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Research Paper

Immune responses elicited against rotavirus middle layer protein VP6 inhibit viral replication in vitro and in vivo

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Pages 2039-2047 | Received 13 Jan 2014, Accepted 11 Apr 2014, Published online: 29 Apr 2014

References

  • Desselberger U, Huppertz HI. Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 2011; 203:188 - 95; http://dx.doi.org/10.1093/infdis/jiq031; PMID: 21288818
  • Estes MK, Kapikian A. Rotaviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, eds. Fields Virology, 5th Edn. Philadelphia: Lippincott Williams & Wilkins, 2007:1917–74.
  • Ludert JE, Feng N, Yu JH, Broome RL, Hoshino Y, Greenberg HB. Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. J Virol 1996; 70:487 - 93; PMID: 8523562
  • Graham KL, Halasz P, Tan Y, Hewish MJ, Takada Y, Mackow ER, Robinson MK, Coulson BS. Integrin-using rotaviruses bind alpha2beta1 integrin alpha2 I domain via VP4 DGE sequence and recognize alphaXbeta2 and alphaVbeta3 by using VP7 during cell entry. J Virol 2003; 77:9969 - 78; http://dx.doi.org/10.1128/JVI.77.18.9969-9978.2003; PMID: 12941907
  • Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M, Johne R. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012; 157:1177 - 82; http://dx.doi.org/10.1007/s00705-012-1273-3; PMID: 22430951
  • 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; http://dx.doi.org/10.1006/viro.1997.8762; PMID: 9344910
  • 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
  • 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; 68:643 - 51; http://dx.doi.org/10.1099/0022-1317-68-3-643; PMID: 3029295
  • Svensson L, Sheshberadaran H, Vesikari T, Norrby E, Wadell G. Immune response to rotavirus polypeptides after vaccination with heterologous rotavirus vaccines (RIT 4237, RRV-1). J Gen Virol 1987; 68:1993 - 9; http://dx.doi.org/10.1099/0022-1317-68-7-1993; PMID: 3037019
  • 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
  • Franco MA, Angel J, Greenberg HB. Immunity and correlates of protection for rotavirus vaccines. Vaccine 2006; 24:2718 - 31; http://dx.doi.org/10.1016/j.vaccine.2005.12.048; PMID: 16446014
  • Offit PA, Blavat G. Identification of the two rotavirus genes determining neutralization specificities. J Virol 1986; 57:376 - 8; PMID: 3001359
  • Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, 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; http://dx.doi.org/10.1056/NEJMoa052434; PMID: 16394298
  • Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, 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; http://dx.doi.org/10.1056/NEJMoa052664; PMID: 16394299
  • Block SL, Vesikari T, Goveia MG, Rivers SB, Adeyi BA, Dallas MJ, Bauder J, Boslego JW, Heaton PM, Pentavalent Rotavirus Vaccine Dose Confirmation Efficacy Study Group. Efficacy, immunogenicity, and safety of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine at the end of shelf life. Pediatrics 2007; 119:11 - 8; http://dx.doi.org/10.1542/peds.2006-2058; PMID: 17200266
  • Vesikari T. Rotavirus vaccination: a concise review. Clin Microbiol Infect 2012; 18:Suppl 5 57 - 63; http://dx.doi.org/10.1111/j.1469-0691.2012.03981.x; PMID: 22882248
  • 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; http://dx.doi.org/10.1006/viro.1998.9060; PMID: 9527925
  • McNeal MM, Rae MN, Bean JA, Ward RL. Antibody-dependent and -independent protection following intranasal immunization of mice with rotavirus particles. J Virol 1999; 73:7565 - 73; PMID: 10438846
  • Ciarlet M, Crawford SE, Barone C, Bertolotti-Ciarlet A, Ramig RF, Estes MK, Conner ME. Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity. J Virol 1998; 72:9233 - 46; PMID: 9765471
  • 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
  • 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; http://dx.doi.org/10.1016/S0264-410X(03)00308-6; PMID: 12922123
  • 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
  • Choi AH, McNeal MM, Basu M, Flint JA, Stone SC, Clements JD, Bean JA, Poe SA, VanCott JL, Ward RL. 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; http://dx.doi.org/10.1016/S0264-410X(02)00315-8; PMID: 12213401
  • Herrmann JE, Chen SC, Fynan EF, Santoro JC, Greenberg HB, Wang S, Robinson HL. Protection against rotavirus infections by DNA vaccination. J Infect Dis 1996; 174:Suppl 1 S93 - 7; http://dx.doi.org/10.1093/infdis/174.Supplement_1.S93; PMID: 8752297
  • Chen SC, Jones DH, Fynan EF, Farrar GH, Clegg JC, Greenberg HB, Herrmann JE. Protective immunity induced by oral immunization with a rotavirus DNA vaccine encapsulated in microparticles. J Virol 1998; 72:5757 - 61; PMID: 9621034
  • Yuan L, Geyer A, Hodgins DC, Fan Z, Qian Y, Chang KO, Crawford SE, Parreño V, Ward LA, Estes MK, et al. Intranasal administration of 2/6-rotavirus-like particles with mutant Escherichia coli heat-labile toxin (LT-R192G) induces antibody-secreting cell responses but not protective immunity in gnotobiotic pigs. J Virol 2000; 74:8843 - 53; http://dx.doi.org/10.1128/JVI.74.19.8843-8853.2000; PMID: 10982326
  • Lee S, Belitsky BR, Brinker JP, Kerstein KO, Brown DW, Clements JD, Keusch GT, Tzipori S, Sonenshein AL, Herrmann JE. Development of a Bacillus subtilis-based rotavirus vaccine. Clin Vaccine Immunol 2010; 17:1647 - 55; http://dx.doi.org/10.1128/CVI.00135-10; PMID: 20810679
  • Zhou H, Guo L, Wang M, Qu J, Zhao Z, Wang J, Hung T. 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; http://dx.doi.org/10.1186/1743-422X-8-3; PMID: 21205330
  • 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; http://dx.doi.org/10.1126/science.272.5258.104; PMID: 8600516
  • 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; http://dx.doi.org/10.1128/JVI.76.16.8110-8117.2002; PMID: 12134016
  • 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; http://dx.doi.org/10.1172/JCI14397; PMID: 11994409
  • Corthésy 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; PMID: 16956954
  • 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; PMID: 23671563
  • 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; http://dx.doi.org/10.1007/s00705-007-1055-5; PMID: 17876681
  • Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, Saif L, Surrey T, Parreño 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; PMID: 18632867
  • Aladin F, Einerhand AW, Bouma J, Bezemer S, Hermans P, Wolvers D, Bellamy K, Frenken LG, Gray J, Iturriza-Gómara M. In vitro neutralisation of rotavirus infection by two broadly specific recombinant monovalent llama-derived antibody fragments. PLoS One 2012; 7:e32949; http://dx.doi.org/10.1371/journal.pone.0032949; PMID: 22403728
  • Vega CG, Bok M, Vlasova AN, Chattha KS, Gómez-Sebastián S, Nuñez C, Alvarado C, Lasa R, Escribano JM, Garaicoechea LL, et al. Recombinant monovalent llama-derived antibody fragments (VHH) to rotavirus VP6 protect neonatal gnotobiotic piglets against human rotavirus-induced diarrhea. PLoS Pathog 2013; 9:e1003334; http://dx.doi.org/10.1371/journal.ppat.1003334; PMID: 23658521
  • Knowlton DR, Spector DM, Ward RL. Development of an improved method for measuring neutralizing antibody to rotavirus. J Virol Methods 1991; 33:127 - 34; http://dx.doi.org/10.1016/0166-0934(91)90013-P; PMID: 1658027
  • 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
  • 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
  • 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; http://dx.doi.org/10.1016/j.vaccine.2011.08.026; PMID: 21854823
  • Vesikari T, Blazevic V, Nurminen K, Huhti L, Lappalainen S, Jokela E. Norovirus capsid and rotavirus VP6 protein for use as combined vaccine. Finnish patent 122520, 15 March 2012.
  • 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; PMID: 23922988
  • Guerrero RA, Ball JM, Krater SS, Pacheco SE, Clements JD, Estes MK. Recombinant Norwalk virus-like particles administered intranasally to mice induce systemic and mucosal (fecal and vaginal) immune responses. J Virol 2001; 75:9713 - 22; http://dx.doi.org/10.1128/JVI.75.20.9713-9722.2001; PMID: 11559804
  • Amuguni JH, Lee S, Kerstein KO, Brown DW, Belitsky BR, Herrmann JE, Keusch GT, Sonenshein AL, Tzipori S. Sublingually administered Bacillus subtilis cells expressing tetanus toxin C fragment induce protective systemic and mucosal antibodies against tetanus toxin in mice. Vaccine 2011; 29:4778 - 84; http://dx.doi.org/10.1016/j.vaccine.2011.04.083; PMID: 21565244
  • 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; http://dx.doi.org/10.4161/hv.25249; PMID: 23777748
  • Angel J, Franco MA, Greenberg HB. Rotavirus immune responses and correlates of protection. Curr Opin Virol 2012; 2:419 - 25; http://dx.doi.org/10.1016/j.coviro.2012.05.003; PMID: 22677178
  • Patel M, Glass RI, Jiang B, Santosham M, Lopman B, Parashar U. A systematic review of anti-rotavirus serum IgA antibody titer as a potential correlate of rotavirus vaccine efficacy. J Infect Dis 2013; 208:284 - 94; http://dx.doi.org/10.1093/infdis/jit166; PMID: 23596320
  • Blutt SE, Conner ME. The Gastrointestinal Frontier: IgA and Viruses. Front Immunol 2013; 4:402; http://dx.doi.org/10.3389/fimmu.2013.00402; PMID: 24348474
  • Cheuvart B, Neuzil KM, Steele AD, Cunliffe N, Madhi SA, Karkada N, Han HH, Vinals C. Association of serum anti-rotavirus immunoglobulin A antibody seropositivity and protection against severe rotavirus gastroenteritis: Analysis of clinical trials of human rotavirus vaccine. Hum Vaccin Immunother 2013; 10:58 - 64; http://dx.doi.org/10.4161/hv.27097; PMID: 24240068
  • Mazanec MB, Kaetzel CS, Lamm ME, Fletcher D, Nedrud JG. Intracellular neutralization of virus by immunoglobulin A antibodies. Proc Natl Acad Sci U S A 1992; 89:6901 - 5; http://dx.doi.org/10.1073/pnas.89.15.6901; PMID: 1323121
  • Tosser G, Delaunay T, Kohli E, Grosclaude J, Pothier P, Cohen J. Topology of bovine rotavirus (RF strain) VP6 epitopes by real-time biospecific interaction analysis. Virology 1994; 204:8 - 16; http://dx.doi.org/10.1006/viro.1994.1505; PMID: 7522377
  • Ward RL, McNeal MM, Sheridan JF. Development of an adult mouse model for studies on protection against rotavirus. J Virol 1990; 64:5070 - 5; PMID: 2168987
  • Pastor AR, Rodríguez-Limas WA, Contreras MA, Esquivel E, Esquivel-Guadarrama F, Ramírez OT, Palomares LA. The assembly conformation of rotavirus VP6 determines its protective efficacy against rotavirus challenge in mice. Vaccine 2014; In press http://dx.doi.org/10.1016/j.vaccine.2014.02.018; PMID: 24583002
  • McNeal MM, Stone SC, Basu M, Bean JA, Clements JD, Hendrickson BA, Choi AH, Ward RL. Protection against rotavirus shedding after intranasal immunization of mice with a chimeric VP6 protein does not require intestinal IgA. Virology 2006; 346:338 - 47; http://dx.doi.org/10.1016/j.virol.2005.11.016; PMID: 16375942
  • Tamminen K, Huhti L, Koho T, Lappalainen S, Hytönen VP, Vesikari T, Blazevic V. A comparison of immunogenicity of norovirus GII-4 virus-like particles and P-particles. Immunology 2012; 135:89 - 99; http://dx.doi.org/10.1111/j.1365-2567.2011.03516.x; PMID: 22044070
  • DiStefano DJ, Gould SL, Munshi S, Robinson DK. Titration of human-bovine rotavirus reassortants using a tetrazolium-based colorimetric end-point dilution assay. J Virol Methods 1995; 55:199 - 208; http://dx.doi.org/10.1016/0166-0934(95)00057-2; PMID: 8537458
  • Pang XL, Joensuu J, Hoshino Y, Kapikian AZ, Vesikari T. Rotaviruses detected by reverse transcription polymerase chain reaction in acute gastroenteritis during a trial of rhesus-human reassortant rotavirus tetravalent vaccine: implications for vaccine efficacy analysis. J Clin Virol 1999; 13:9 - 16; http://dx.doi.org/10.1016/S1386-6532(98)00013-4; PMID: 10405887
  • Ward RL, Bernstein DI, Shukla R, Young EC, Sherwood JR, McNeal MM, Walker MC, Schiff GM. Effects of antibody to rotavirus on protection of adults challenged with a human rotavirus. J Infect Dis 1989; 159:79 - 88; http://dx.doi.org/10.1093/infdis/159.1.79; PMID: 2535868
  • 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; http://dx.doi.org/10.1007/s007050050674; PMID: 10893159