Advanced search
Publication Cover
Expert Review of Vaccines Volume 11, 2012 - Issue 12
Submit an article Journal homepage
524
Views
23
CrossRef citations to date
0
Altmetric
Review

The role of dendritic cells in innate and adaptive immunity to respiratory syncytial virus, and implications for vaccine development

Ravendra Garg VIDO-Intervac, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada; VIDO-Intervac, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada
,
Pratima Shrivastava VIDO-Intervac, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada; VIDO-Intervac, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada
&
Sylvia van Drunen Littel-van den Hurk VIDO-Intervac, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada; Microbiology & Immunology, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada. [email protected]; Microbiology & Immunology, University of Saskatchewan, Saskatoon, SK, S7N 5E3, Canada. [email protected]
Pages 1441-1457 | Published online: 09 Jan 2014

References

  • Wright M, Piedimonte G. Respiratory syncytial virus prevention and therapy: past, present, and future. Pediatr. Pulmonol. 46(4), 324–347 (2011).
  • Howard TS, Hoffman LH, Stang PE, Simoes EA. Respiratory syncytial virus pneumonia in the hospital setting: length of stay, charges, and mortality. J. Pediatr. 137(2), 227–232 (2000).
  • Shay DK, Holman RC, Roosevelt GE, Clarke MJ, Anderson LJ. Bronchiolitis-associated mortality and estimates of respiratory syncytial virus-associated deaths among US children, 1979-1997. J. Infect. Dis. 183(1), 16–22 (2001).
  • Nair H, Nokes DJ, Gessner BD et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375(9725), 1545–1555 (2010).
  • Kim HW, Arrobio JO, Brandt CD et al. Epidemiology of respiratory syncytial virus infection in Washington, D.C. I. Importance of the virus in different respiratory tract disease syndromes and temporal distribution of infection. Am. J. Epidemiol. 98(3), 216–225 (1973).
  • Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am. J. Respir. Crit. Care Med. 161(5), 1501–1507 (2000).
  • Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352(17), 1749–1759 (2005).
  • Kapikian AZ, Mitchell RH, Chanock RM, Shvedoff RA, Stewart CE. 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(4), 405–421 (1969).
  • Kim HW, Canchola JG, Brandt CD et al. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am. J. Epidemiol. 89(4), 422–434 (1969).
  • Prince GA, Curtis SJ, Yim KC, Porter DD. Vaccine-enhanced respiratory syncytial virus disease in cotton rats following immunization with Lot 100 or a newly prepared reference vaccine. J. Gen. Virol. 82(Pt 12), 2881–2888 (2001).
  • Murphy BR, Alling DW, Snyder MH et al. Effect of age and preexisting antibody on serum antibody response of infants and children to the F and G glycoproteins during respiratory syncytial virus infection. J. Clin. Microbiol. 24(5), 894–898 (1986).
  • Collins PL, Melero JA. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 162(1–2), 80–99 (2011).
  • van Drunen Littel-van den Hurk S, Mapletoft JW, Arsic N, Kovacs-Nolan J. Immunopathology of RSV infection: prospects for developing vaccines without this complication. Rev. Med. Virol. 17(1), 5–34 (2007).
  • Mukherjee S, Lindell DM, Berlin AA et al. IL-17-induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease. Am. J. Pathol. 179(1), 248–258 (2011).
  • van Bleek GM, Osterhaus AD, de Swart RL. RSV 2010: recent advances in research on respiratory syncytial virus and other pneumoviruses. Vaccine 29(43), 7285–7291 (2011).
  • Fulton RB, Meyerholz DK, Varga SM. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185(4), 2382–2392 (2010).
  • Lee DC, Harker JA, Tregoning JS et al. CD25+ natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J. Virol. 84(17), 8790–8798 (2010).
  • Ruckwardt TJ, Bonaparte KL, Nason MC, Graham BS. Regulatory T cells promote early influx of CD8+ T cells in the lungs of respiratory syncytial virus-infected mice and diminish immunodominance disparities. J. Virol. 83(7), 3019–3028 (2009).
  • Moghaddam A, Olszewska W, Wang B et al. A potential molecular mechanism for hypersensitivity caused by formalin-inactivated vaccines. Nat. Med. 12(8), 905–907 (2006).
  • Delgado MF, Coviello S, Monsalvo AC et al. Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat. Med. 15(1), 34–41 (2009).
  • Klein Klouwenberg P, Tan L, Werkman W, van Bleek GM, Coenjaerts F. The role of Toll-like receptors in regulating the immune response against respiratory syncytial virus. Crit. Rev. Immunol. 29(6), 531–550 (2009).
  • Condon TV, Sawyer RT, Fenton MJ, Riches DW. Lung dendritic cells at the innate-adaptive immune interface. J. Leukoc. Biol. 90(5), 883–895 (2011).
  • Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu. Rev. Immunol. 30, 243–270 (2012).
  • Lukens MV, Kruijsen D, Coenjaerts FE, Kimpen JL, van Bleek GM. Respiratory syncytial virus-induced activation and migration of respiratory dendritic cells and subsequent antigen presentation in the lung-draining lymph node. J. Virol. 83(14), 7235–7243 (2009).
  • Davidson S, Kaiko G, Loh Z et al. Plasmacytoid dendritic cells promote host defense against acute pneumovirus infection via the TLR7-MyD88-dependent signaling pathway. J. Immunol. 186(10), 5938–5948 (2011).
  • Fitzgerald-Bocarsly P, Feng D. The role of type I interferon production by dendritic cells in host defense. Biochimie 89(6–7), 843–855 (2007).
  • Colonna M, Trinchieri G, Liu YJ. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5(12), 1219–1226 (2004).
  • Takagi H, Fukaya T, Eizumi K et al. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 35(6), 958–971 (2011).
  • Tang F, Du Q, Liu YJ. Plasmacytoid dendritic cells in antiviral immunity and autoimmunity. Sci. China. Life Sci. 53(2), 172–182 (2010).
  • Plantinga M, Hammad H, Lambrecht BN. Origin and functional specializations of DC subsets in the lung. Eur. J. Immunol. 40(8), 2112–2118 (2010).
  • Lukacs NW, Smit JJ, Schaller MA, Lindell DM. Regulation of immunity to respiratory syncytial virus by dendritic cells, Toll-like receptors, and notch. Viral Immunol. 21(2), 115–122 (2008).
  • Kurt-Jones EA, Popova L, Kwinn L et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1(5), 398–401 (2000).
  • Polack FP, Irusta PM, Hoffman SJ et al. The cysteine-rich region of respiratory syncytial virus attachment protein inhibits innate immunity elicited by the virus and endotoxin. Proc. Natl Acad. Sci. USA 102(25), 8996–9001 (2005).
  • Gill MA, Palucka AK, Barton T et al. Mobilization of plasmacytoid and myeloid dendritic cells to mucosal sites in children with respiratory syncytial virus and other viral respiratory infections. J. Infect. Dis. 191(7), 1105–1115 (2005).
  • Guerrero-Plata A, Kolli D, Hong C, Casola A, Garofalo RP. Subversion of pulmonary dendritic cell function by paramyxovirus infections. J. Immunol. 182(5), 3072–3083 (2009).
  • Wythe SE, Dodd JS, Openshaw PJ, Schwarze J. OX40 ligand and programmed cell death 1 ligand 2 expression on inflammatory dendritic cells regulates CD4 T cell cytokine production in the lung during viral disease. J. Immunol. 188(4), 1647–1655 (2012).
  • Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11(11), 762–774 (2011).
  • Wang H, Peters N, Laza-Stanca V, Nawroly N, Johnston SL, Schwarze J. Local CD11c+ MHC class II- precursors generate lung dendritic cells during respiratory viral infection, but are depleted in the process. J. Immunol. 177(4), 2536–2542 (2006).
  • Smit JJ, Rudd BD, Lukacs NW. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203(5), 1153–1159 (2006).
  • Bondue B, Vosters O, de Nadai P et al. ChemR23 dampens lung inflammation and enhances anti-viral immunity in a mouse model of acute viral pneumonia. PLoS Pathog. 7(11), e1002358 (2011).
  • Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 392(6673), 245–252 (1998).
  • Liu YJ. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106(3), 259–262 (2001).
  • Cella M, Facchetti F, Lanzavecchia A, Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 1(4), 305–310 (2000).
  • von Garnier C, Filgueira L, Wikstrom M et al. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J. Immunol. 175(3), 1609–1618 (2005).
  • Wikstrom ME, Stumbles PA. Mouse respiratory tract dendritic cell subsets and the immunological fate of inhaled antigens. Immunol. Cell Biol. 85(3), 182–188 (2007).
  • Kallal LE, Schaller MA, Lindell DM, Lira SA, Lukacs NW. CCL20/CCR6 blockade enhances immunity to RSV by impairing recruitment of DC. Eur. J. Immunol. 40(4), 1042–1052 (2010).
  • Hussell T, Spender LC, Georgiou A, O’Garra A, Openshaw PJ. Th1 and Th2 cytokine induction in pulmonary T cells during infection with respiratory syncytial virus. J. Gen. Virol. 77(Pt 10), 2447–2455 (1996).
  • Varga SM, Wang X, Welsh RM, Braciale TJ. Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4(+) T cells. Immunity 15(4), 637–646 (2001).
  • 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. 77(21), 11303–11311 (2003).
  • Belz GT, Smith CM, Kleinert L et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl Acad. Sci. USA 101(23), 8670–8675 (2004).
  • Yoon H, Legge KL, Sung SS, Braciale TJ. Sequential activation of CD8+ T cells in the draining lymph nodes in response to pulmonary virus infection. J. Immunol. 179(1), 391–399 (2007).
  • Kim TS, Hufford MM, Sun J, Fu YX, Braciale TJ. Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection. J. Exp. Med. 207(6), 1161–1172 (2010).
  • Olson MR, Hartwig SM, Varga SM. The number of respiratory syncytial virus (RSV)-specific memory CD8 T cells in the lung is critical for their ability to inhibit RSV vaccine-enhanced pulmonary eosinophilia. J. Immunol. 181(11), 7958–7968 (2008).
  • Stevens WW, Sun J, Castillo JP, Braciale TJ. Pulmonary eosinophilia is attenuated by early responding CD8(+) memory T cells in a murine model of RSV vaccine-enhanced disease. Viral Immunol. 22(4), 243–251 (2009).
  • Graham BS, Bunton LA, Wright PF, Karzon DT. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Invest. 88(3), 1026–1033 (1991).
  • Beyer M, Bartz H, Hörner K, Doths S, Koerner-Rettberg C, Schwarze J. Sustained increases in numbers of pulmonary dendritic cells after respiratory syncytial virus infection. J. Allergy Clin. Immunol. 113(1), 127–133 (2004).
  • Domachowske JB, Rosenberg HF. Respiratory syncytial virus infection: immune response, immunopathogenesis, and treatment. Clin. Microbiol. Rev. 12(2), 298–309 (1999).
  • Graham BS. Pathogenesis of respiratory syncytial virus vaccine-augmented pathology. Am. J. Respir. Crit. Care Med. 152(4 Pt 2), S63–S66 (1995).
  • Chang J, Braciale TJ. Respiratory syncytial virus infection suppresses lung CD8+ T-cell effector activity and peripheral CD8+ T-cell memory in the respiratory tract. Nat. Med. 8(1), 54–60 (2002).
  • Chang J, Srikiatkhachorn A, Braciale TJ. Visualization and characterization of respiratory syncytial virus F-specific CD8(+) T cells during experimental virus infection. J. Immunol. 167(8), 4254–4260 (2001).
  • Lukens MV, Claassen EA, de Graaff PM et al. Characterization of the CD8+ T cell responses directed against respiratory syncytial virus during primary and secondary infection in C57BL/6 mice. Virology 352(1), 157–168 (2006).
  • Chang J, Choi SY, Jin HT, Sung YC, Braciale TJ. Improved effector activity and memory CD8 T cell development by IL-2 expression during experimental respiratory syncytial virus infection. J. Immunol. 172(1), 503–508 (2004).
  • Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202(5), 637–650 (2005).
  • Boogaard I, van Oosten M, van Rijt LS et al. Respiratory syncytial virus differentially activates murine myeloid and plasmacytoid dendritic cells. Immunology 122(1), 65–72 (2007).
  • Smit JJ, Lindell DM, Boon L, Kool M, Lambrecht BN, Lukacs NW. The balance between plasmacytoid DC versus conventional DC determines pulmonary immunity to virus infections. PLoS ONE 3(3), e1720 (2008).
  • Wang H, Peters N, Schwarze J. Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. J. Immunol. 177(9), 6263–6270 (2006).
  • Jewell NA, Vaghefi N, Mertz SE et al. Differential type I interferon induction by respiratory syncytial virus and influenza a virus in vivo. J. Virol. 81(18), 9790–9800 (2007).
  • Guerrero-Plata A, Casola A, Suarez G et al. Differential response of dendritic cells to human metapneumovirus and respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 34(3), 320–329 (2006).
  • Thompson LJ, Kolumam GA, Thomas S, Murali-Krishna K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 177(3), 1746–1754 (2006).
  • Ruuskanen O, Arola M, Putto-Laurila A et al. Acute otitis media and respiratory virus infections. Pediatr. Infect. Dis. J. 8(2), 94–99 (1989).
  • Meurman O, Ruuskanen O, Sarkkinen H, Hänninen P, Halonen P. Immunoglobulin class-specific antibody response in respiratory syncytial virus infection measured by enzyme immunoassay. J. Med. Virol. 14(1), 67–72 (1984).
  • Welliver RC, Kaul TN, Putnam TI, Sun M, Riddlesberger K, Ogra PL. The antibody response to primary and secondary infection with respiratory syncytial virus: kinetics of class-specific responses. J. Pediatr. 96(5), 808–813 (1980).
  • Shay DK, Holman RC, Newman RD, Liu LL, Stout JW, Anderson LJ. Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 282(15), 1440–1446 (1999).
  • Stein RT, Sherrill D, Morgan WJ et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 354(9178), 541–545 (1999).
  • Golding J, Rogers IS, Emmett PM. Association between breast feeding, child development and behaviour. Early Hum. Dev. 49(Suppl.), S175–S184 (1997).
  • Angel Rico M, Trento A, Ramos M et al. Human respiratory syncytial virus infects and induces activation markers in mouse B lymphocytes. Immunol. Cell Biol. 87(4), 344–350 (2009).
  • Malhotra R, Ward M, Bright H et al. Isolation and characterisation of potential respiratory syncytial virus receptor(s) on epithelial cells. Microbes Infect. 5(2), 123–133 (2003).
  • de Graaff PM, de Jong EC, van Capel TM et al. Respiratory syncytial virus infection of monocyte-derived dendritic cells decreases their capacity to activate CD4 T cells. J. Immunol. 175(9), 5904–5911 (2005).
  • Johnson TR, Johnson CN, Corbett KS, Edwards GC, Graham BS. Primary human mDC1, mDC2, and pDC dendritic cells are differentially infected and activated by respiratory syncytial virus. PLoS ONE 6(1), e16458 (2011).
  • González PA, Prado CE, Leiva ED et al. Respiratory syncytial virus impairs T cell activation by preventing synapse assembly with dendritic cells. Proc. Natl Acad. Sci. USA 105(39), 14999–15004 (2008).
  • Hammad H, Lambrecht BN. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8(3), 193–204 (2008).
  • Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: soldier in the fight against respiratory viruses. Clin. Microbiol. Rev. 24(1), 210–229 (2011).
  • Qiao J, Li A, Jin X. TSLP from RSV-stimulated rat airway epithelial cells activates myeloid dendritic cells. Immunol. Cell Biol. 89(2), 231–238 (2011).
  • Tayyari F, Marchant D, Moraes TJ, Duan W, Mastrangelo P, Hegele RG. Identification of nucleolin as a cellular receptor for human respiratory syncytial virus. Nat. Med. 17(9), 1132–1135 (2011).
  • Hovanessian AG, Soundaramourty C, El Khoury D, Nondier I, Svab J, Krust B. Surface expressed nucleolin is constantly induced in tumor cells to mediate calcium-dependent ligand internalization. PLoS ONE 5(12), e15787 (2010).
  • Johnson TR, McLellan JS, Graham BS. Respiratory syncytial virus glycoprotein G interacts with DC-SIGN and L-SIGN to activate ERK1 and ERK2. J. Virol. 86(3), 1339–1347 (2012).
  • Jones A, Morton I, Hobson L, Evans GS, Everard ML. Differentiation and immune function of human dendritic cells following infection by respiratory syncytial virus. Clin. Exp. Immunol. 143(3), 513–522 (2006).
  • Hornung V, Schlender J, Guenthner-Biller M et al. Replication-dependent potent IFN-α induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J. Immunol. 173(10), 5935–5943 (2004).
  • Schlender J, Hornung V, Finke S et al. Inhibition of Toll-like receptor 7- and 9-mediated α/β interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79(9), 5507–5515 (2005).
  • Spann KM, Tran KC, Chi B, Rabin RL, Collins PL. Suppression of the induction of alpha, beta, and gamma interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages. J. Virol. 78(8), 4363–4369 (2004).
  • Munir S, Le Nouen C, Luongo C, Buchholz UJ, Collins PL, Bukreyev A. Nonstructural proteins 1 and 2 of respiratory syncytial virus suppress maturation of human dendritic cells. J. Virol. 82(17), 8780–8796 (2008).
  • Munir S, Hillyer P, Le Nouën C et al. Respiratory syncytial virus interferon antagonist NS1 protein suppresses and skews the human T lymphocyte response. PLoS Pathog. 7(4), e1001336 (2011).
  • Johnson JE, Gonzales RA, Olson SJ, Wright PF, Graham BS. The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 20(1), 108–119 (2007).
  • Le Nouën C, Hillyer P, Winter CC et al. Low CCR7-mediated migration of human monocyte derived dendritic cells in response to human respiratory syncytial virus and human metapneumovirus. PLoS Pathog. 7(6), e1002105 (2011).
  • Yeo SJ, Yun YJ, Lyu MA et al. Respiratory syncytial virus infection induces matrix metalloproteinase-9 expression in epithelial cells. Arch. Virol. 147(2), 229–242 (2002).
  • Pletneva LM, Haller O, Porter DD, Prince GA, Blanco JC. Induction of type I interferons and interferon-inducible Mx genes during respiratory syncytial virus infection and reinfection in cotton rats. J. Gen. Virol. 89(Pt 1), 261–270 (2008).
  • Guerrero-Plata A, Baron S, Poast JS, Adegboyega PA, Casola A, Garofalo RP. Activity and regulation of α interferon in respiratory syncytial virus and human metapneumovirus experimental infections. J. Virol. 79(16), 10190–10199 (2005).
  • Bartz H, Türkel O, Hoffjan S, Rothoeft T, Gonschorek A, Schauer U. Respiratory syncytial virus decreases the capacity of myeloid dendritic cells to induce interferon-gamma in naive T cells. Immunology 109(1), 49–57 (2003).
  • Schauer U, Hoffjan S, Rothoeft T et al. Severe respiratory syncytial virus infections and reduced interferon-gamma generation in vitro. Clin. Exp. Immunol. 138(1), 102–109 (2004).
  • Kondo Y, Matsuse H, Machida I et al. Regulation of mite allergen-pulsed murine dendritic cells by respiratory syncytial virus. Am. J. Respir. Crit. Care Med. 169(4), 494–498 (2004).
  • Chi B, Dickensheets HL, Spann KM et al. α and λ interferon together mediate suppression of CD4 T cells induced by respiratory syncytial virus. J. Virol. 80(10), 5032–5040 (2006).
  • Schlender J, Walliser G, Fricke J, Conzelmann KK. Respiratory syncytial virus fusion protein mediates inhibition of mitogen-induced T-cell proliferation by contact. J. Virol. 76(3), 1163–1170 (2002).
  • Plotkin SA. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47(3), 401–409 (2008).
  • Karron RA, Buonagurio DA, Georgiu AF et al. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl Acad. Sci. USA 94(25), 13961–13966 (1997).
  • Tripp RA, Moore D, Jones L, Sullender W, Winter J, Anderson LJ. Respiratory syncytial virus G and/or SH protein alters Th1 cytokines, natural killer cells, and neutrophils responding to pulmonary infection in BALB/c mice. J. Virol. 73(9), 7099–7107 (1999).
  • Johnson TR, Johnson JE, Roberts SR, Wertz GW, Parker RA, Graham BS. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosinophilia after RSV challenge. J. Virol. 72(4), 2871–2880 (1998).
  • Bukreyev A, Yang L, Fricke J et al. The secreted form of respiratory syncytial virus G glycoprotein helps the virus evade antibody-mediated restriction of replication by acting as an antigen decoy and through effects on Fc receptor-bearing leukocytes. J. Virol. 82(24), 12191–12204 (2008).
  • Johnson PR Jr, Olmsted RA, Prince GA et al. Antigenic relatedness between glycoproteins of human respiratory syncytial virus subgroups A and B: evaluation of the contributions of F and G glycoproteins to immunity. J. Virol. 61(10), 3163–3166 (1987).
  • Cane PA, Pringle CR. Evolution of subgroup A respiratory syncytial virus: evidence for progressive accumulation of amino acid changes in the attachment protein. J. Virol. 69(5), 2918–2925 (1995).
  • Sullender WM, Anderson K, Wertz GW. The respiratory syncytial virus subgroup B attachment glycoprotein: analysis of sequence, expression from a recombinant vector, and evaluation as an immunogen against homologous and heterologous subgroup virus challenge. Virology 178(1), 195–203 (1990).
  • Walsh EE, Hruska J. Monoclonal antibodies to respiratory syncytial virus proteins: identification of the fusion protein. J. Virol. 47(1), 171–177 (1983).
  • Ehl S, Bischoff R, Ostler T et al. The role of Toll-like receptor 4 versus interleukin-12 in immunity to respiratory syncytial virus. Eur. J. Immunol. 34(4), 1146–1153 (2004).
  • Lizundia R, Sauter KS, Taylor G, Werling D. Host species-specific usage of the TLR4-LPS receptor complex. Innate Immun. 14(4), 223–231 (2008).
  • Gan SW, Ng L, Lin X, Gong X, Torres J. Structure and ion channel activity of the human respiratory syncytial virus (hRSV) small hydrophobic protein transmembrane domain. Protein Sci. 17(5), 813–820 (2008).
  • Murphy BR, Hall SL, Kulkarni AB et al. An update on approaches to the development of respiratory syncytial virus (RSV) and parainfluenza virus type 3 (PIV3) vaccines. Virus Res. 32(1), 13–36 (1994).
  • Driver LC, Oertel MD. Synagis: an anti-RSV monoclonal antibody. Pediatr. Nurs. 25(5), 527–530 (1999).
  • Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today 14(7), 353–356 (1993).
  • Holt PG. Functionally mature virus-specific CD8(+) T memory cells in congenitally infected newborns: proof of principle for neonatal vaccination? J. Clin. Invest. 111(11), 1645–1647 (2003).
  • Deacock SJ, Schwarer AP, Bridge J, Batchelor JR, Goldman JM, Lechler RI. Evidence that umbilical cord blood contains a higher frequency of HLA class II-specific alloreactive T cells than adult peripheral blood. A limiting dilution analysis. Transplantation 53(5), 1128–1134 (1992).
  • Hunt DW, Huppertz HI, Jiang HJ, Petty RE. Studies of human cord blood dendritic cells: evidence for functional immaturity. Blood 84(12), 4333–4343 (1994).
  • Koga Y, Matsuzaki A, Suminoe A, Hattori H, Hara T. Expression of cytokine-associated genes in dendritic cells (DCs): comparison between adult peripheral blood- and umbilical cord blood-derived DCs by cDNA microarray. Immunol. Lett. 116(1), 55–63 (2008).
  • Levy O, Zarember KA, Roy RM, Cywes C, Godowski PJ, Wessels MR. Selective impairment of TLR-mediated innate immunity in human newborns: neonatal blood plasma reduces monocyte TNF-α induction by bacterial lipopeptides, lipopolysaccharide, and imiquimod, but preserves the response to R-848. J. Immunol. 173(7), 4627–4634 (2004).
  • Levy O, Suter EE, Miller RL, Wessels MR. Unique efficacy of Toll-like receptor 8 agonists in activating human neonatal antigen-presenting cells. Blood 108(4), 1284–1290 (2006).
  • Weeratna RD, Brazolot Millan CL, McCluskie MJ, Davis HL. CpG ODN can re-direct the Th bias of established Th2 immune responses in adult and young mice. FEMS Immunol. Med. Microbiol. 32(1), 65–71 (2001).
  • Siegrist CA. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21(24), 3406–3412 (2003).
  • O’Hagan DT, De Gregorio E. The path to a successful vaccine adjuvant – ‘the long and winding road’. Drug Discov. Today 14(11–12), 541–551 (2009).
  • Adair BM. Nanoparticle vaccines against respiratory viruses. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1(4), 405–414 (2009).
  • Widjojoatmodjo MN, Boes J, van Bers M, van Remmerden Y, Roholl PJ, Luytjes W. A highly attenuated recombinant human respiratory syncytial virus lacking the G protein induces long-lasting protection in cotton rats. Virol. J. 7, 114 (2010).
  • Schickli JH, Dubovsky F, Tang RS. Challenges in developing a pediatric RSV vaccine. Hum. Vaccin. 5(9), 582–591 (2009).
  • Karron RA, Wright PF, Belshe RB et al. Identification of a recombinant live attenuated respiratory syncytial virus vaccine candidate that is highly attenuated in infants. J. Infect. Dis. 191(7), 1093–1104 (2005).
  • Luongo C, Yang L, Winter CC et al. Codon stabilization analysis of the ‘248’ temperature sensitive mutation for increased phenotypic stability of respiratory syncytial virus vaccine candidates. Vaccine 27(41), 5667–5676 (2009).
  • Tang RS, MacPhail M, Schickli JH et al. Parainfluenza virus type 3 expressing the native or soluble fusion (F) protein of respiratory syncytial virus (RSV) confers protection from RSV infection in African green monkeys. J. Virol. 78(20), 11198–11207 (2004).
  • Jones B, Zhan X, Mishin V et al. Human PIV-2 recombinant Sendai virus (rSeV) elicits durable immunity and combines with two additional rSeVs to protect against hPIV-1, hPIV-2, hPIV-3, and RSV. Vaccine 27(12), 1848–1857 (2009).
  • Collins PL, Purcell RH, London WT, Lawrence LA, Chanock RM, Murphy BR. Evaluation in chimpanzees of vaccinia virus recombinants that express the surface glycoproteins of human respiratory syncytial virus. Vaccine 8(2), 164–168 (1990).
  • Martinez-Sobrido L, Gitiban N, Fernandez-Sesma A et al. Protection against respiratory syncytial virus by a recombinant Newcastle disease virus vector. J. Virol. 80(3), 1130–1139 (2006).
  • McGinnes LW, Gravel KA, Finberg RW et al. Assembly and immunological properties of Newcastle disease virus-like particles containing the respiratory syncytial virus F and G proteins. J. Virol. 85(1), 366–377 (2011).
  • Kim S, Jang JE, Yu JR, Chang J. Single mucosal immunization of recombinant adenovirus-based vaccine expressing F1 protein fragment induces protective mucosal immunity against respiratory syncytial virus infection. Vaccine 28(22), 3801–3808 (2010).
  • Chen M, Hu KF, Rozell B, Orvell C, Morein B, Liljeström P. Vaccination with recombinant alphavirus or immune-stimulating complex antigen against respiratory syncytial virus. J. Immunol. 169(6), 3208–3216 (2002).
  • Mok H, Lee S, Utley TJ et al. Venezuelan equine encephalitis virus replicon particles encoding respiratory syncytial virus surface glycoproteins induce protective mucosal responses in mice and cotton rats. J. Virol. 81(24), 13710–13722 (2007).
  • van Drunen Littel-van den Hurk S, Hannaman D. Electroporation for DNA immunization: clinical application. Expert Rev. Vaccines 9(5), 503–517 (2010).
  • Park EK, Soh BY, Jang YS, Park JH, Chung GH. Immune induction and modulation in mice following immunization with DNA encoding F protein of respiratory syncytial virus. Mol. Cells 12(1), 50–56 (2001).
  • Bembridge GP, Rodriguez N, Garcia-Beato R, Nicolson C, Melero JA, 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(Pt 10), 2519–2523 (2000).
  • Vaughan K, Rhodes GH, Gershwin LJ. DNA immunization against respiratory syncytial virus (RSV) in infant rhesus monkeys. Vaccine 23(22), 2928–2942 (2005).
  • De Gregorio E, D’Oro U, Wack A. Immunology of TLR-independent vaccine adjuvants. Curr. Opin. Immunol. 21(3), 339–345 (2009).
  • Prince GA, Denamur F, Deschamps M et al. Monophosphoryl lipid A adjuvant reverses a principal histologic parameter of formalin-inactivated respiratory syncytial virus vaccine-induced disease. Vaccine 19(15–16), 2048–2054 (2001).
  • Boukhvalova MS, Prince GA, Soroush L, Harrigan DC, Vogel SN, Blanco JC. The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease. Vaccine 24(23), 5027–5035 (2006).
  • Mapletoft JW, Latimer L, Babiuk LA, van Drunen Littel-van den Hurk S. 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. 17(1), 23–35 (2010).
  • Mapletoft JW, Oumouna M, Kovacs-Nolan J et al. Intranasal immunization of mice with a formalin-inactivated bovine respiratory syncytial virus vaccine co-formulated with CpG oligodeoxynucleotides and polyphosphazenes results in enhanced protection. J. Gen. Virol. 89(Pt 1), 250–260 (2008).
  • Oumouna M, Mapletoft JW, Karvonen BC, Babiuk LA, 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(4), 2024–2032 (2005).
  • Mapletoft JW, Oumouna M, Townsend HG, Gomis S, Babiuk LA, 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(2), 316–323 (2006).
  • Johnson TR, Rao S, Seder RA, Chen M, Graham BS. 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 27(23), 3045–3052 (2009).
  • Hancock GE, Heers KM, Smith JD, Scheuer CA, Ibraghimov AR, Pryharski KS. CpG containing oligodeoxynucleotides are potent adjuvants for parenteral vaccination with the fusion (F) protein of respiratory syncytial virus (RSV). Vaccine 19(32), 4874–4882 (2001).
  • Kovacs-Nolan J, Mapletoft JW, Lawman Z, Babiuk LA, van Drunen Littel-van den Hurk S. Formulation of bovine respiratory syncytial virus fusion protein with CpG oligodeoxynucleotide, cationic host defence peptide and polyphosphazene enhances humoral and cellular responses and induces a protective type 1 immune response in mice. J. Gen. Virol. 90(Pt 8), 1892–1905 (2009).
  • Kovacs-Nolan J, Latimer L, Landi A et al. The novel adjuvant combination of CpG ODN, indolicidin and polyphosphazene induces potent antibody- and cell-mediated immune responses in mice. Vaccine 27(14), 2055–2064 (2009).
  • Kovacs-Nolan J, Mapletoft JW, Latimer L, Babiuk LA, Hurk SD. CpG oligonucleotide, host defense peptide and polyphosphazene act synergistically, inducing long-lasting, balanced immune responses in cattle. Vaccine 27(14), 2048–2054 (2009).
  • Ioannou XP, Griebel P, Mena A et al. Safety of CpG oligodeoxynucleotides in veterinary species. Antisense Nucleic Acid Drug Dev. 13(3), 157–167 (2003).
  • Garlapati S, Eng NF, Wilson HL et al. PCPP (poly[di(carboxylatophenoxy)-phosphazene]) microparticles co-encapsulating ovalbumin and CpG oligo-deoxynucleotides are potent enhancers of antigen specific Th1 immune responses in mice. Vaccine 29(38), 6540–6548 (2010).
  • Garlapati S, Eng NF, Wilson HL et al. Immunization with PCEP microparticles containing pertussis toxoid, CpG ODN and a synthetic innate defense regulator peptide induces protective immunity against pertussis. Vaccine 28(52), 8306–8314 (2011).
  • Garlapati S, Garg R, Brownlie R et al. Enhanced immune responses and protection by vaccination with respiratory syncytial virus fusion protein formulated with CpG oligodeoxynucleotide and innate defense regulator peptide in polyphosphazene microparticles. Vaccine 30(35), 5206–5214 (2012).
  • Shafique M, Wilschut J, de Haan A. Induction of mucosal and systemic immunity against respiratory syncytial virus by inactivated virus supplemented with TLR9 and NOD2 ligands. Vaccine 30(3), 597–606 (2012).
  • Mottram PL, Leong D, Crimeen-Irwin B et al. Type 1 and 2 immunity following vaccination is influenced by nanoparticle size: formulation of a model vaccine for respiratory syncytial virus. Mol. Pharm. 4(1), 73–84 (2007).
  • Lindell DM, Morris SB, White MP et al. A novel inactivated intranasal respiratory syncytial virus vaccine promotes viral clearance without Th2 associated vaccine-enhanced disease. PLoS ONE 6(7), e21823 (2011).
  • 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 28(34), 5543–5550 (2010).
  • Habibi MS, Patel S, Openshaw P. Hot topics in the prevention of respiratory syncytial virus disease. Expert Rev. Vaccines 10(3), 291–293 (2011).

Patent

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.