Induction of mucosal and systemic immunity against respiratory syncytial virus by inactivated virus supplemented with TLR9 and NOD2 ligands

Vaccine

Volumn 30, Issue 3, 2012, Pages 597-606

  Shafique, Muhammad ^a   Wilschut, Jan ^a   de Haan, Aalzen ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Mucosal immunity; NOD2 ligand; Respiratory syncytial virus; TLR9 ligand; Vaccine

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CPG OLIGODEOXYNUCLEOTIDE; EOTAXIN; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G2A; INACTIVATED RESPIRATORY SYNCYTIAL VIRUS VACCINE; INACTIVATED VIRUS VACCINE; INTERLEUKIN 5; MESSENGER RNA; PROPIOLACTONE; RESPIRATORY SYNCYTIAL VIRUS VACCINE; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN BINDING; ANTIGEN PRESENTING CELL; ARTICLE; CELL ACTIVATION; CELL LINE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EFFICACY; DRUG SAFETY; EOSINOPHIL; FEMALE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LUNG INFILTRATE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RESPIRATORY SYSTEM; T LYMPHOCYTE; TH1 CELL; UPPER RESPIRATORY TRACT; VIRUS IMMUNITY; VIRUS INACTIVATION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, MUCOSAL; ANIMALS; CELL LINE; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MACROPHAGES; MICE; MICE, INBRED BALB C; NOD2 SIGNALING ADAPTOR PROTEIN; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; TH1 CELLS; TOLL-LIKE RECEPTOR 9; VACCINES, INACTIVATED;

EID: 84355166406     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.11.054     Document Type: Article

References (50)

1. Dowell S.F., Anderson L.J., Gary H.E., Erdman D.D., Plouffe J.F., File T.M., et al. Respiratory syncytial virus is an important cause of community-acquired lower respiratory infection among hospitalized adults. J Infect Dis 1996, 174(3):456-462.
2. Falsey A.R., Hennessey P.A., Formica M.A., Cox C., Walsh E.E. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005, 352(17):1749-1759.
3. 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 1969, 89(4):422-434.
4. Graham B.S. Biological challenges and technological opportunities for respiratory syncytial virus vaccine development. Immunol Rev 2011, 239(1):149-166.
5. Waris M.E., Tsou C., Erdman D.D., Zaki S.R., Anderson L.J. Respiratory synctial virus infection in BALB/c mice previously immunized with formalin-inactivated virus induces enhanced pulmonary inflammatory response with a predominant Th2-like cytokine pattern. J Virol 1996, 70(5):2852-2860.
6. Culley F.J., Pennycook A.M., Tregoning J.S., Hussell T., Openshaw P.J. Differential chemokine expression following respiratory virus infection reflects Th1- or Th2-biased immunopathology. J Virol 2006, 80(9):4521-4527.
7. Miller A.L., Bowlin T.L., Lukacs N.W. Respiratory syncytial virus-induced chemokine production: linking viral replication to chemokine production in vitro and in vivo. J Infect Dis 2004, 189(8):1419-1430.
8. Delgado M.F., Coviello S., Monsalvo A.C., Melendi G.A., Hernandez J.Z., Batalle J.P., et al. Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat Med 2009, 15(1):34-41.
9. Hussell T., Humphreys I.R. Nasal vaccination induces protective immunity without immunopathology. Clin Exp Immunol 2002, 130(3):359-362.
10. Singleton R., Etchart N., Hou S., Hyland L. Inability to evoke a long-lasting protective immune response to respiratory syncytial virus infection in mice correlates with ineffective nasal antibody responses. J Virol 2003, 77(21):11303-11311.
11. Mapletoft J.W., Latimer L., Babiuk L.A., van Drunen Littel-van d.H. Intranasal immunization of mice with a bovine respiratory syncytial virus vaccine induces superior immunity and protection compared to those by subcutaneous delivery or combinations of intranasal and subcutaneous prime-boost strategies. Clin Vaccine Immunol 2010, 17(1):23-35.
12. Kimman T.G., Westenbrink F., Schreuder B.E., 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 1987, 25(6):1097-1106.
13. Hall C.B., Walsh E.E., Long C.E., Schnabel K.C. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991, 163(4):693-698.
14. Taylor C.E., Craft A.W., Kernahan J., Millman R., Reid M.M., Scott R., et al. Local antibody production and respiratory syncytial virus infection in children with leukaemia. J Med Virol 1990, 30(4):277-281.
15. Belyakov I.M. What role does the route of immunization play in the generation of protective immunity against mucosal pathogens. J Immunol 2009, 183(11):6883-6892.
16. Boukhvalova M.S., Prince G.A., Soroush L., Harrigan D.C., Vogel S.N., Blanco J.C. The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease. Vaccine 2006, 24(23):5027-5035.
17. Johnson T.R., Rao S., Seder R.A., Chen M., Graham B.S. TLR9 agonist, but not TLR7/8, functions as an adjuvant to diminish FI-RSV vaccine-enhanced disease, while either agonist used as therapy during primary RSV infection increases disease severity. Vaccine 2009, 27(23):3045-3052.
18. Stegmann T., Kamphuis T., Meijerhof T., Goud E., De Haan A., Wilschut J. Lipopeptide-adjuvanted respiratory syncytial virus virosomes: a safe and immunogenic non-replicating vaccine formulation. Vaccine 2010, 28(34):5543-5550.
19. Tada H., Aiba S., Shibata K., Ohteki T., Takada H. Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect Immun 2005, 73(12):7967-7976.
20. McCluskie M.J., Weeratna R.D., Davis H.L. Intranasal immunization of mice with CpG DNA induces strong systemic and mucosal responses that are influenced by other mucosal adjuvants and antigen distribution. Mol Med 2000, 6(10):867-877.
21. Fukushima A., Yoo Y.C., Yoshimatsu K., Matsuzawa K., Tamura M., Tono-oka S., et al. Effect of MDP-Lys(L18) as a mucosal immunoadjuvant on protection of mucosal infections by Sendai virus and rotavirus. Vaccine 1996, 14(6):485-491.
22. Gallichan W.S., Woolstencroft R.N., Guarasci T., McCluskie M.J., Davis H.L., Rosenthal K.L. Intranasal immunization with CpG oligodeoxynucleotides as an adjuvant dramatically increases IgA and protection against herpes simplex virus-2 in the genital tract. J Immunol 2001, 166(5):3451-3457.
23. Lin L., Gerth A.J., Peng S.L. CpG DNA redirects class-switching towards Th1-like Ig isotype production via TLR9 and MyD88. Eur J Immunol 2004, 34(5):1483-1487.
24. Ogawa T., Shimauchi H., Hamada S. Mucosal and systemic immune responses in BALB/c mice to Bacteroides gingivalis fimbriae administered orally. Infect Immun 1989, 57(11):3466-3471.
25. Southam D.S., Dolovich M., O'Byrne P.M., Inman M.D. Distribution of intranasal instillations in mice: effects of volume, time, body position, and anesthesia. Am J Physiol Lung Cell Mol Physiol 2002, 282(4):L833-L839.
26. De Haan A., Geerligs H.J., Huchshorn J.P., van Scharrenburg G.J., Palache A.M., Wilschut J. Mucosal immunoadjuvant activity of liposomes: induction of systemic IgG and secretory IgA responses in mice by intranasal immunization with an influenza subunit vaccine and coadministered liposomes. Vaccine 1995, 13(2):155-162.
27. Yuan J.S., Reed A., Chen F., Stewart C.N. Statistical analysis of real-time PCR data. BMC Bioinformatics 2006, 7:85.
28. Prince G.A., Mond J.J., Porter D.D., Yim K.C., Lan S.J., Klinman D.M. Immunoprotective activity and safety of a respiratory syncytial virus vaccine: mucosal delivery of fusion glycoprotein with a CpG oligodeoxynucleotide adjuvant. J Virol 2003, 77(24):13156-13160.
29. Jakob T., Walker P.S., Krieg A.M., von Stebut E., Udey M.C., Vogel J.C., et al. CpG-containing oligodeoxynucleotides activate cutaneous dendritic cells and induce IL-12 production: implications for the augmentation of Th1 responses. Int Arch Allergy Immunol 1999, 118(2-4):457-461.
30. Amidi M., Romeijn S.G., Verhoef J.C., Junginger H.E., Bungener L., Huckriede A., et al. N-trimethyl chitosan (TMC) nanoparticles loaded with influenza subunit antigen for intranasal vaccination: biological properties and immunogenicity in a mouse model. Vaccine 2007, 25(1):144-153.
31. Wolvers D.A., van dC, Kraal G. Mucosal tolerance is associated with, but independent of, up-regulation of Th2 responses. Immunology 1997, 92(3):328-333.
32. Mestecky J., Moldoveanu Z., Elson C.O. Immune response versus mucosal tolerance to mucosally administered antigens. Vaccine 2005, 23(15):1800-1803.
33. Balmelli C., Demotz S., cha-Orbea H., De G.P., Nardelli-Haefliger D. Trachea, lung, and tracheobronchial lymph nodes are the major sites where antigen-presenting cells are detected after nasal vaccination of mice with human papillomavirus type 16 virus-like particles. J Virol 2002, 76(24):12596-12602.
34. Bessa J., Jegerlehner A., Hinton H.J., Pumpens P., Saudan P., Schneider P., et al. Alveolar macrophages and lung dendritic cells sense RNA and drive mucosal IgA responses. J Immunol 2009, 183(6):3788-3799.
35. Klinman D.M., Yi A.K., Beaucage S.L., Conover J., Krieg A.M. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci USA 1996, 93(7):2879-2883.
36. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374(6522):546-549.
37. Yi A.K., Hornbeck P., Lafrenz D.E., Krieg A.M. CpG DNA rescue of murine B lymphoma cells from anti-IgM-induced growth arrest and programmed cell death is associated with increased expression of c-myc and bcl-xL. J Immunol 1996, 157(11):4918-4925.
38. Petterson T., Jendholm J., Mansson A., Bjartell A., Riesbeck K., Cardell L.O. Effects of NOD-like receptors in human B lymphocytes and crosstalk between NOD1/NOD2 and Toll-like receptors. J Leukoc Biol 2011, 89(2):177-187.
39. Litinskiy M.B., Nardelli B., Hilbert D.M., He B., Schaffer A., Casali P., et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 2002, 3(9):822-829.
40. Craxton A., Magaletti D., Ryan E.J., Clark E.A. Macrophage- and dendritic cell-dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF. Blood 2003, 101(11):4464-4471.
41. Katsenelson N., Kanswal S., Puig M., Mostowski H., Verthelyi D., Akkoyunlu M. Synthetic CpG oligodeoxynucleotides augment BAFF- and APRIL-mediated immunoglobulin secretion. Eur J Immunol 2007, 37(7):1785-1795.
42. Nardelli B., Belvedere O., Roschke V., Moore P.A., Olsen H.S., Migone T.S., et al. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 2001, 97(1):198-204.
43. Xu W., Santini P.A., Matthews A.J., Chiu A., Plebani A., He B., et al. Viral double-stranded RNA triggers Ig class switching by activating upper respiratory mucosa B cells through an innate TLR3 pathway involving BAFF. J Immunol 2008, 181(1):276-287.
44. Fisher R.G., Crowe J.E., Johnson T.R., Tang Y.W., Graham B.S. Passive IgA monoclonal antibody is no more effective than IgG at protecting mice from mucosal challenge with respiratory syncytial virus. J Infect Dis 1999, 180(4):1324-1327.
45. Weltzin R., Hsu S.A., Mittler E.S., Georgakopoulos K., Monath T.P. Intranasal monoclonal immunoglobulin A against respiratory syncytial virus protects against upper and lower respiratory tract infections in mice. Antimicrob Agents Chemother 1994, 38(12):2785-2791.
46. Weltzin R., Traina-Dorge V., Soike K., Zhang J.Y., Mack P., Soman G., et al. Intranasal monoclonal IgA antibody to respiratory syncytial virus protects rhesus monkeys against upper and lower respiratory tract infection. J Infect Dis 1996, 174(2):256-261.
47. Kim S., Jang J.E., Yu J.R., Chang J. Single mucosal immunization of recombinant adenovirus-based vaccine expressing F1 protein fragment induces protective mucosal immunity against respiratory syncytial virus infection. Vaccine 2010, 28(22):3801-3808.
48. Valosky J., Hishiki H., Zaoutis T.E., Coffin S.E. Induction of mucosal B-cell memory by intranasal immunization of mice with respiratory syncytial virus. Clin Diagn Lab Immunol 2005, 12(1):171-179.
49. De Swart R.L., LiCalsi C., Quirk A.V., van Amerongen G., Nodelman V., Alcock R., et al. Measles vaccination of macaques by dry powder inhalation. Vaccine 2007, 25(7):1183-1190.
50. Sou T., Meeusen E.N., de Veer M., Morton D.A., Kaminskas L.M., McIntosh M.P. New developments in dry powder pulmonary vaccine delivery. Trends Biotechnol 2011, 29(4):191-198.