Antibodies play a pivotal role against viral infection, and maintenance of protection is dependent on plasma and memory B-cells. Understanding antigen-specific B-cell responses in cattle is essential to inform future vaccine design. We have previously defined T-cell-dependent and -independent B-cell responses in cattle, as a prelude to investigating foot-and-mouth-disease-virus (FMDV)-specific B-cell responses. In this study, we have used an FMDV O-serotype vaccination (O1-Manisa or O SKR) and live-virus challenge (FMDV O SKR) to investigate the homologous and heterologous B-cell response in cattle following both vaccination and live-virus challenge. The FMDV O-serotype vaccines were able to induce a cross-reactive plasma-cell response, specific for both O1-Manisa and O SKR, post-vaccination. Post-FMDV O SKR live-virus challenge, the heterologous O1-Manisa vaccination provided cross-protection against O SKR challenge and cross-reactive O SKR-specific plasma cells were induced. However, vaccination and live-virus challenge were not able to induce a detectable FMDV O-serotype-specific memory B-cell response in any of the cattle. The aim of new FMDV vaccines should be to induce memory responses and increased duration of immunity in cattle.
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AibaY.,
KometaniK.,
HamadateM.,
MoriyamaS.,
Sakaue-SawanoA.,
TomuraM.,
LucheH.,
FehlingH. J.,
CasellasR. et al.2010; Preferential localization of IgG memory B cells adjacent to contracted germinal centers. Proc Natl Acad Sci U S A 107:12192–12197 [View Article][PubMed]
BaumgarthN.2013; How specific is too specific? B-cell responses to viral infections reveal the importance of breadth over depth. Immunol Rev 255:82–94 [View Article][PubMed]
BernasconiN. L.,
TraggiaiE.,
LanzavecchiaA.2002; Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199–2202 [View Article][PubMed]
CarrB. V.,
LefevreE. A.,
WindsorM. A.,
IngheseC.,
GubbinsS.,
PrenticeH.,
JuleffN. D.,
CharlestonB.2013; CD4+ T-cell responses to foot-and-mouth disease virus in vaccinated cattle. J Gen Virol 94:97–107 [View Article][PubMed]
CunliffeH. R.1964; Observations on the duration of immunity in cattle after experimental infection with foot-and-mouth disease virus. Cornell Vet 54:501–510
FehrT.,
BachmannM. F.,
BluethmannH.,
KikutaniH.,
HengartnerH.,
ZinkernagelR. M.1996; T-independent activation of B cells by vesicular stomatitis virus: no evidence for the need of a second signal. Cell Immunol 168:184–192 [View Article][PubMed]
FeldmannM.,
EastenA.1971; The relationship between antigenic structure and the requirement for thymus-derived cells in the immune response. J Exp Med 134:103–119[PubMed][CrossRef]
GrantC. F.,
LefevreE. A.,
CarrB. V.,
PrenticeH.,
GubbinsS.,
PollardA. J.,
CharreyreC.,
CharlestonB.2012; Assessment of T-dependent and T-independent immune responses in cattle using a B cell ELISPOT assay. Vet Res 43:68 [View Article][PubMed]
HamblinC.,
BarnettI. T.,
HedgerR. S.1986; A new enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies against foot-and-mouth disease virus. I. Development and method of ELISA. J Immunol Methods 93:115–121[PubMed][CrossRef]
JuleffN.,
WindsorM.,
ReidE.,
SeagoJ.,
ZhangZ.,
MonaghanP.,
MorrisonI. W.,
CharlestonB.2008; Foot-and-mouth disease virus persists in the light zone of germinal centres. PLoS One 3:e3434 [View Article][PubMed]
JuleffN.,
WindsorM.,
LefevreE. A.,
GubbinsS.,
HamblinP.,
ReidE.,
McLaughlinK.,
BeverleyP. C.,
MorrisonI. W.,
CharlestonB.2009; Foot-and-mouth disease virus can induce a specific and rapid CD4+ T-cell-independent neutralizing and isotype class-switched antibody response in naïve cattle. J Virol 83:3626–3636 [View Article][PubMed]
KellyD. F.,
SnapeM. D.,
CutterbuckE. A.,
GreenS.,
SnowdenC.,
DiggleL.,
YuL. M.,
BorkowskiA.,
MoxonE. R. et al.2006; CRM197-conjugated serogroup C meningococcal capsular polysaccharide, but not the native polysaccharide, induces persistent antigen-specific memory B cells. Blood 108:2642–2647 [View Article][PubMed]
KitchingR. P.,
BarnettP.,
PatonD. J.,
MacKayD.2008; Foot and mouth disease. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Mammals, Birds and Bees), 6th edn. pp. 145–173 Paris: Office international des epizooties (OIE);
LefevreE. A.,
CarrB. V.,
PrenticeH.,
CharlestonB.2009; A quantitative assessment of primary and secondary immune responses in cattle using a B cell ELISPOT assay. Vet Res 40:3 [View Article][PubMed]
MartinW. B.,
ChapmanW. G.1961; The tissue culture colour test for assaying the virus and neutralizing antibody of foot and mouth disease and its application to the measurement of immunity in cattle. Research in Veterinary Science 2:53–61
NdunguF. M.,
CadmanE. T.,
CoulcherJ.,
NduatiE.,
CouperE.,
MacdonaldD. W.,
NgD.,
LanghorneJ.2009; Functional memory B cells and long-lived plasma cells are generated after a single Plasmodium chabaudi infection in mice. PLoS Pathog 5:e1000690 [View Article][PubMed]
PegaJ.,
BucafuscoD.,
Di GiacomoS.,
SchammasJ. M.,
MalacariD.,
CapozzoA. V.,
ArztJ.,
Pérez-BeascoecheaC.,
MaradeiE. et al.2013; Early adaptive immune responses in the respiratory tract of foot-and-mouth disease virus-infected cattle. J Virol 87:2489–2495 [View Article][PubMed]
PegaJ.,
Di GiacomoS.,
BucafuscoD.,
SchammasJ. M.,
MalacariD.,
BarrionuevoF.,
CapozzoA. V.,
RodríguezL. L.,
BorcaM. V.,
Pérez-FilgueiraM.2015; Systemic foot-and-mouth disease vaccination in cattle promotes specific antibody-secreting cells at the respiratory tract and triggers local anamnestic responses upon aerosol infection. J Virol 89:9581–9590 [View Article][PubMed]
PortaC.,
KotechaA.,
BurmanA.,
JacksonT.,
RenJ.,
LoureiroS.,
JonesI. M.,
FryE. E.,
StuartD. I.,
CharlestonB.2013; Rational engineering of recombinant picornavirus capsids to produce safe, protective vaccine antigen. PLoS Pathog 9:e1003255 [View Article][PubMed]