boost immunization generates a high frequency, high-avidity CD8(+) cytotoxic T lymphocyte population. Int Immunol 14 (2002) 31-37
72. Loehr B.I., Pontarollo R., Rankin R., Latimer L., Willson P., Babiuk L.A., et al. Priming by DNA immunization augments T-cell responses induced by modified live bovine herpesvirus vaccine. J Gen Virol 82 (2001) 3035-3043
73. Kong W.-p., Xu l., Stadler K., Ulmer J.B., Abrignani S., Rappuoli R., et al. Modulation of the immune response to the severe acute respiratory syndrome spike glycoprotein by gene-based and inactivated virus immunization. J Virol 79 (2005) 13915-13923
74. Cristillo A.D., Wang S., Caskey M.S., Unangst T., Hocker L., He L., et al. Preclinical evaluation of cellular immune responses elicited by a polyvalent DNA prime/protein boost HIV-1 vaccine. Virology 346 (2006) 151-168