Mammalian cell-derived respiratory syncytial virus-like particles protect the lower as well as the upper respiratory tract

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Walpita, Pramila ^a   Johns, Lisa M ^a   Tandon, Ravi ^a   Moore, Martin L ^b,c  

^a UNIVERSITY OF HAWAII   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GLYCOPROTEIN; GLYCOPROTEIN F; IMMUNOGLOBULIN G; MATRIX PROTEIN; MATRIX PROTEIN M; RESPIRATORY SYNCYTIAL VIRUS VACCINE; THROMBOSPONDIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NEUTRALIZING ANTIBODY; TLR4 PROTEIN, RAT; TOLL LIKE RECEPTOR 4; VIRAL PROTEIN;

ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RESPONSE; DRUG EFFICACY; DRUG SAFETY; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMORAL IMMUNITY; IMMUNOREACTIVITY; IN VITRO STUDY; MACROPHAGE; MAMMAL CELL; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; UPREGULATION; VACCINATION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; CHEMISTRY; HEK293 CELL LINE; IMMUNOLOGY; LUNG; METABOLISM; NOSE; RAT; TH1 CELL; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; CYTOKINES; HEK293 CELLS; HUMANS; IMMUNITY, HUMORAL; LUNG; NOSE; RATS; RESPIRATORY SYNCYTIAL VIRUSES; TH1 CELLS; TOLL-LIKE RECEPTOR 4; UP-REGULATION; VACCINATION; VIRAL PROTEINS;

EID: 84940399188     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130755     Document Type: Article

References (68)

1. Feldman SA, Hendry RM, Beeler JA (1999) Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J Virol 73: 6610-6617. PMID: 10400758
2. Tayyari F, Marchant D, Moraes TJ, Duan W, Mastrangelo P, Hegele RG (2011) Identification of nucleolin as a cellular receptor for human respiratory syncytial virus. Nat Med 17: 1132-1135. doi: 10.1038/nm.2444 PMID: 21841784
3. Hendry RM, Talis AL, Godfrey E, Anderson LJ, Fernie BF, McIntosh K (1986) Concurrent circulation of antigenically distinct strains of respiratory syncytial virus during community outbreaks. J Infect Dis 153:291-297. PMID: 2418126
4. Graham BS (2011) Biological challenges and technological opportunities for respiratory syncytial virus vaccine development. Immunological Reviews 239: 149-166. doi: 10.1111/j.1600-065X.2010.00972.x PMID: 21198670
5. Anderson R, Huang Y, Langley JM (2010) Prospects for defined epitope vaccines for respiratory syncytial virus. Future Microbiology 5: 585-602. doi: 10.2217/fmb.10.22 PMID: 20353300
6. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, et al. (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375: 1545-1555. doi: 10.1016/S0140-6736(10)60206-1 PMID: 20399493
7. Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, Staat MA, et al. (2009) The burden of respiratory syncytial virus infection in young children. N Engl J Med 360: 588-598. doi: 10.1056/NEJMoa0804877 PMID: 19196675
8. Falsey AR, Walsh EE (2000) Respiratory syncytial virus infection in adults. Clinical Microbiology Reviews 13: 371-+. PMID: 10885982
9. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE (2005) Respiratory syncytial virus infection in elderly and high-risk adults. New England Journal of Medicine 352: 1749-1759. PMID: 15858184
10. Sandritter T (1999) Palivizumab for respiratory syncytial virus prophylaxis. Journal of pediatric health care: official publication of National Association of Pediatric Nurse Associates & Practitioners 13: 191-195; quiz 196-197.
11. Collins PL, Whitehead SS, Bukreyev A, Fearns R, Teng MN, Juhasz K, et al. (1999) Rational design of live-attenuated recombinant vaccine virus for human respiratory syncytial virus by reverse genetics. Advances in Virus Research, Vol 54 54: 423-451.
12. Piedra PA, Cron SG, Jewell A, Hamblett N, McBride R, Palacio MA, et al. (2003) Immunogenicity of a new purified fusion protein vaccine to respiratory syncytial virus: a multi-center trial in children with cystic fibrosis. Vaccine 21: 2448-2460. PMID: 12744878
13. Borchers AT, Chang C, Gershwin ME, Gershwin LJ (2013) Respiratory Syncytial Virus-A Comprehensive Review. Clin Rev Allergy Immunol.
14. Schmidt AC (2011) Progress in respiratory virus vaccine development. Semin Respir Crit Care Med 32: 527-540. doi: 10.1055/s-0031-1283289 PMID: 21858754
15. Johnson TR, Rangel D, Graham BS, Brough DE, Gall JG (2014) Genetic vaccine for respiratory syncytial virus provides protection without disease potentiation. Mol Ther 22: 196-205. doi: 10.1038/mt.2013.142 PMID: 23752342
16. Kamphuis T, Stegmann T, Meijerhof T, Wilschut J, de Haan A (2013) A virosomal respiratory syncytial virus vaccine adjuvanted with monophosphoryl lipid A provides protection against viral challenge without priming for enhanced disease in cotton rats. Influenza Other Respir Viruses 7: 1227-1236. doi: 10.1111/irv.12112 PMID: 23575113
17. Shafique M, Meijerhof T, Wilschut J, de Haan A (2013) Evaluation of an intranasal virosomal vaccine against respiratory syncytial virus in mice: effect of TLR2 and NOD2 ligands on induction of systemic and mucosal immune responses. PLoS One 8: e61287. doi: 10.1371/journal.pone.0061287 PMID: 23593453
18. Jorquera PA, Choi Y, Oakley KE, Powell TJ, Boyd JG, Palath N, et al. (2013) Nanoparticle vaccines encompassing the respiratory syncytial virus (RSV) G protein CX3C chemokine motif induce robust immunity protecting from challenge and disease. PLoS One 8: e74905. doi: 10.1371/journal.pone.0074905 PMID: 24040360
19. Stone JW, Thornburg NJ, Blum DL, Kuhn SJ, Wright DW, Crowe JE Jr (2013) Gold nanorod vaccine for respiratory syncytial virus. Nanotechnology 24: 295102. doi: 10.1088/0957-4484/24/29/295102 PMID: 23799651
20. Quan FS, Kim Y, Lee S, Yi H, Kang SM, Bozja J, et al. (2011) Viruslike particle vaccine induces protection against respiratory syncytial virus infection in mice. J Infect Dis 204: 987-995. doi: 10.1093/infdis/jir474 PMID: 21881112
21. Murawski MR, McGinnes LW, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, et al. (2010) New-castle Disease Virus-Like Particles Containing Respiratory Syncytial Virus G Protein Induced Protection in BALB/c Mice, with No Evidence of Immunopathology. Journal of Virology 84: 1110-1123. doi: 10.1128/JVI.01709-09 PMID: 19889768
22. McGinnes LW, Gravel KA, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, et al. (2011) Assembly and immunological properties of Newcastle disease virus-like particles containing the respiratory syncytial virus F and G proteins. J Virol 85: 366-377. doi: 10.1128/JVI.01861-10 PMID: 20980510
23. Singleton R, Etchart N, Hou S, Hyland L (2003) 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: 11303-11311. PMID: 14557616
24. Oshansky CM, Zhang W, Moore E, Tripp RA (2009) The host response and molecular pathogenesis associated with respiratory syncytial virus infection. Future Microbiol 4: 279-297. doi: 10.2217/fmb.09.1 PMID: 19327115
25. Kim HW, Canchola JG, Brandt CD, Pyles G, Chanock RM, Jensen K, et al. (1969) Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 89: 422-434. PMID: 4305198
26. Kapikian AZ, Mitchell RH, Chanock RM, Shvedoff RA, Stewart CE (1969) 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: 405-421. PMID: 4305197
27. Collins PL, Crowe JE Jr (2007) Respiratory syncytial virus and metapneumovirus. Fields Virology. 5 ed. Philadelphia, PA: Lippincott, Williams and Wilkins.
28. Murphy BR, Prince GA, Walsh EE, Kim HW, Parrott RH, Hemming VG, et al. (1986) Dissociation between serum neutralizing and glycoprotein antibody responses of infants and children who received inactivated respiratory syncytial virus vaccine. J Clin Microbiol 24: 197-202. PMID: 3755730
29. Graham BS, Henderson GS, Tang YW, Lu X, Neuzil KM, Colley DG (1993) Priming immunization determines T helper cytokine mRNA expression patterns in lungs of mice challenged with respiratory syncytial virus. J Immunol 151: 2032-2040. PMID: 8345194
30. Waris ME, Tsou C, Erdman DD, Zaki SR, Anderson LJ (1996) 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. Journal of Virology 70: 2852-2860. PMID: 8627759
31. Connors M, Giese NA, Kulkarni AB, Firestone CY, Morse HC 3rd, Murphy BR (1994) 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: 5321-5325. PMID: 8035532
32. Connors M, Collins PL, Firestone CY, Sotnikov AV, Waitze A, Davis AR, et al. (1992) Cotton rats previously immunized with a chimeric RSV FG glycoprotein develop enhanced pulmonary pathology when infected with RSV, a phenomenon not encountered following immunization with vaccinia - RSV recombinants or RSV. Vaccine 10: 475-484. PMID: 1609551
33. Murphy BR, Sotnikov AV, Lawrence LA, Banks SM, Prince GA (1990) Enhanced pulmonary histopathology is observed in cotton rats immunized with formalin-inactivated respiratory syncytial virus (RSV) or purified F glycoprotein and challenged with RSV 3-6 months after immunization. Vaccine 8: 497-502. PMID: 2251875
34. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995. PMID: 15454922
35. Delgado MF, Coviello S, Monsalvo AC, Melendi GA, Hernandez JZ, Batalle JP, et al. (2009) Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat Med 15: 34-41. doi: 10.1038/nm.1894 PMID: 19079256
36. Boukhvalova MS, Prince GA, Soroush L, Harrigan DC, Vogel SN, Blanco JC (2006) The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease. Vaccine 24: 5027-5035. PMID: 16675071
37. Prince GA, Mond JJ, Porter DD, Yim KC, Lan SJ, Klinman DM (2003) Immunoprotective activity and safety of a respiratory syncytial virus vaccine: mucosal delivery of fusion glycoprotein with a CpG oligodeoxynucleotide adjuvant. J Virol 77: 13156-13160. PMID: 14645572
38. Shafique M, Wilschut J, de Haan A (2012) Induction of mucosal and systemic immunity against respiratory syncytial virus by inactivated virus supplemented with TLR9 and NOD2 ligands. Vaccine 30: 597-606. doi: 10.1016/j.vaccine.2011.11.054 PMID: 22120195
39. Coffman RL, Sher A, Seder RA (2010) Vaccine adjuvants: putting innate immunity to work. Immunity 33: 492-503. doi: 10.1016/j.immuni.2010.10.002 PMID: 21029960
40. Casella CR, Mitchell TC (2008) Putting endotoxin to work for us: Monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cellular and Molecular Life Sciences 65: 3231-3240. doi: 10.1007/s00018-008-8228-6 PMID: 18668203
41. Awate S, Babiuk LA, Mutwiri G (2013) Mechanisms of action of adjuvants. Front Immunol 4: 114. doi: 10.3389/fimmu.2013.00114 PMID: 23720661
42. Liu F, Wu X, Li L, Liu Z, Wang Z (2013) Use of baculovirus expression system for generation of virus-like particles: successes and challenges. Protein Expr Purif 90: 104-116. doi: 10.1016/j.pep.2013.05.009 PMID: 23742819
43. Didierlaurent AM, Morel S, Lockman L, Giannini SL, Bisteau M, Carlsen H, et al. (2009) AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol 183: 6186-6197. doi: 10.4049/jimmunol.0901474 PMID: 19864596
44. Garcon N, Wettendorff M, Van Mechelen M (2011) Role of AS04 in human papillomavirus vaccine: mode of action and clinical profile. Expert Opinion on Biological Therapy 11: 667-677. doi: 10.1517/14712598.2011.573624 PMID: 21457083
45. Stokes KL, Currier MG, Sakamoto K, Lee S, Collins PL, Plemper RK, et al. (2013) The respiratory syncytial virus fusion protein and neutrophils mediate the airway mucin response to pathogenic respiratory syncytial virus infection. J Virol 87: 10070-10082. doi: 10.1128/JVI.01347-13 PMID: 23843644
46. Walpita P, Barr J, Sherman M, Basler CF, Wang L (2011) Vaccine potential of Nipah virus-like particles. PLoS One 6: e18437. doi: 10.1371/journal.pone.0018437 PMID: 21494680
47. Schmitt AP, Leser GP, Waning DL, Lamb RA (2002) Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J Virol 76: 3952-3964. PMID: 11907235
48. Piedra PA, Wyde PR, Castleman WL, Ambrose MW, Jewell AM, Speelman DJ, et al. (1993) Enhanced pulmonary pathology associated with the use of formalin-inactivated respiratory syncytial virus vaccine in cotton rats is not a unique viral phenomenon. Vaccine 11: 1415-1423. PMID: 7508665
49. Crameri G, Wang LF, Morrissy C, White J, Eaton BT (2002) A rapid immune plaque assay for the detection of Hendra and Nipah viruses and anti-virus antibodies. J Virol Methods 99: 41-51. PMID: 11684302
50. Rixon HW, Brown C, Brown G, Sugrue RJ (2002) Multiple glycosylated forms of the respiratory syncytial virus fusion protein are expressed in virus-infected cells. J Gen Virol 83: 61-66. PMID: 11752701
51. Cheon IS, Shim BS, Park SM, Choi Y, Jang JE, Jung DI, et al. (2014) Development of safe and effective RSV Vaccine by modified CD4 epitope in G protein core fragment (Gcf). PLoS One 9: e94269. doi: 10.1371/journal.pone.0094269 PMID: 24736750
52. Waris ME, Tsou C, Erdman DD, Zaki SR, Anderson LJ (1996) 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 70: 2852-2860. PMID: 8627759
53. Haynes LM, Moore DD, Kurt-Jones EA, Finberg RW, Anderson LJ, Tripp RA (2001) Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 75: 10730-10737. PMID: 11602714
54. Murawski MR, Bowen GN, Cerny AM, Anderson LJ, Haynes LM, Tripp RA, et al. (2009) Respiratory syncytial virus activates innate immunity through Toll-like receptor 2. J Virol 83: 1492-1500. doi: 10.1128/JVI.00671-08 PMID: 19019963
55. Jensen S, Thomsen AR (2012) Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J Virol 86: 2900-2910. doi: 10.1128/JVI.05738-11 PMID: 22258243
56. Nish S, Medzhitov R (2011) Host defense pathways: role of redundancy and compensation in infectious disease phenotypes. Immunity 34: 629-636. doi: 10.1016/j.immuni.2011.05.009 PMID: 21616433
57. Luchsinger V, Piedra PA, Ruiz M, Zunino E, Martinez MA, Machado C, et al. (2012) Role of neutralizing antibodies in adults with community-acquired pneumonia by respiratory syncytial virus. Clin Infect Dis 54: 905-912. doi: 10.1093/cid/cir955 PMID: 22238168
58. Plotkin SA (2010) Correlates of protection induced by vaccination. Clin Vaccine Immunol 17: 1055-1065. doi: 10.1128/CVI.00131-10 PMID: 20463105
59. Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO (2003) Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. American Journal of Respiratory and Critical Care Medicine 168: 633-639. PMID: 12773328
60. Neuzil KM, Tang YW, Graham BS (1996) Protective Role of TNF-alpha in respiratory syncytial virus infection in vitro and in vivo. Am J Med Sci 311: 201-204. PMID: 8615393
61. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, Tripp RA, et al. (2000) Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nature Immunology 1: 398-401. PMID: 11062499
62. Heydenreich B, Bellinghausen I, Lund L, Henmar H, Lund G, Adler Wurtzen P, et al. (2014) Adjuvant effects of aluminium hydroxide-adsorbed allergens and allergoids-differences in vivo and in vitro. Clin Exp Immunol 176: 310-319. doi: 10.1111/cei.12294 PMID: 24528247
63. Garcon N, Morel S, Didierlaurent A, Descamps D, Wettendorff M, Van Mechelen M (2011) Development of an AS04-adjuvanted HPV vaccine with the adjuvant system approach. BioDrugs 25: 217-226. doi: 10.2165/11591760-000000000-00000 PMID: 21815697
64. Kamphuis T, Meijerhof T, Stegmann T, Lederhofer J, Wilschut J, de Haan A (2012) Immunogenicity and Protective Capacity of a Virosomal Respiratory Syncytial Virus Vaccine Adjuvanted with Monophosphoryl Lipid A in Mice. Plos One 7.
65. Blanco JCG, Boukhvalova MS, Shirey KA, Prince GA, Vogel SN (2010) New insights for development of a safe and protective RSV vaccine. Human Vaccines 6: 482-492. PMID: 20671419
66. Wright PF, Karron RA, Belshe RB, Thompson J, Crowe JE, Boyce TG, et al. (2000) Evaluation of a live, cold-passaged, temperature-sensitive, respiratory syncytial virus vaccine candidate in infancy. Journal of Infectious Diseases 182: 1331-1342. PMID: 11010838
67. Teng MN, Whitehead SS, Bermingham A, St Claire M, Elkins WR, Murphy BR, et al. (2000) Recombinant respiratory syncytial virus that does not express the NS1 or M2-2 protein is highly attenuated and immunogenic in chimpanzees. J Virol 74: 9317-9321. PMID: 10982380
68. Chackerian B (2007) Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 6: 381-390.