TLR4 and MyD88 control protection and pulmonary granulocytic recruitment in a murine intranasal RSV immunization and challenge model

Vaccine

Volumn 27, Issue 3, 2009, Pages 421-430

  Cyr, Sonya L ^a,b   Angers, Isabelle ^c   Guillot, Loic ^c   Stoica Popescu, Ioana ^b   Lussier, Michèle ^b   Qureshi, Salman ^c   Burt, David S ^b   Ward, Brian J ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b GLAXOSMITHKLINE   (Canada)

^c MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Lung inflammation; MyD88; RSV; TLR2; TLR4; Vaccine

Indexed keywords

BETA INTERFERON; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 5; MYELOID DIFFERENTIATION FACTOR 88; PROTOLLIN ENRICHED RESPIRATORY SYNCYTIAL VIRUS VACCINE; RESPIRATORY SYNCYTIAL VIRUS VACCINE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; FEMALE; GENE EXPRESSION; GRANULOCYTE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOSTIMULATION; LUNG INFILTRATE; MALE; MOUSE; MOUSE STRAIN; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION; SPLEEN CELL; TH1 CELL; TH2 CELL; UPREGULATION; VACCINATION; VIRUS INFECTION; VIRUS NEUTRALIZATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, VIRAL; BACTERIAL OUTER MEMBRANE PROTEINS; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; FEMALE; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NEISSERIA MENINGITIDIS; NEUTROPHILS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; SHIGELLA FLEXNERI; SPLEEN; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 57749193730     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2008.10.073     Document Type: Article

References (61)

1. Kapikian A.Z., Mitchell R.H., Chanock R.M., Shvedoff R.A., and Stewart C.E. An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol 89 April (4) (1969) 405-421
2. Prince G.A., Curtis S.J., Yim K.C., and Porter D.D. Vaccine-enhanced respiratory syncytial virus disease in cotton rats following immunization with Lot 100 or a newly prepared reference vaccine. J Gen Virol 82 December (Pt 12) (2001) 2881-2888
3. Haynes L.M., Jones L.P., Barskey A., Anderson L.J., and Tripp R.A. Enhanced disease and pulmonary eosinophilia associated with formalin-inactivated respiratory syncytial virus vaccination are linked to G glycoprotein CX3C-CX3CR1 interaction and expression of substance P. J Virol 77 September (18) (2003) 9831-9844
4. 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 August (8) (1994) 5321-5325
5. Waris M.E., Tsou C., Erdman D.D., Zaki S.R., and Anderson L.J. Respiratory syncytial 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 70 May (5) (1996) 2852-2860
6. Boelen A., Andeweg A., Kwakkel J., Lokhorst W., Bestebroer T., Dormans J., et al. Both immunisation with a formalin-inactivated respiratory syncytial virus (RSV) vaccine and a mock antigen vaccine induce severe lung pathology and a Th2 cytokine profile in RSV-challenged mice. Vaccine 19 November (7-8) (2000) 982-991
7. Boukhvalova M.S., Prince G.A., Soroush L., Harrigan D.C., Vogel S.N., and Blanco J.C. The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease. Vaccine 24 June (23) (2006) 5027-5035
8. Cyr S.L., Jones T., Stoica-Popescu I., Burt D., and Ward B.J. C57Bl/6 mice are protected from respiratory syncytial virus (RSV) challenge and IL-5 associated pulmonary eosinophilic infiltrates following intranasal immunization with Protollin-eRSV vaccine. Vaccine 25 April (16) (2007) 3228-3232
9. Etchart N., Baaten B., Andersen S.R., Hyland L., Wong S.Y., and Hou S. Intranasal immunisation with inactivated RSV and bacterial adjuvants induces mucosal protection and abrogates eosinophilia upon challenge. Eur J Immunol 36 May (5) (2006) 1136-1144
10. Cyr S.L., Jones T., Stoica-Popescu I., Brewer A., Chabot S., Lussier M., et al. Intranasal proteosome-based respiratory syncytial virus (RSV) vaccines protect BALB/c mice against challenge without eosinophilia or enhanced pathology. Vaccine 25 July (29) (2007) 5378-5389
11. Jegerlehner A., Maurer P., Bessa J., Hinton H.J., Kopf M., and Bachmann M.F. TLR9 signaling in B cells determines class switch recombination to IgG2a. J Immunol 178 February (4) (2007) 2415-2420
12. Reinhardt R.L., Hong S., Kang S.J., Wang Z.E., and Locksley R.M. Visualization of IL-12/23p40 in vivo reveals immunostimulatory dendritic cell migrants that promote Th1 differentiation. J Immunol 177 August (3) (2006) 1618-1627
13. Jones T., Cyr S., Allard F., Bellerose N., Lowell G.H., and Burt D.S. Protollin: a novel adjuvant for intranasal vaccines. Vaccine 22 September (27-28) (2004) 3691-3697
14. Massari P., Visintin A., Gunawardana J., Halmen K.A., King C.A., Golenbock D.T., et al. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J Immunol 176 February (4) (2006) 2373-2380
15. Saitoh S., Akashi S., Yamada T., Tanimura N., Kobayashi M., Konno K., et al. Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int Immunol 16 July (7) (2004) 961-969
16. Chabot S., Brewer A., Lowell G., Plante M., Cyr S., Burt D.S., et al. A novel intranasal Protollin-based measles vaccine induces mucosal and systemic neutralizing antibody responses and cell-mediated immunity in mice. Vaccine 23 February (11) (2005) 1374-1383
17. Fries L.F., Montemarano A.D., Mallett C.P., Taylor D.N., Hale T.L., and Lowell G.H. Safety and immunogenicity of a proteosome-Shigella flexneri 2a lipopolysaccharide vaccine administered intranasally to healthy adults. Infect Immun 69 July (7) (2001) 4545-4553
18. Jones T., Adamovicz J.J., Cyr S.L., Bolt C.R., Bellerose N., Pitt L.M., et al. Intranasal Protollintrade mark/F1-V vaccine elicits respiratory and serum antibody responses and protects mice against lethal aerosolized plague infection. Vaccine October (2005) 7
19. Hawrylowicz C.M., and O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol 5 April (4) (2005) 271-283
20. O'Garra A., and Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 7 June (6) (2007) 425-428
21. Urry Z., Xystrakis E., and Hawrylowicz C.M. Interleukin-10-secreting regulatory T cells in allergy and asthma. Curr Allergy Asthma Rep 6 September (5) (2006) 363-371
22. Burdin N., Van K.C., Galibert L., Abrams J.S., Wijdenes J., Banchereau J., et al. Endogenous IL-6 and IL-10 contribute to the differentiation of CD40-activated human B lymphocytes. J Immunol 154 March (6) (1995) 2533-2544
23. Moore K.W., de Waal M.R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19 (2001) 683-765
24. Sun J., Walsh M., Villarino A.V., Cervi L., Hunter C.A., Choi Y., et al. TLR ligands can activate dendritic cells to provide a MyD88-dependent negative signal for Th2 cell development. J Immunol 174 January (2) (2005) 742-751
25. Sun J., Krawczyk C.J., and Pearce E.J. Suppression of Th2 cell development by Notch ligands Delta1 and Delta4. J Immunol 180 February (3) (2008) 1655-1661
26. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int Immunol 17 January (1) (2005) 1-14
27. van D.D., Medzhitov R., and Shaw A.C. Triggering TLR signaling in vaccination. Trends Immunol 27 January (1) (2006) 49-55
28. Blander J.M., and Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 304 May (5673) (2004) 1014-1018
29. West M.A., Wallin R.P., Matthews S.P., Svensson H.G., Zaru R., Ljunggren H.G., et al. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305 August (5687) (2004) 1153-1157
30. Steinman R.M., Hawiger D., and Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 21 (2003) 685-711
31. Lanzavecchia A., and Sallusto F. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr Opin Immunol 13 June (3) (2001) 291-298
32. Kalinski P., Hilkens C.M., Wierenga E.A., and Kapsenberg M.L. T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today 20 December (12) (1999) 561-567
33. Pasare C., and Medzhitov R. Control of B-cell responses by Toll-like receptors. Nature 438 November (7066) (2005) 364-368
34. Ruprecht C.R., and Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 36 April (4) (2006) 810-816
35. Merolla R., Rebert N.A., Tsiviste P.T., Hoffmann S.P., and Panuska J.R. Respiratory syncytial virus replication in human lung epithelial cells: inhibition by tumor necrosis factor alpha and interferon beta. Am J Respir Crit Care Med 152 October (4 Pt 1) (1995) 1358-1366
36. Yamamoto M., Sato S., Hemmi H., Uematsu S., Hoshino K., Kaisho T., et al. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 4 November (11) (2003) 1144-1150
37. Covert M.W., Leung T.H., Gaston J.E., and Baltimore D. Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 309 September (5742) (2005) 1854-1857
38. Yamamoto M., Sato S., Mori K., Hoshino K., Takeuchi O., Takeda K., et al. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 169 December (12) (2002) 6668-6672
39. Jones T., Allard F., Cyr S.L., Tran S.P., Plante M., Gauthier J., et al. A nasal Proteosome influenza vaccine containing baculovirus-derived hemagglutinin induces protective mucosal and systemic immunity. Vaccine 21 September (25-26) (2003) 3706-3712
40. Payment P., and Trudel M. Isolation and identification of viruses. Methods and techniques in virology (1993), Marccel Dekker, Inc., New York
41. Steinman R.M., and Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311 (2006) 17-58
42. Rudd B.D., Schaller M.A., Smit J.J., Kunkel S.L., Neupane R., Kelley L., et al. MyD88-mediated instructive signals in dendritic cells regulate pulmonary immune responses during respiratory virus infection. J Immunol 178 May (9) (2007) 5820-5827
43. Sahi-Ozaki Y., Itamura S., Ichinohe T., Strong P., Tamura S., Takahashi H., et al. Intranasal administration of adjuvant-combined recombinant influenza virus HA vaccine protects mice from the lethal H5N1 virus infection. Microbes Infect 8 October (12-13) (2006) 2706-2714
44. Schulze K., Olive C., Ebensen T., and Guzman C.A. Intranasal vaccination with SfbI or M protein-derived peptides conjugated to diphtheria toxoid confers protective immunity against a lethal challenge with Streptococcus pyogenes. Vaccine 24 August (35-36) (2006) 6088-6095
45. Becker P.D., Fiorentini S., Link C., Tosti G., Ebensen T., Caruso A., et al. The HIV-1 matrix protein p17 can be efficiently delivered by intranasal route in mice using the TLR 2/6 agonist MALP-2 as mucosal adjuvant. Vaccine 24 June (25) (2006) 5269-5276
46. Guay H.M., Andreyeva T.A., Garcea R.L., Welsh R.M., and Szomolanyi-Tsuda E. MyD88 is required for the formation of long-term humoral immunity to virus infection. J Immunol 178 April (8) (2007) 5124-5131
47. Ehlers M., Fukuyama H., McGaha T.L., Aderem A., and Ravetch J.V. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med 203 March (3) (2006) 553-561
48. Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., and Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2 October (10) (2001) 947-950
49. Blander J.M., and Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440 April (7085) (2006) 808-812
50. Rutz S., Janke M., Kassner N., Hohnstein T., Krueger M., and Scheffold A. Notch regulates IL-10 production by T helper 1 cells. Proc Natl Acad Sci U S A 105 March (9) (2008) 3497-3502
51. Briere F., Servet-Delprat C., Bridon J.M., Saint-Remy J.M., and Banchereau J. Human interleukin 10 induces naive surface immunoglobulin D+ (sIgD+) B cells to secrete IgG1 and IgG3. J Exp Med 179 February (2) (1994) 757-762
52. Rousset F., Garcia E., Defrance T., Peronne C., Vezzio N., Hsu D.H., et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci USA 89 March (5) (1992) 1890-1893
53. Bembridge G.P., Rodriguez N., Garcia-Beato R., Nicolson C., Melero J.A., and Taylor G. Respiratory syncytial virus infection of gene gun vaccinated mice induces Th2-driven pulmonary eosinophilia even in the absence of sensitisation to the fusion (F) or attachment (G) protein. Vaccine 19 December (9-10) (2000) 1038-1046
54. Johnson T.R., Johnson J.E., Roberts S.R., Wertz G.W., Parker R.A., and Graham B.S. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosinophilia after RSV challenge. J Virol 72 April (4) (1998) 2871-2880
55. Yasui K., Baba A., Iwasaki Y., Kubo T., Aoyama K., Mori T., et al. Neutrophil-mediated inflammation in respiratory syncytial viral bronchiolitis. Pediatr Int 47 April (2) (2005) 190-195
56. McNamara P.S., Ritson P., Selby A., Hart C.A., and Smyth R.L. Bronchoalveolar lavage cellularity in infants with severe respiratory syncytial virus bronchiolitis. Arch Dis Child 88 October (10) (2003) 922-926
57. Smith P.K., Wang S.Z., Dowling K.D., and Forsyth K.D. Leucocyte populations in respiratory syncytial virus-induced bronchiolitis. J Paediatr Child Health 37 April (2) (2001) 146-151
58. Bataki E.L., Evans G.S., and Everard M.L. Respiratory syncytial virus and neutrophil activation. Clin Exp Immunol 140 June (3) (2005) 470-477
59. Wang S.Z., Smith P.K., Lovejoy M., Bowden J.J., Alpers J.H., and Forsyth K.D. Shedding of L-selectin and PECAM-1 and upregulation of Mac-1 and ICAM-1 on neutrophils in RSV bronchiolitis. Am J Physiol 275 November (5 Pt 1) (1998) L983-L989
60. Bukreyev A., Belyakov I.M., Prince G.A., Yim K.C., Harris K.K., Berzofsky J.A., et al. Expression of interleukin-4 by recombinant respiratory syncytial virus is associated with accelerated inflammation and a nonfunctional cytotoxic T-lymphocyte response following primary infection but not following challenge with wild-type virus. J Virol 79 August (15) (2005) 9515-9526
61. Schramm R., and Thorlacius H. Neutrophil recruitment in mast cell-dependent inflammation: inhibitory mechanisms of glucocorticoids. Inflamm Res 53 December (12) (2004) 644-652