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2016 ; 90
(21
): 9920-9930
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Exploitation of Interleukin-10 (IL-10) Signaling Pathways: Alternate Roles of
Viral and Cellular IL-10 in Rhesus Cytomegalovirus Infection
#MMPMID27558431
Eberhardt MK
; Deshpande A
; Fike J
; Short R
; Schmidt KA
; Blozis SA
; Walter MR
; Barry PA
J Virol
2016[Nov]; 90
(21
): 9920-9930
PMID27558431
show ga
There is accumulating evidence that the viral interleukin-10 (vIL-10) ortholog of
both human and rhesus cytomegalovirus (HCMV and RhCMV, respectively) suppresses
the functionality of cell types that are critical to contain virus dissemination
and help shape long-term immunity during the earliest virus-host interactions. In
particular, exposure of macrophages, peripheral blood mononuclear cells,
monocyte-derived dendritic cells, and plasmacytoid dendritic cells to vIL-10
suppresses multiple effector functions including, notably, those that link innate
and adaptive immune responses. Further, vaccination of RhCMV-uninfected rhesus
macaques with nonfunctional forms of RhCMV vIL-10 greatly restricted parameters
of RhCMV infection following RhCMV challenge of the vaccinees. Vaccinees
exhibited significantly reduced shedding of RhCMV in saliva and urine following
RhCMV challenge compared to shedding in unvaccinated controls. Based on the
evidence that vIL-10 is critical during acute infection, the role of vIL-10
during persistent infection was analyzed in rhesus macaques infected long term
with RhCMV to determine whether postinfection vaccination against vIL-10 could
change the virus-host balance. RhCMV-seropositive macaques, which shed RhCMV in
saliva, were vaccinated with nonfunctional RhCMV vIL-10, and shedding levels of
RhCMV in saliva were evaluated. Following robust increases in vIL-10-binding and
vIL-10-neutralizing antibodies, shedding levels of RhCMV modestly declined,
consistent with the interpretation that vIL-10 may play a functional role during
persistent infection. However, a more significant association was observed
between the levels of cellular IL-10 secreted in peripheral blood mononuclear
cells exposed to RhCMV antigens and shedding of RhCMV in saliva. This result
implies that RhCMV persistence is associated with the induction of cellular IL-10
receptor-mediated signaling pathways. IMPORTANCE: Human health is adversely
impacted by viruses that establish lifelong infections that are often accompanied
with increased morbidity and mortality (e.g., infections with HIV, hepatitis C
virus, or human cytomegalovirus). A longstanding but unfulfilled goal has been to
develop postinfection vaccine strategies that could "reboot" the immune system of
an infected individual in ways that would enable the infected host to develop
immune responses that clear reservoirs of persistent virus infection, effectively
curing the host of infection. This concept was evaluated in rhesus macaques
infected long term with rhesus cytomegalovirus by repeatedly immunizing infected
animals with nonfunctional versions of the rhesus cytomegalovirus-encoded viral
interleukin-10 immune-modulating protein. Following vaccine-mediated boosting of
antibody titers to viral interleukin-10, there was modest evidence for increased
immunological control of the virus following vaccination. More significantly,
data were also obtained that indicated that rhesus cytomegalovirus is able to
persist due to upregulation of the cellular interleukin-10 signaling pathway.
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