Modification of the respiratory syncytial virus f protein in virus- like particles impacts generation of B cell memory

Journal of Virology

Volumn 88, Issue 17, 2014, Pages 10165-10176

  Schmidt, Madelyn R ^a   McGinnes Cullen, Lori W ^a   Kenward, Sarah A ^a   Willems, Kristin N ^b   Woodland, Robert T ^a   Morrison, Trudy G ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b REGIS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F PROTEIN, HUMAN RESPIRATORY SYNCYTIAL VIRUS; HYBRID PROTEIN; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS ANTIBODY; VIRUS FUSION PROTEIN; VIRUS LIKE PARTICLE VACCINE;

ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; BLOOD; GENE VECTOR; GENETICS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; NEWCASTLE DISEASE VIRUS; SERODIAGNOSIS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; GENETIC VECTORS; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; MICE, INBRED BALB C; NEUTRALIZATION TESTS; NEWCASTLE DISEASE VIRUS; RECOMBINANT FUSION PROTEINS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VACCINES, SYNTHETIC; VACCINES, VIRUS-LIKE PARTICLE; VIRAL FUSION PROTEINS;

EID: 84921420479     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01250-14     Document Type: Article

References (52)

1. Karron RA. 2008. Respiratory syncytial virus and parainfluenza virus vaccines, p 1283. In Plotkin SA, Orenstein WA, Offit PA (ed), Vaccines, 5th ed. Saunders-Elsevier, Philadelphia, PA.
2. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O'Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simoes EAF, Rudan I, Weber MW, Campbell H. 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. http://dx.doi.org/10.1016/S0140-6736(10)60206-1.
3. Han LL, Alexander JP, Anderson LJ. 1999. Respiratory syncytial virus pneumonia among the elderly: an assessment of disease burden. J. Infect. Dis. 179:25-30. http://dx.doi.org/10.1086/314567.
4. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352:1749-1759. http://dx.doi.org/10.1056/NEJMoa043951.
5. Falsey AR, Walsh EE. 2000. Respiratory syncytial virus infection in adults. Clin. Microbiol. Rev. 13:371-384. http://dx.doi.org/10.1128/CMR.13.3.371-384.2000.
6. Raboni SM, Nogueira MB, Tsuchiya LR, Takahashi GA, Pereira LA, Pasquini R, Siqueira MM. 2003. Respiratory tract viral infections in bone marrow transplant patients. Transplantation 76:142-146. http://dx.doi.org/10.1097/01.TP.0000072012.26176.58.
7. Walsh EE, Falsey AR, Hennessey PA. 1999. Respiratory syncytial and other virus infections in persons with chronic cardiopulmonary disease. Am. J. Respir. Crit. Care Med. 160:791-795. http://dx.doi.org/10.1164/ajrccm.160.3.9901004.
8. Collins PL, Crowe JE. 2007. Respiratory syncytial virus and metapneumovirus, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
9. van Drunen Littel-van den Hurk S, Mapletoft JW, Arsic N, Kovacs-Nolan J. 2007. Immunopathology of RSV infection: prospects for developing vaccines without this complication. Rev. Med. Virol. 17:5-34. http://dx.doi.org/10.1002/rmv.518.
10. Openshaw PJ, Culley FJ, Olszewska W. 2002. Immunopathogenesis of vaccine-enhanced RSV disease. Vaccine 20(Suppl 1):S27-S31. http://dx.doi.org/10.1016/S0264-410X(01)00301-2.
11. Openshaw PJ, Tregoning JS. 2005. Immune responses and disease enhancement during respiratory syncytial virus infection. Clin. Microbiol. Rev. 18:541-555. http://dx.doi.org/10.1128/CMR.18.3.541-555.2005.
12. Power UF. 2008. Respiratory syncytial virus (RSV) vaccines-two steps back for one leap forward. J. Clin. Virol. 41:38-44. http://dx.doi.org/10.1016/j.jcv.2007.10.024.
13. Jardetzky TS, Lamb RA. 2004. A class act. Nature 427:307-308. http://dx.doi.org/10.1038/427307a.
14. Smith EC, Popa A, Chang A, Masante C, Dutch RE. 2009. Viral entry mechanisms: the increasing diversity of paramyxovirus entry. FEBS J. 276: 7217-7227. http://dx.doi.org/10.1111/j.1742-4658.2009.07401.x.
15. Lamb RA, Parks GD. 2007. Paramyxoviridae: the viruses and their replication, p 1450-1496. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Strauss SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
16. Yin H-S, Paterson RG, Wen X, Lamb RA, Jardetzky TS. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U. S. A. 102:9288-9293. http://dx.doi.org/10.1073/pnas.0503989102.
17. Yin H-S, Wen X, Paterson RG, Lamb RA, Jardetzky TS. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38-44. http://dx.doi.org/10.1038/nature04322.
18. McLellan JS, Yang Y, Graham BS, Kwong PD. 2011. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J. Virol. 85:7788-7796. http://dx.doi.org/10.1128/JVI.00555-11.
19. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340:1113-1117. http://dx.doi.org/10.1126/science.1234914.
20. Magro M, Mas V, Chappell K, Vazquez M, Cano O, Luque D, Terron MC, Melero JA, Palomo C. 2012. Neutralizing antibodies against the preactive form of respiratory syncytial virus fusion protein offer unique possibilities for clinical intervention. Proc. Natl. Acad. Sci. U. S. A. 109: 3089-3094. http://dx.doi.org/10.1073/pnas.1115941109.
21. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GBE, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, Zhou T, Graepel KW, Kumar A, Moin S, Boyington JC, Chuang G-Y, Soto C, Baxa U, Bakker AQ, Spits H, Beaumont T, Zheng Z, Xia N, Ko S-Y, Todd J-P, Rao S, Graham BS, Kwong PD. 2013. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342:592-598. http://dx.doi.org/10.1126/science.1243283.
22. Smith G, Raghunandan R, Wu Y, Liu Y, Massare M, Nathan M, Zhou B, Lu H, Boddapati S, Li J, Flyer D, Glenn G. 2012. Respiratory syncytial virus fusion glycoprotein expressed in insect cells form protein nanoparticles that induce protective immunity in cotton rats. PLoS One 7:e50852. http://dx.doi.org/10.1371/journal.pone.0050852.
23. Hall CB. 2001. Respiratory syncytial virus and parainfluenza virus. N. Engl. J. Med. 344:1917-1928. http://dx.doi.org/10.1056/NEJM200106213442507.
24. Schmidt MR, McGinnes LW, Kenward SA, Willems KN, Woodland RT, Morrison TG. 2012. Long term and memory immune responses in mice against Newcastle disease virus-like particles containing respiratory syncytial virus glycoprotein ectodomains. J. Virol. 86:11654-11662. http://dx.doi.org/10.1128/JVI.01510-12.
25. Murawski MR, McGinnes LW, Finberg RW, Kurt-Jones EA, Massare M, Smith G, Heaton PM, Fraire A, Morrison TG. 2010. Newcastle disease virus-like particles containing respiratory syncytial virusGprotein induced protection in BALB/c mice with no evidence of immunopathology. J. Virol. 84:1110-1123. http://dx.doi.org/10.1128/JVI.01709-09.
26. McGinnes LW, Gravel KA, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, Schmidt MR, Morrison TG. 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. http://dx.doi.org/10.1128/JVI.01861-10.
27. McGinnes LW, Pantua H, Laliberte JP, Gravel KA, Jain S, Morrison TG. 2010. Assembly and biological and immunological properties of Newcastle disease virus-like particles. J. Virol. 84:4513-4523. http://dx.doi.org/10.1128/JVI.01931-09.
28. Pantua HD, McGinnes LW, Peeples ME, Morrison TG. 2006. Requirements for the assembly and release of Newcastle disease virus-like particles. J. Virol. 80:11062-11073. http://dx.doi.org/10.1128/JVI.00726-06.
29. Laliberte JP, McGinnes LW, Peeples ME, Morrison TG. 2006. Integrity of membrane lipid rafts is necessary for the ordered assembly and release of infectious Newcastle disease virus particles. J. Virol. 80:10652-10662. http://dx.doi.org/10.1128/JVI.01183-06.
30. Beeler JA, van Wyke Coelingh K. 1989. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J. Virol. 63:2941-2950.
31. Dolganiuc V, McGinnes L, Luna EJ, Morrison TG. 2003. Role of the cytoplasmic domain of the Newcastle disease virus fusion protein in association with lipid rafts. J. Virol. 77:12968-12979. http://dx.doi.org/10.1128/JVI.77.24.12968-12979.2003.
32. Jain S, McGinnes LW, Morrison TG. 2007. Thiol/disulfide exchange is required for membrane fusion directed by the Newcastle disease virus fusion protein. J. Virol. 81:2328-2339. http://dx.doi.org/10.1128/JVI.01940-06.
33. Jain S, McGinnes LW, Morrison TG. 2008. Overexpression of thiol/disulfide isomerases enhances membrane fusion directed by Newcastle disease virus fusion protein. J. Virol. 82:12039-12048. http://dx.doi.org/10.1128/JVI.01406-08.
34. Laliberte JP, McGinnes LW, Morrison TG. 2007. Incorporation of functional HN-F glycoprotein containing complexes into Newcastle disease virus is dependent on cholesterol and membrane lipid raft integrity. J. Virol. 81:10636-10648. http://dx.doi.org/10.1128/JVI.01119-07.
35. Schmidt MR, Appel MC, Giassi LJ, Greiner DL, Shultz LD, Woodland RT. 2008. Human BLyS facilitates engraftment of human PBL derived B cells in immunodeficient mice. PLoS One 3:e3192. http://dx.doi.org/10.1371/journal.pone.0003192.
36. Murawski MR, Bowen GN, Cerny AM, Anderson LJ, Haynes LM, Tripp RA, Kurt-Jones EA, Finberg RW. 2009. Respiratory syncytial virus activates innate immunity through Toll-like receptor 2. J. Virol. 83:1492-1500. http://dx.doi.org/10.1128/JVI.00671-08.
37. Mok H, Lee S, Utley TJ, Shepherd BE, Polosukhin VV, Collier ML, Davis NL, Johnson RE, Crowe JE. 2007. Venezuelan equine encephalitis virus replicon particles encoding respiratory syncytial virus surface glycoproteins induce protective mucosal responses in mice and cotton rats. J. Virol. 81:13710-13722. http://dx.doi.org/10.1128/JVI.01351-07.
38. Collins PL, Graham BS. 2008. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 82:2040-2055. http://dx.doi.org/10.1128/JVI.01625-07.
39. Delgado MF, Coviello S, Monsalvo AC, Melendi GA, Hernandez JZ, Batalle JP, Diaz L, Trento A, Chang H-Y, Mitzner W, Ravetch J, Melero JA, Irusta PM, Polack FP. 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. http://dx.doi.org/10.1038/nm.1894.
40. Markine-Goriaynoff D, Coutelier J-P. 2002. Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. J. Virol. 76:432-435. http://dx.doi.org/10.1128/JVI.76.1.432-435.2002.
41. Shlomchik MJ, Weisel F. 2012. Germinal centers. Immunol. Rev. 247:5-10. http://dx.doi.org/10.1111/j.1600-065X.2012.01125.x.
42. Shlomchik MJ, Weisel F. 2012. Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 247:52-63. http://dx.doi.org/10.1111/j.1600-065X.2012.01124.x.
43. Bortnick A, Chernova I, Quinn WJ, Mugnier M, Cancro MP, Allman D. 2012. Long-lived bone marrow plasma cells are induced early in response to T cell-independent or T cell-dependent antigens. J. Immunol. 188: 5389-5396. http://dx.doi.org/10.4049/jimmunol.1102808.
44. Pulendran B, Ahmed R. 2011. Immunological mechanisms of vaccination. Nat. Immunol. 12:509-517. http://dx.doi.org/10.1038/ni.2039.
45. Kaji T, Ishige A, Hikida M, Taka J, Hijikata A, Kubo M, Nagashima T, Takahashi Y, Kurosaki T, Okada M, Ohara O, Rajewsky K, Takemori T. 2012. Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J. Exp. Med. 209:2079-2097. http://dx.doi.org/10.1084/jem.20120127.
46. Hebeis BJ, Klenovsek K, Rohwer P, Ritter U, Schneider A, Mach M, Winkler TH. 2004. Activation of virus-specific memory B Cells in the absence of T cell help. J. Exp. Med. 199:593-602. http://dx.doi.org/10.1084/jem.20030091.
47. Klenovsek K, Weisel F, Schneider A, Appelt U, Jonjic S, Messerle M, Bradel-Tretheway B, Winkler TH, Mach M. 2007. Protection from CMV infection in immunodeficient hosts by adoptive transfer of memory B cells. Blood 110:3472-3479. http://dx.doi.org/10.1182/blood-2007-06-095414.
48. Leclerc C, Sedlik C, Lo-Man R, Charlot B, Rojas M, Dériaud E. 1995. Stimulation of a memory B cell response does not require primed helper T cells. Eur. J. Immunol. 25:2533-2538. http://dx.doi.org/10.1002/eji.1830250919.
49. MacLeod MKL, Clambey ET, Kappler JW, Marrack P. 2009. CD4 memory T cells: what are they and what can they do? Semin. Immunol. 21:53-61. http://dx.doi.org/10.1016/j.smim.2009.02.006.
50. Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, Villinger F, Murthy N, Steel J, Jacob J, Hogan RJ, Garcia-Sastre A, Compans R, Pulendran B. 2011. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470:543-547. http://dx.doi.org/10.1038/nature09737.
51. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, Tripp RA, Walsh EE, Freeman MW, Golenbock DT, Anderson LJ, Finberg RW. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401. http://dx.doi.org/10.1038/80833.
52. Ballesteros-Tato A, Randall TD. 2014. Priming of T follicular helper cells by dendritic cells. Immunol. Cell Biol. 92:22-27. http://dx.doi.org/10.1038/icb.2013.62.