1,745
Views
30
CrossRef citations to date
0
Altmetric
Research Papers

Rotavirus capsid VP6 protein acts as an adjuvant in vivo for norovirus virus-like particles in a combination vaccine

, , , &
Pages 740-748 | Received 07 Jul 2015, Accepted 21 Sep 2015, Published online: 05 May 2016

References

  • Roldao A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. Virus-like particles in vaccine development. Expert Rev Vaccines 2010; 9:1149-76; PMID:20923267; http://dx.doi.org/10.1586/erv.10.115
  • Pushko P, Pumpens P, Grens E. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology 2013; 56:141-65; PMID:23594863; http://dx.doi.org/10.1159/000346773
  • Lavelle L, Gingery M, Phillips M, Gelbart WM, Knobler CM, Cadena-Nava RD, Vega-Acosta JR, Pinedo-Torres LA, Ruiz-Garcia J. Phase diagram of self-assembled viral capsid protein polymorphs. J Phys Chem B 2009; 113:3813-9PMID:19673134; http://dx.doi.org/10.1021/jp8079765
  • Ghosh MK, Deriaud E, Saron MF, Lo-Man R, Henry T, Jiao X, Roy P, Leclerc C. Induction of protective antiviral cytotoxic T cells by a tubular structure capable of carrying large foreign sequences. Vaccine 2002; 20:1369-77; PMID:11818155; http://dx.doi.org/10.1016/S0264-410X(01)00467-4
  • Prasad BV, Wang GJ, Clerx JP, Chiu W. Three-dimensional structure of rotavirus. J Mol Biol 1988; 199:269-75; http://dx.doi.org/10.1016/0022-2836(88)90313-0
  • Estes MK, Crawford SE, Penaranda ME, Petrie BL, Burns JW, Chan WK, Ericson B, Smith GE, Summers MD. Synthesis and immunogenicity of the rotavirus major capsid antigen using a baculovirus expression system. J Virol 1987; 61:1488-94; PMID:3033276
  • Bugli F, Caprettini V, Cacaci M, Martini C, Paroni Sterbini F, Torelli R, Della Longa S, Papi M, Palmieri V, Giardina B, et al. Synthesis and characterization of different immunogenic viral nanoconstructs from rotavirus VP6 inner capsid protein. Int J Nanomedicine 2014; 9:2727-39; PMID:24936129
  • Li T, Lin H, Zhang Y, Li M, Wang D, Che Y, Zhu Y, Li S, Zhang J, Ge S, et al. Improved characteristics and protective efficacy in an animal model of E. coli-derived recombinant double-layered rotavirus virus-like particles. Vaccine 2014; 32:1921-31; PMID:24530406; http://dx.doi.org/10.1016/j.vaccine.2014.01.093
  • Lepault J, Petitpas I, Erk I, Navaza J, Bigot D, Dona M, Vachette P, Cohen J, Rey FA. Structural polymorphism of the major capsid protein of rotavirus. EMBO J 2001; 20:1498-507; PMID:11285214; http://dx.doi.org/10.1093/emboj/20.7.1498
  • Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008; 38:1404-13; PMID:18389478; http://dx.doi.org/10.1002/eji.200737984
  • Xiang SD, Scholzen A, Minigo G, David C, Apostolopoulos V, Mottram PL, Plebanski M. Pathogen recognition and development of particulate vaccines: Does size matter? Methods 2006; 40:1-9; http://dx.doi.org/10.1016/j.ymeth.2006.05.016
  • Hubbell JA, Thomas SN, Swartz MA. Materials engineering for immunomodulation. Nature 2009; 462:449-60; PMID:19940915; http://dx.doi.org/10.1038/nature08604
  • Cubas R, Zhang S, Kwon S, Sevick-Muraca EM, Li M, Chen C, Yao Q. Virus-like particle (VLP) lymphatic trafficking and immune response generation after immunization by different routes. J Immunother 2009; 32:118-28; PMID:19238010; http://dx.doi.org/10.1097/CJI.0b013e31818f13c4
  • Svensson L, Sheshberadaran H, Vene S, Norrby E, Grandien M, Wadell G. Serum antibody responses to individual viral polypeptides in human rotavirus infections. J Gen Virol 1987; 68 (Pt 3):643-51; PMID:3029295; http://dx.doi.org/10.1099/0022-1317-68-3-643
  • Ward RL, McNeal MM. VP6: A candidate rotavirus vaccine. J Infect Dis 2010; 202 Suppl:S101-7; PMID:20684688; http://dx.doi.org/10.1086/653556
  • Ishida S, Feng N, Tang B, Gilbert JM, Greenberg HB. Quantification of systemic and local immune responses to individual rotavirus proteins during rotavirus infection in mice. J Clin Microbiol 1996; 34:1694-700; PMID:8784572
  • Corthesy B, Benureau Y, Perrier C, Fourgeux C, Parez N, Greenberg H, Schwartz-Cornil I. Rotavirus anti-VP6 secretory immunoglobulin A contributes to protection via intracellular neutralization but not via immune exclusion. J Virol 2006; 80:10692-9; http://dx.doi.org/10.1128/JVI.00927-06
  • Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, Saif L, Surrey T, Parreno V. Llama-derived single-chain antibody fragments directed to rotavirus VP6 protein possess broad neutralizing activity in vitro and confer protection against diarrhea in mice. J Virol 2008; 82:9753-64; http://dx.doi.org/10.1128/JVI.00436-08
  • Aiyegbo MS, Sapparapu G, Spiller BW, Eli IM, Williams DR, Kim R, Lee DE, Liu T, Li S, Woods VL, Jr, et al. Human rotavirus VP6-specific antibodies mediate intracellular neutralization by binding to a quaternary structure in the transcriptional pore. PLoS One 2013; 8:e61101; http://dx.doi.org/10.1371/journal.pone.0061101
  • Lappalainen S, Pastor AR, Tamminen K, Lopez-Guerrero V, Esquivel-Guadarrama F, Palomares LA, Vesikari T, Blazevic V. Immune responses elicited against rotavirus middle layer protein VP6 inhibit viral replication in vitro and in vivo. Hum Vaccin Immunother 2014; 10:2039-47; PMID:25424814; http://dx.doi.org/10.4161/hv.28858
  • Burns JW, Siadat-Pajouh M, Krishnaney AA, Greenberg HB. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science 1996; 272:104-7; PMID:8600516; http://dx.doi.org/10.1126/science.272.5258.104
  • Feng N, Lawton JA, Gilbert J, Kuklin N, Vo P, Prasad BV, Greenberg HB. Inhibition of rotavirus replication by a non-neutralizing, rotavirus VP6-specific IgA mAb. J Clin Invest 2002; 109:1203-13; PMID:11994409; http://dx.doi.org/10.1172/JCI14397
  • Patel NC, Hertel PM, Estes MK, de la Morena M, Petru AM, Noroski LM, Revell PA, Hanson IC, Paul ME, Rosenblatt HM, et al. Vaccine-acquired rotavirus in infants with severe combined immunodeficiency. N Engl J Med 2010; 362:314-9; PMID:20107217; http://dx.doi.org/10.1056/NEJMoa0904485
  • Weintraub ES, Baggs J, Duffy J, Vellozzi C, Belongia EA, Irving S, Klein NP, Glanz JM, Jacobsen SJ, Naleway A, et al. Risk of intussusception after monovalent rotavirus vaccination. N Engl J Med 2014; 370:513-9; http://dx.doi.org/10.1056/NEJMoa1311738
  • Hemming M, Vesikari T. Vaccine-derived human-bovine double reassortant rotavirus in infants with acute gastroenteritis. Pediatr Infect Dis J 2012; 31:992-4; http://dx.doi.org/10.1097/INF.0b013e31825d611e
  • Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, et al. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 2006; 354:23-33; PMID:16394299; http://dx.doi.org/10.1056/NEJMoa052664
  • Murphy TV, Gargiullo PM, Massoudi MS, Nelson DB, Jumaan AO, Okoro CA, Zanardi LR, Setia S, Fair E, LeBaron CW, et al. Intussusception among infants given an oral rotavirus vaccine. N Engl J Med 2001; 344:564-72; PMID:11207352; http://dx.doi.org/10.1056/NEJM200102223440804
  • Blazevic V, Lappalainen S, Nurminen K, Huhti L, Vesikari T. Norovirus VLPs and rotavirus VP6 protein as combined vaccine for childhood gastroenteritis. Vaccine 2011; 29:8126-33; PMID:21854823; http://dx.doi.org/10.1016/j.vaccine.2011.08.026
  • Tamminen K, Lappalainen S, Huhti L, Vesikari T, Blazevic V. Trivalent combination vaccine induces broad heterologous immune responses to norovirus and rotavirus in mice. PLoS One 2013; 8:e70409; http://dx.doi.org/10.1371/journal.pone.0070409
  • Glass RI, Parashar UD, Estes MK. Norovirus gastroenteritis. N Engl J Med 2009; 361:1776-85; PMID:19864676; http://dx.doi.org/10.1056/NEJMra0804575
  • Kroneman A, Vega E, Vennema H, Vinje J, White PA, Hansman G, Green K, Martella V, Katayama K, Koopmans M. Proposal for a unified norovirus nomenclature and genotyping Arch Virol 2013; 158:2059-68; PMID:23615870; http://dx.doi.org/10.1007/s00705-013-1708-5
  • Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinje J. Genotypic and epidemiologic trends of norovirus outbreaks in the united states, 2009 to 2013. J Clin Microbiol 2014; 52:147-55; http://dx.doi.org/10.1128/JCM.02680-13
  • Lappalainen S, Pastor AR, Malm M, Lopez-Guerrero V, Esquivel-Guadarrama F, Palomares LA, Vesikari T, Blazevic V. Protection against live rotavirus challenge in mice induced by parenteral and mucosal delivery of VP6 subunit rotavirus vaccine. Arch Virol 2015; 160:2075-8; PMID:26016444.
  • Redmond MJ, Ohmann HB, Hughes HP, Sabara M, Frenchick PJ, Poku SK, Ijaz MK, Parker MD, Laarveld B, Babiuk LA. Rotavirus particles function as immunological carriers for the delivery of peptides from infectious agents and endogenous proteins. Mol Immunol 1991; 28:269-78; PMID:1850113; http://dx.doi.org/10.1016/0161-5890(91)90073-S
  • Frenchick PJ, Sabara MI, Ready KF, Babiuk LA. Biochemical and immunological characterization of a novel peptide carrier system using rotavirus VP6 particles. Vaccine 1992; 10:783-91; http://dx.doi.org/10.1016/0264-410X(92)90514-K
  • Peralta A, Molinari P, Taboga O. Chimeric recombinant rotavirus-like particles as a vehicle for the display of heterologous epitopes. Virol J 2009; 6:192,422X-6-192; PMID:19891790; http://dx.doi.org/10.1186/1743-422X-6-192
  • Chen Q, He F, Kwang J, Chan JK, Chen J. GM-CSF and IL-4 stimulate antibody responses in humanized mice by promoting T, B, and dendritic cell maturation. J Immunol 2012; 189:5223-9; PMID:23089398; http://dx.doi.org/10.4049/jimmunol.1201789
  • Lappalainen S, Tamminen K, Vesikari T, Blazevic V. Comparative immunogenicity in mice of rotavirus VP6 tubular structures and virus-like particles. Hum Vaccin Immunother 2013; 9:1991-2001; PMID:23777748; http://dx.doi.org/10.4161/hv.25249
  • Treanor JJ, Atmar RL, Frey SE, Gormley R, Chen WH, Ferreira J, Goodwin R, Borkowski A, Clemens R, Mendelman PM. A novel intramuscular bivalent norovirus virus-like particle vaccine candidate-reactogenicity, safety, and immunogenicity in a phase 1 trial in healthy adults. J Infect Dis 2014; 210:1763-71.
  • Bernstein DI, Atmar RL, Lyon GM, Treanor JJ, Chen WH, Jiang X, Vinje J, Gregoricus N, Frenck RW, Jr, Moe CL, et al. Norovirus vaccine against experimental human GII.4 virus illness: A challenge study in healthy adults. J Infect Dis 2014; 211:870-8; PMID:25210140
  • Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, Ferreira J, Estes MK, Graham DY, Opekun AR, Richardson C, et al. Norovirus vaccine against experimental human norwalk virus illness. N Engl J Med 2011; 365:2178-87; PMID:22150036; http://dx.doi.org/10.1056/NEJMoa1101245
  • Abe T, Takahashi H, Hamazaki H, Miyano-Kurosaki N, Matsuura Y, Takaku H. Baculovirus induces an innate immune response and confers protection from lethal influenza virus infection in mice. J Immunol 2003; 171:1133-9; PMID:12874198; http://dx.doi.org/10.4049/jimmunol.171.3.1133
  • Hervas-Stubbs S, Rueda P, Lopez L, Leclerc C. Insect baculoviruses strongly potentiate adaptive immune responses by inducing type I IFN. J Immunol 2007; 178:2361-9; PMID:17277142; http://dx.doi.org/10.4049/jimmunol.178.4.2361
  • Harrington PR, Lindesmith L, Yount B, Moe CL, Baric RS. Binding of norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol 2002; 76:12335-43; PMID:12414974; http://dx.doi.org/10.1128/JVI.76.23.12335-12343.2002
  • Marionneau S, Cailleau-Thomas A, Rocher J, Le Moullac-Vaidye B, Ruvoen N, Clement M, Le Pendu J. ABH and lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 2001; 83:565-73; http://dx.doi.org/10.1016/S0300-9084(01)01321-9
  • Hutson AM, Atmar RL, Graham DY, Estes MK. Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis 2002; 185:1335-7; http://dx.doi.org/10.1086/339883
  • Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, Graham DY, Atmar RL. Serological correlate of protection against norovirus-induced gastroenteritis. J Infect Dis 2010; 202:1212-8; PMID:20815703; http://dx.doi.org/10.1086/656364
  • Nurminen K, Blazevic V, Huhti L, Rasanen S, Koho T, Hytonen VP, Vesikari T. Prevalence of norovirus GII-4 antibodies in finnish children. J Med Virol 2011; 83:525-31; PMID:21264875; http://dx.doi.org/10.1002/jmv.21990
  • Malm M, Uusi-Kerttula H, Vesikari T, Blazevic V. High serum levels of norovirus genotype-specific blocking antibodies correlate with protection from infection in children. J Infect Dis 2014; 210:1755-62; PMID:24970849; http://dx.doi.org/10.1093/infdis/jiu361
  • Debbink K, Lindesmith LC, Baric RS. The state of norovirus vaccines. Clin Infect Dis 2014; 58:1746-52; PMID:24585561; http://dx.doi.org/10.1093/cid/ciu120
  • Atmar RL, Estes MK. Norovirus vaccine development: Next steps. Expert Rev Vaccines 2012; 11:1023-5; http://dx.doi.org/10.1586/erv.12.78
  • Choi P, Reiser H. IL-4: Role in disease and regulation of production. Clin Exp Immunol 1998; 113:317-9; PMID:9737656; http://dx.doi.org/10.1046/j.1365-2249.1998.00690.x
  • Geginat J, Paroni M, Maglie S, Alfen JS, Kastirr I, Gruarin P, De Simone M, Pagani M, Abrignani S. Plasticity of human CD4 T cell subsets. Front Immunol 2014; 5:630; PMID:25566245; http://dx.doi.org/10.3389/fimmu.2014.00630
  • Esquivel FR, Lopez S, Guitierrez-X L, Arias C. The internal rotavirus protein VP6 primes for an enhanced neutralizing antibody response. Arch Virol 2000; 145:813-25; PMID:10893159; http://dx.doi.org/10.1007/s007050050674
  • Ghosh MK, Borca MV, Roy P. Virus-derived tubular structure displaying foreign sequences on the surface elicit CD4+ th cell and protective humoral responses. Virology 2002; 302:383-92; http://dx.doi.org/10.1006/viro.2002.1648
  • Rodriguez M, Wood C, Sanchez-Lopez R, Castro-Acosta RM, Ramirez OT, Palomares LA. Understanding internalization of rotavirus VP6 nanotubes by cells: Towards a recombinant vaccine. Arch Virol 2014; 159:1005-15; PMID:24232915; http://dx.doi.org/10.1007/s00705-013-1916-z
  • Fifis T, Gamvrellis A, Crimeen-Irwin B, Pietersz GA, Li J, Mottram PL, McKenzie IF, Plebanski M. Size-dependent immunogenicity: Therapeutic and protective properties of nano-vaccines against tumors. J Immunol 2004; 173:3148-54; PMID:15322175; http://dx.doi.org/10.4049/jimmunol.173.5.3148
  • Hoebe K, Janssen E, Beutler B. The interface between innate and adaptive immunity. Nat Immunol 2004; 5:971-4; PMID:15454919; http://dx.doi.org/10.1038/ni1004-971
  • Huhti L, Blazevic V, Nurminen K, Koho T, Hytonen VP, Vesikari T. A comparison of methods for purification and concentration of norovirus GII-4 capsid virus-like particles. Arch Virol 2010; 155:1855-8; PMID:20721592; http://dx.doi.org/10.1007/s00705-010-0768-z
  • Huhti L, Tamminen K, Vesikari T, Blazevic V. Characterization and immunogenicity of norovirus capsid-derived virus-like particles purified by anion exchange chromatography. Arch Virol 2013; 158:933-42; PMID:23229011; http://dx.doi.org/10.1007/s00705-012-1565-7
  • Tamminen K, Huhti L, Koho T, Lappalainen S, Hytonen VP, Vesikari T, Blazevic V. A comparison of immunogenicity of norovirus GII-4 virus-like particles and P-particles. Immunology 2012; 135:89-99; PMID:22044070; http://dx.doi.org/10.1111/j.1365-2567.2011.03516.x
  • Malm M, Tamminen K, Lappalainen S, Uusi-Kerttula H, Vesikari T, Blazevic V. Genotype considerations for virus-like particle-based bivalent norovirus vaccine composition. Clin Vaccine Immunol 2015; 22:656-63; PMID:25903355; http://dx.doi.org/10.1128/CVI.00015-15
  • Uusi-Kerttula H, Tamminen K, Malm M, Vesikari T, Blazevic V. Comparison of human saliva and synthetic histo-blood group antigens usage as ligands in norovirus-like particle binding and blocking assays. Microbes Infect 2014; 16:472-80; PMID:24631874; http://dx.doi.org/10.1016/j.micinf.2014.02.010