Comparative immunogenicity in mice of rotavirus VP6 tubular structures and virus-like particles

Human Vaccines and Immunotherapeutics

Volumn 9, Issue 9, 2013, Pages 1991-2001

  Lappalainen, Suvi ^a   Tamminen, Kirsi ^a   Vesikari, Timo ^a   Blazevic, Vesna ^a  

^a UNIVERSITY OF TAMPERE MEDICAL SCHOOL   (Finland)

Author keywords

dl2 6 VLP; Immunogenicity; Rotavirus; Vaccine; VP6

Indexed keywords

EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; PROTEIN VP6; RECOMBINANT VP6 PROTEIN; ROTAVIRUS VACCINE; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGENICITY; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RELEASE; ELECTRON MICROSCOPY; FECES CULTURE; FEMALE; IMMUNOGENICITY; INFECTION PREVENTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PROTEIN EXPRESSION; ROTAVIRUS INFECTION; TH1 TH2 BALANCE; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS STRAIN;

DL2/6-VLP; IMMUNOGENICITY; ROTAVIRUS; VACCINE; VP6;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BACULOVIRIDAE; CAPSID PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; FEMALE; GASTROINTESTINAL TRACT; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INJECTIONS, INTRAMUSCULAR; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; ROTAVIRUS VACCINES; SF9 CELLS; SPODOPTERA; VACCINES, SYNTHETIC; VACCINES, VIRUS-LIKE PARTICLE; VAGINA;

EID: 84884619017     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.25249     Document Type: Article

References (54)

1. Parez N. Rotavirus gastroenteritis: why to back up the development of new vaccines? Comp Immunol Microbiol Infect Dis 2008; 31:253-69; PMID:17698192; http://dx.doi.org/10.1016/j. cimid.2007.07.005
2. Franco MA, Angel J, Greenberg HB. Immunity and correlates of protection for rotavirus vaccines. Vaccine 2006; 24:2718-31; PMID:16446014; http://dx.doi.org/10.1016/j.vaccine.2005.12.048
3. Labbé M, Charpilienne A, Crawford SE, Estes MK, Cohen J. Expression of rotavirus VP2 produces empty corelike particles. J Virol 1991; 65:2946-52; PMID:1851866
4. Prasad BV, Wang GJ, Clerx JP, Chiu W. Threedimensional structure of rotavirus. J Mol Biol 1988; 199:269-75; PMID:2832610; http://dx.doi.org/10.1016/ 0022-2836(88)90313-0
5. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 2008; 82:3204-19; PMID:18216098; http://dx.doi.org/10.1128/JVI.02257-07
6. Kapikian AZ, Hoshino Y, Chanock RM. Rotaviruses. In: Knipe DM, Howley PM, eds. Fields Virology. 4th Edn. Philadelphia: Lippincott Williams & Wilkins, 2001:1787-833.
7. Tang B, Gilbert JM, Matsui SM, Greenberg HB. Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology 1997; 237:89-96; PMID:9344910; http://dx.doi.org/10.1006/viro.1997.8762
8. Estes MK, Crawford SE, Penaranda ME, Petrie BL, Burns JW, Chan WK, et al. Synthesis and immunogenicity of the rotavirus major capsid antigen using a baculovirus expression system. J Virol 1987; 61:1488-94; PMID:3033276
9. 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
10. Angel J, Franco MA, Greenberg HB. Rotavirus vaccines: recent developments and future considerations. Nat Rev Microbiol 2007; 5:529-39; PMID:17571094; http://dx.doi.org/10.1038/nrmicro1692
11. Lepault J, Petitpas I, Erk I, Navaza J, Bigot D, Dona M, et al. 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
12. Crawford SE, Labbé M, Cohen J, Burroughs MH, Zhou YJ, Estes MK. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J Virol 1994; 68:5945-52; PMID:8057471
13. Centers for Disease Control and Prevention. Statement regarding Rotarix® and RotaTeq® rotavirus vaccines and intussusception. Available from: http://www.cdc. gov/vaccines/vpd-vac/rotavirus/intussusception-studies- Acip.htm [accessed 20.8.2012].
14. McNeal MM, Rae MN, Conner ME, Ward RL. Stimulation of local immunity and protection in mice by intramuscular immunization with triple-or double-layered rotavirus particles and QS-21. Virology 1998; 243:158-66; PMID:9527925; http://dx.doi.org/10.1006/viro.1998.9060
15. McNeal MM, Rae MN, Bean JA, Ward RL. Antibodydependent and -independent protection following intranasal immunization of mice with rotavirus particles. J Virol 1999; 73:7565-73; PMID:10438846
16. Ciarlet M, Crawford SE, Barone C, Bertolotti-Ciarlet A, Ramig RF, Estes MK, et al. Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity. J Virol 1998; 72:9233-46; PMID:9765471
17. O'Neal CM, Crawford SE, Estes MK, Conner ME. Rotavirus virus-like particles administered mucosally induce protective immunity. J Virol 1997; 71:8707-17; PMID:9343229
18. Bertolotti-Ciarlet A, Ciarlet M, Crawford SE, Conner ME, Estes MK. Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine 2003; 21:3885-900; PMID:12922123; http://dx.doi.org/10.1016/S0264-410X(03)00308-6
19. Choi AH, Basu M, McNeal MM, Clements JD, Ward RL. Antibody-independent protection against rotavirus infection of mice stimulated by intranasal immunization with chimeric VP4 or VP6 protein. J Virol 1999; 73:7574-81; PMID:10438847
20. Choi AH, McNeal MM, Basu M, Flint JA, Stone SC, Clements JD, et al. Intranasal or oral immunization of inbred and outbred mice with murine or human rotavirus VP6 proteins protects against viral shedding after challenge with murine rotaviruses. Vaccine 2002; 20:3310-21; PMID:12213401; http://dx.doi.org/10.1016/S0264-410X(02)00315-8
21. Herrmann JE, Chen SC, Fynan EF, Santoro JC, Greenberg HB, Wang S, et al. Protection against rotavirus infections by DNA vaccination. J Infect Dis 1996; 174(Suppl 1):S93-7; PMID:8752297; http://dx.doi.org/10.1093/infdis/174. Supplement-1.S93
22. Chen SC, Jones DH, Fynan EF, Farrar GH, Clegg JC, Greenberg HB, et al. Protective immunity induced by oral immunization with a rotavirus DNA vaccine encapsulated in microparticles. J Virol 1998; 72:5757-61; PMID:9621034
23. 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
24. McNeal MM, Basu M, Bean JA, Clements JD, Choi AH, Ward RL. Identification of an immunodominant CD4+ T cell epitope in the VP6 protein of rotavirus following intranasal immunization of BALB/c mice. Virology 2007; 363:410-8; PMID:17337285; http://dx.doi.org/10.1016/j.virol.2007.01.041
25. Choi AH, Basu M, McNeal MM, Flint J, VanCott JL, Clements JD, et al. Functional mapping of protective domains and epitopes in the rotavirus VP6 protein. J Virol 2000; 74:11574-80; PMID:11090155; http://dx.doi.org/10.1128/ JVI.74.24.11574-11580.2000
26. McNeal MM, VanCott JL, Choi AH, Basu M, Flint JA, Stone SC, et al. CD4 T cells are the only lymphocytes needed to protect mice against rotavirus shedding after intranasal immunization with a chimeric VP6 protein and the adjuvant LT(R192G). J Virol 2002; 76:560-8; PMID:11752147; http://dx.doi.org/10.1128/JVI. 76.2.560-568.2002
27. Zhou H, Guo L, Wang M, Qu J, Zhao Z, Wang J, et al. Prime immunization with rotavirus VLP 2/6 followed by boosting with an adenovirus expressing VP6 induces protective immunization against rotavirus in mice. Virol J 2011; 8:3; PMID:21205330; http://dx.doi.org/10.1186/1743-422X-8-3
28. Lee S, Belitsky BR, Brinker JP, Kerstein KO, Brown DW, Clements JD, et al. Development of a Bacillus subtilis-based rotavirus vaccine. Clin Vaccine Immunol 2010; 17:1647-55; PMID:20810679; http://dx.doi.org/10.1128/CVI.00135-10
29. Schwartz-Cornil I, Benureau Y, Greenberg H, Hendrickson BA, Cohen J. Heterologous protection induced by the inner capsid proteins of rotavirus requires transcytosis of mucosal immunoglobulins. J Virol 2002; 76:8110-7; PMID:12134016; http://dx.doi.org/10.1128/JVI.76.16.8110-8117.2002
30. González SA, Affranchino JL. Assembly of doublelayered virus-like particles in mammalian cells by coexpression of human rotavirus VP2 and VP6. J Gen Virol 1995; 76:2357-60; PMID:7561777; http://dx.doi.org/10.1099/0022-1317- 76-9-2357
31. Finkelman FD, Holmes J, Katona IM, Urban JF Jr., Beckmann MP, Park LS, et al. Lymphokine control of in vivo immunoglobulin isotype selection. Annu Rev Immunol 1990; 8:303-33; PMID:1693082; http://dx.doi.org/10.1146/annurev.iy.08. 040190.001511
32. Ruggeri FM, Johansen K, Basile G, Kraehenbuhl JP, Svensson L. Antirotavirus immunoglobulin A neutralizes virus in vitro after transcytosis through epithelial cells and protects infant mice from diarrhea. J Virol 1998; 72:2708-14; PMID:9525588
33. 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
34. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, et al.; Human Rotavirus Vaccine Study Group. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 2006; 354:11-22; PMID:16394298; http://dx.doi.org/10.1056/ NEJMoa052434
35. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, et al.; Rotavirus Efficacy and Safety Trial (REST) Study Team. 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
36. Bachmann MF, Rohrer UH, Kündig TM, Bürki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 1993; 262:1448-51; PMID:8248784; http://dx.doi.org/10.1126/science. 8248784
37. Fifis T, Gamvrellis A, Crimeen-Irwin B, Pietersz GA, Li J, Mottram PL, et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J Immunol 2004; 173:3148-54; PMID:15322175
38. Keller SA, Bauer M, Manolova V, Muntwiler S, Saudan P, Bachmann MF. Cutting edge: limited specialization of dendritic cell subsets for MHC class II-Associated presentation of viral particles. J Immunol 2010; 184:26-9; PMID:19949081; http://dx.doi.org/10.4049/jimmunol.0901540
39. Ghosh MK, Dériaud E, Saron MF, Lo-Man R, Henry T, Jiao X, et al. 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
40. Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med 2012; 18:274-80; PMID:22286307; http://dx.doi.org/10.1038/nm.2612
41. 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
42. Sabara M, Gilchrist JE, Hudson GR, Babiuk LA. Preliminary characterization of an epitope involved in neutralization and cell attachment that is located on the major bovine rotavirus glycoprotein. J Virol 1985; 53:58-66; PMID:2578197
43. Gualtero DF, Guzmán F, Acosta O, Guerrero CA. Amino acid domains 280-297 of VP6 and 531-554 of VP4 are implicated in heat shock cognate protein hsc70-mediated rotavirus infection. Arch Virol 2007; 152:2183-96; PMID:17876681; http://dx.doi.org/10.1007/s00705-007-1055-5
44. Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, Saif L, et al. Llamaderived 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; PMID:18632867; http://dx.doi.org/10.1128/JVI.00436-08
45. Aladin F, Einerhand AW, Bouma J, Bezemer S, Hermans P, Wolvers D, et al. In vitro neutralisation of rotavirus infection by two broadly specific recombinant monovalent llama-derived antibody fragments. PLoS One 2012; 7:e32949; PMID:22403728; http://dx.doi.org/10.1371/journal.pone.0032949
46. Butler JE, Heo Y, Adams P, Richerson HB. The antigen-limited nature of microtiter ELISAs requires partial depletion of IgG to permit reliable determination of rabbit serum IgA antibody activity. Mol Immunol 1990; 27:319-25; PMID:2359410; http://dx.doi.org/10.1016/0161-5890(90)90044-Z
47. Jauhiainen T, Tuomi T, Leinonen M, Kark JD, Saikku P. Interference of immunoglobulin G (IgG) antibodies in IgA antibody determinations of Chlamydia pneumoniae by microimmunofluorescence test. J Clin Microbiol 1994; 32:839-40; PMID:8195403
48. Coffin SE, Clark SL, Bos NA, Brubaker JO, Offit PA. Migration of antigen-presenting B cells from peripheral to mucosal lymphoid tissues may induce intestinal antigen-specific IgA following parenteral immunization. J Immunol 1999; 163:3064-70; PMID:10477570
49. Corthésy B, Benureau Y, Perrier C, Fourgeux C, Parez N, Greenberg H, et al. Rotavirus anti-VP6 secretory immunoglobulin A contributes to protection via intracellular neutralization but not via immune exclusion. J Virol 2006; 80:10692-9; PMID:16956954; http://dx.doi.org/10.1128/JVI.00927-06
50. Fromantin C, Jamot B, Cohen J, Piroth L, Pothier P, Kohli E. Rotavirus 2/6 virus-like particles administered intranasally in mice, with or without the mucosal adjuvants cholera toxin and Escherichia coli heat-labile toxin, induce a Th1/Th2-like immune response. J Virol 2001; 75:11010-6; PMID:11602741; http://dx.doi.org/10.1128/JVI.75.22.11010-11016.2001
51. Matthijnssens J, Rahman M, Martella V, Xuelei Y, De Vos S, De Leener K, et al. Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J Virol 2006; 80:3801-10; PMID:16571797; http://dx.doi.org/10.1128/JVI.80.8.3801-3810. 2006
52. Tamminen K, Huhti L, Koho T, Lappalainen S, Hytönen VP, Vesikari T, et al. 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
53. Knowlton DR, Spector DM, Ward RL. Development of an improved method for measuring neutralizing antibody to rotavirus. J Virol Methods 1991; 33:127-34; PMID:1658027; http://dx.doi.org/10.1016/0166-0934(91)90013-P
54. Ward RL, Kapikian AZ, Goldberg KM, Knowlton DR, Watson MW, Rappaport R. Serum rotavirus neutralizing-Antibody titers compared by plaque reduction and enzyme-linked immunosorbent assay-based neutralization assays. J Clin Microbiol 1996; 34:983-5; PMID:8815124