Packaging and prefusion stabilization separately and additively increase the quantity and quality of respiratory syncytial virus (RSV)-neutralizing antibodies induced by an RSV fusion protein expressed by a parainfluenza virus vector

Journal of Virology

Volumn 90, Issue 21, 2016, Pages 10022-10038

  Liang, Bo ^a   Ngwuta, Joan O ^a   Herbert, Richard ^a   Swerczek, Joanna ^a   Dorward, David W ^b   Amaro Carambot, Emerito ^a   Mackow, Natalie ^a   Kabatova, Barbora ^a   Lingemann, Matthias ^a   Surman, Sonja ^a   Yang, Lijuan ^a   Chen, Man ^a   Moin, Syed M ^a   Kumar, Azad ^a   McLellan, Jason S ^a,c   Kwong, Peter D ^a   Graham, Barney S ^a   Schaap Nutt, Anne ^a   Collins, Peter L ^a   Munir, Shirin ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; VIRUS FUSION PROTEIN; VIRUS VECTOR; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DRUG PACKAGING; DRUG STABILITY; HAMSTER; HUMAN PARAINFLUENZA VIRUS 3; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; RHESUS MONKEY; VIRUS PARTICLE; ANIMAL; BOVINE; BOVINE PARAINFLUENZA VIRUS 3; CELL LINE; CHLOROCEBUS AETHIOPS; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RESPIROVIRUS INFECTION; VERO CELL LINE; VIROLOGY; VIRUS CAPSID; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CAPSID; CATTLE; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; GENETIC VECTORS; HUMANS; MACACA MULATTA; PARAINFLUENZA VIRUS 3, BOVINE; PARAINFLUENZA VIRUS 3, HUMAN; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; RESPIROVIRUS INFECTIONS; VERO CELLS; VIRAL FUSION PROTEINS; VIRUS REPLICATION;

EID: 84994048510     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01196-16     Document Type: Article

References (54)

1. 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 EA, 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.
2. Murphy BR, Prince GA, Collins PL, Van Wyke Coelingh K, Olmsted RA, Spriggs MK, Parrott RH, Kim HW, Brandt CD, Chanock RM. 1988. Current approaches to the development of vaccines effective against parainfluenza and respiratory syncytial viruses. Virus Res 11:1-15.
3. Klein MI, Coviello S, Bauer G, Benitez A, Serra ME, Schiatti MP, Delgado MF, Melendi GA, Novalli L, Pena HG, Karron RA, Kleeberger SR, Polack FP. 2006. The impact of infection with human metapneumovirus and other respiratory viruses in young infants and children at high risk for severe pulmonary disease. J Infect Dis 193:1544-1551. http://dx.doi.org/10.1086/503806.
4. Ottolini MG, Porter DD, Hemming VG, Prince GA. 2000. Enhanced pulmonary pathology in cotton rats upon challenge after immunization with inactivated parainfluenza virus 3 vaccines. Viral Immunol 13:231-236. http://dx.doi.org/10.1089/vim.2000.13.231.
5. Kim HW, Canchola JG, Brandt CD, Pyles G, Chanock RM, Jensen K, Parrott RH. 1969. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 89:422-434.
6. Wright P, Karron R, Belshe R, Shi J, Randolph V, Collins P, O'Shea A, Gruber W, Murphy B. 2007. The absence of enhanced disease with wild type respiratory syncytial virus infection occurring after receipt of live, attenuated, respiratory syncytial virus vaccines. Vaccine 25:7372-7378. http://dx.doi.org/10.1016/j.vaccine.2007.08.014.
7. Bernstein D, Malkin E, Abughali N, Falloon J, Yi T, Dubovsky F. 2012. Phase 1 study of the safety and immunogenicity of a live, attenuated respiratory syncytial virus and parainfluenza virus type 3 vaccine in seronegative children. Pediatr Infect Dis J 31:109-114. http://dx.doi.org/10.1097/INF.0b013e31823386f1.
8. Karron RA, Wright PF, Belshe RB, Thumar B, Casey R, Newman F, Polack FP, Randolph VB, Deatly A, Hackell J, Gruber W, Murphy BR, Collins PL. 2005. Identification of a recombinant live attenuated respiratory syncytial virus vaccine candidate that is highly attenuated in infants. J Infect Dis 191:1093-1104. http://dx.doi.org/10.1086/427813.
9. Englund JA, Karron RA, Cunningham CK, Larussa P, Melvin A, Yogev R, Handelsman E, Siberry GK, Thumar B, Schappell E, Bull CV, Chu HY, Schaap-Nutt A, Buchholz U, Collins PL, Schmidt AC, International Maternal Pediatric Adolescent AIDS Clinical Trials (IMPAACT) P1096 Study Group. 2013. Safety and infectivity of two doses of liveattenuated recombinant cold-passaged human parainfluenza type 3 virus vaccine rHPIV3cp45 in HPIV3-seronegative young children. Vaccine 31: 5706-5712. http://dx.doi.org/10.1016/j.vaccine.2013.09.046.
10. Karron RA, Luongo C, Thumar B, Loehr KM, Englund JA, Collins PL, Buchholz UJ. 2015. A gene deletion that up-regulates viral gene expression yields an attenuated RSV vaccine with improved antibody responses in children. Sci Transl Med 7:312ra175. http://dx.doi.org/10.1126/scitranslmed.aac8463.
11. Haller AA, Miller T, Mitiku M, Coelingh K. 2000. Expression of the surface glycoproteins of human parainfluenza virus type 3 by bovine parainfluenza virus type 3, a novel attenuated virus vaccine vector. J Virol 74:11626-11635. http://dx.doi.org/10.1128/JVI.74.24.11626-11635.2000.
12. Karron RA, Thumar B, Schappell E, Surman S, Murphy BR, Collins PL, Schmidt AC. 2012. Evaluation of two chimeric bovine-human parainfluenza virus type 3 vaccines in infants and young children. Vaccine 30:3975-3981. http://dx.doi.org/10.1016/j.vaccine.2011.12.022.
13. Schmidt AC, McAuliffe JM, Murphy BR, Collins PL. 2001. Recombinant bovine/human parainfluenza virus type 3 (B/HPIV3) expressing the respiratory syncytial virus (RSV) G and F proteins can be used to achieve simultaneous mucosal immunization against RSV and HPIV3. J Virol 75:4594-4603. http://dx.doi.org/10.1128/JVI.75.10.4594-4603.2001.
14. Schmidt AC, Wenzke DR, McAuliffe JM, St Claire M, Elkins WR, Murphy BR, Collins PL. 2002. Mucosal immunization of rhesus monkeys against respiratory syncytial virus subgroups A and B and human parainfluenza virus type 3 by using a live cDNA-derived vaccine based on a host range-attenuated bovine parainfluenza virus type 3 vector backbone. J Virol 76:1089-1099. http://dx.doi.org/10.1128/JVI.76.3.1089-1099.2002.
15. Yang C-F, Wang CK, Malkin E, Schickli JH, Shambaugh C, Zuo F, Galinski MS, Dubovsky F, Tang RS. 2013. Implication of respiratory syncytial virus (RSV) F transgene sequence heterogeneity observed in phase 1 evaluation of MEDI-534, a live attenuated parainfluenza type 3 vectored RSV vaccine. Vaccine 31:2822-2827. http://dx.doi.org/10.1016/j.vaccine.2013.04.006.
16. Shaikh FY, Cox RG, Lifland AW, Hotard AL, Williams JV, Moore ML, Santangelo PJ, Crowe JE, Jr. 2012. A critical phenylalanine residue in the respiratory syncytial virus fusion protein cytoplasmic tail mediates assembly of internal viral proteins into viral filaments and particles. mBio 3:e00270-11. http://dx.doi.org/10.1128/mBio.00270-11.
17. Harrison MS, Sakaguchi T, Schmitt AP. 2010. Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol 42:1416-1429. http://dx.doi.org/10.1016/j.biocel.2010.04.005.
18. Zokarkar A, Lamb RA. 2012. The paramyxovirus fusion protein C-terminal region: mutagenesis indicates an indivisible protein unit. J Virol 86:2600-2609. http://dx.doi.org/10.1128/JVI.06546-11.
19. Smith EC, Smith SE, Carter JR, Webb SR, Gibson KM, Hellman LM, Fried MG, Dutch RE. 2013. Trimeric transmembrane domain interactions in paramyxovirus fusion proteins: roles in protein folding, stability, and function. J Biol Chem 288:35726-35735. http://dx.doi.org/10.1074/jbc.M113.514554.
20. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, Zhou T, Graepel KW, Kumar A, Moin S, Boyington JC, Chuang GY, Soto C, Baxa U, Bakker AQ, Spits H, Beaumont T, Zheng Z, Xia N, Ko SY, Todd JP, 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.
21. 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.
22. Swanson KA, Settembre EC, Shaw CA, Dey AK, Rappuoli R, Mandl CW, Dormitzer PR, Carfi A. 2011. Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc Natl Acad Sci U S A 108: 9619-9624. http://dx.doi.org/10.1073/pnas.1106536108.
23. Kwakkenbos MJ, Diehl SA, Yasuda E, Bakker AQ, van Geelen CM, Lukens MV, van Bleek GM, Widjojoatmodjo MN, Bogers WM, Mei H, Radbruch A, Scheeren FA, Spits H, Beaumont T. 2010. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nat Med 16:123-128. http://dx.doi.org/10.1038/nm.2071.
24. Gilman MS, Moin SM, Mas V, Chen M, Patel NK, Kramer K, Zhu Q, Kabeche SC, Kumar A, Palomo C, Beaumont T, Baxa U, Ulbrandt ND, Melero JA, Graham BS, McLellan JS. 2015. Characterization of a prefusion-specific antibody that recognizes a quaternary, cleavage-dependent epitope on the RSV fusion glycoprotein. PLoS Pathog 11:e1005035. http://dx.doi.org/10.1371/journal.ppat.1005035.
25. Corti D, Bianchi S, Vanzetta F, Minola A, Perez L, Agatic G, Guarino B, Silacci C, Marcandalli J, Marsland BJ, Piralla A, Percivalle E, Sallusto F, Baldanti F, Lanzavecchia A. 2013. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature 501:439-443. http://dx.doi.org/10.1038/nature12442.
26. 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.
27. Ngwuta JO, Chen M, Modjarrad K, Joyce MG, Kanekiyo M, Kumar A, Yassine HM, Moin SM, Killikelly AM, Chuang GY, Druz A, Georgiev IS, Rundlet EJ, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Nason MC, Capella C, Peeples ME, Ledgerwood JE, McLellan JS, Kwong PD, Graham BS. 2015. Prefusion F-specific antibodies determine the magnitude of RSV neutralizing activity in human sera. Sci Transl Med 7:309ra162. http://dx.doi.org/10.1126/scitranslmed.aac4241.
28. Liang B, Munir S, Amaro-Carambot E, Surman S, Mackow N, Yang L, Buchholz UJ, Collins PL, Schaap-Nutt A. 2014. Chimeric bovine/human parainfluenza virus type 3 expressing respiratory syncytial virus (RSV) F glycoprotein: effect of insert position on expression, replication, immunogenicity, stability, and protection against RSV infection. J Virol 88: 4237-4250. http://dx.doi.org/10.1128/JVI.03481-13.
29. Liang B, Surman S, Amaro-Carambot E, Kabatova B, Mackow N, Lingemann M, Yang L, McLellan JS, Graham BS, Kwong PD, Schaap-Nutt A, Collins PL, Munir S. 2015. Enhanced neutralizing antibody response induced by respiratory syncytial virus prefusion F protein expressed by a vaccine candidate. J Virol 89:9499-9510. http://dx.doi.org/10.1128/JVI.01373-15.
30. Buchholz UJ, Finke S, Conzelmann K-K. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251-259.
31. Collins PL, Hill MG, Camargo E, Grosfeld H, Chanock RM, Murphy BR. 1995. Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5= proximal open reading frame of theM2mRNAin gene expression and provides a capability for vaccine development. Proc Natl Acad Sci U S A 92:11563-11567. http://dx.doi.org/10.1073/pnas.92.25.11563.
32. Collins PL. September 2004. Methods for producing self-replicating infectious RSV particles comprising recombinant RSV genomes or antigenomes and the N, P, L, and M2 proteins. US patent 6,790,449.
33. Whitehead SS, Juhasz K, Firestone CY, Collins PL, Murphy BR. 1998. Recombinant respiratory syncytial virus (RSV) bearing a set of mutations from cold-passaged RSV is attenuated in chimpanzees. J Virol 72:4467-4471.
34. Calain P, Roux L. 1993. The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67:4822-4830.
35. Kolakofsky D, Pelet T, Garcin D, Hausmann S, Curran J, Roux L. 1998. Paramyxovirus RNA synthesis and the requirement for hexamer genome length: the rule of six revisited. J Virol 72:891-899.
36. Luongo C, Winter CC, Collins PL, Buchholz UJ. 2012. Increased genetic and phenotypic stability of a promising live-attenuated respiratory syncytial virus vaccine candidate by reverse genetics. J Virol 86:10792-10804. http://dx.doi.org/10.1128/JVI.01227-12.
37. DiNapoli JM, Yang L, Suguitan A, Jr, Elankumaran S, Dorward DW, Murphy BR, Samal SK, Collins PL, Bukreyev A. 2007. Immunization of primates with a Newcastle disease virus-vectored vaccine via the respiratory tract induces a high titer of serum neutralizing antibodies against highly pathogenic avian influenza virus. J Virol 81:11560-11568. http://dx.doi.org/10.1128/JVI.00713-07.
38. Yoder SM, Zhu Y, Ikizler MR, Wright PF. 2004. Role of complement in neutralization of respiratory syncytial virus. J Med Virol 72:688-694. http://dx.doi.org/10.1002/jmv.20046.
39. Oomens AG, Megaw AG, Wertz GW. 2003. Infectivity of a human respiratory syncytial virus lacking the SH, G, and F proteins is efficiently mediated by the vesicular stomatitis virusGprotein. J Virol 77:3785-3798. http://dx.doi.org/10.1128/JVI.77.6.3785-3798.2003.
40. Bukreyev A, Yang L, Zaki SR, Shieh WJ, Rollin PE, Murphy BR, Collins PL, Sanchez A. 2006. A single intranasal inoculation with a paramyxovirus-vectored vaccine protects guinea pigs against a lethal-dose Ebola virus challenge. J Virol 80:2267-2279. http://dx.doi.org/10.1128/JVI.80.5.2267-2279.2006.
41. Veits J, Wiesner D, Fuchs W, Hoffmann B, Granzow H, Starick E, Mundt E, Schirrmeier H, Mebatsion T, Mettenleiter TC, Romer-Oberdorfer A. 2006. Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc Natl Acad Sci U S A 103:8197-8202. http://dx.doi.org/10.1073/pnas.0602461103.
42. Zimmer G, Bossow S, Kolesnikova L, Hinz M, Neubert WJ, Herrler G. 2005. A chimeric respiratory syncytial virus fusion protein functionally replaces the F and HN glycoproteins in recombinant Sendai virus. J Virol 79:10467-10477. http://dx.doi.org/10.1128/JVI.79.16.10467-10477.2005.
43. Park MS, Steel J, Garcia-Sastre A, Swayne D, Palese P. 2006. Engineered viral vaccine constructs with dual specificity: avian influenza and Newcastle disease. Proc Natl Acad Sci U S A 103:8203-8208. http://dx.doi.org/10.1073/pnas.0602566103.
44. Bachmann MF, Rohrer UH, Kundig TM, Burki K, Hengartner H, Zinkernagel RM. 1993. The influence of antigen organization on B cell responsiveness. Science 262:1448-1451. http://dx.doi.org/10.1126/science.8248784.
45. Denis J, Majeau N, Acosta-Ramirez E, Savard C, Bedard MC, Simard S, Lecours K, Bolduc M, Pare C, Willems B, Shoukry N, Tessier P, Lacasse P, Lamarre A, Lapointe R, Lopez Macias C, Leclerc D. 2007. Immunogenicity of papaya mosaic virus-like particles fused to a hepatitis C virus epitope: evidence for the critical function of multimerization. Virology 363:59-68. http://dx.doi.org/10.1016/j.virol.2007.01.011.
46. Bachmann MF, Zinkernagel RM. 1997. Neutralizing antiviral B cell responses. Annu Rev Immunol 15:235-270. http://dx.doi.org/10.1146/annurev.immunol.15.1.235.
47. Russell CJ, Hurwitz JL. 2016. Sendai virus as a backbone for vaccines against RSV and other human paramyxoviruses. Expert Rev Vaccines 15: 189-200. http://dx.doi.org/10.1586/14760584.2016.1114418.
48. Luongo C, Winter CC, Collins PL, Buchholz UJ. 2013. Respiratory syncytial virus modified by deletions of the NS2 gene and amino acid S1313 of the L polymerase protein is a temperature-sensitive, live-attenuated vaccine candidate that is phenotypically stable at physiological temperature. J Virol 87: 1985-1996. http://dx.doi.org/10.1128/JVI.02769-12.
49. Rostad CA, Stobart CC, Gilbert BE, Pickles RJ, Hotard AL, Meng J, Blanco JC, Moin SM, Graham BS, Piedra PA, Moore ML. 2016. A recombinant respiratory syncytial virus vaccine candidate attenuated by a low-fusion F protein is immunogenic and protective against challenge in cotton rats. J Virol 90:7508-7518. http://dx.doi.org/10.1128/JVI.00012-16.
50. Meng J, Lee S, Hotard AL, Moore ML. 2014. Refining the balance of attenuation and immunogenicity of respiratory syncytial virus by targeted codon deoptimization of virulence genes. mBio 5:e01704-14. http://dx.doi.org/10.1128/mBio.01704-14.
51. Le Nouen C, Brock LG, Luongo C, McCarty T, Yang L, Mehedi M, Wimmer E, Mueller S, Collins PL, Buchholz UJ, DiNapoli JM. 2014. Attenuation of human respiratory syncytial virus by genome-scale codonpair deoptimization. Proc Natl Acad SciUSA111:13169-13174. http://dx.doi.org/10.1073/pnas.1411290111.
52. Krarup A, Truan D, Furmanova-Hollenstein P, Bogaert L, Bouchier P, Bisschop IJ, Widjojoatmodjo MN, Zahn R, Schuitemaker H, McLellan JS, Langedijk JP. 2015. A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism. Nat Commun 6:8143. http://dx.doi.org/10.1038/ncomms9143.
53. Collins PL, Huang YT, Wertz GW. 1984. Nucleotide sequence of the gene encoding the fusion (F) glycoprotein of human respiratory syncytial virus. Proc Natl Acad Sci U S A 81:7683-7687. http://dx.doi.org/10.1073/pnas.81.24.7683.
54. Brock SC, Heck JM, McGraw PA, Crowe JE, Jr. 2005. The transmembrane domain of the respiratory syncytial virus F protein is an orientationindependent apical plasma membrane sorting sequence. J Virol 79: 12528-12535. http://dx.doi.org/10.1128/JVI.79.19.12528-12535.2005.