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*
The Rockefeller University, New York, NY 10021; and
The Virogenetics Corporation, Troy, NY
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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We speculated that access to dendritic cells (DCs)3 in vivo may be critical for vaccinia and other poxviruses to elicit potent immune responses. DCs are potent APCs that activate CD4+ and CD8+ T lymphocytes and do so in small numbers (6, 7, 8, 9, 10, 11). Traditionally, vaccinia is delivered by scarification, and local epidermal DCs (Langerhans cells) in the skin may provide a vehicle to traffic vaccinia to draining lymph nodes. In the skin and in most tissues, DCs exist as immature cells, expressing low levels of MHC and costimulator molecules such as CD86. In this stage, DCs are equipped to acquire Ags via phagocytosis, macropinocytosis, and receptor-mediated endocytosis. After Ag acquisition, immature DCs are induced to migrate to the lymph nodes and undergo maturation. Maturation entails the down-regulation of Ag-acquiring and Ag-processing properties and the up-regulation of MHC and costimulator molecules to activate Ag-specific T cells (12, 13, 14).
In this study, we analyzed human DCs for the ability to support vaccinia infection and replication. Our results indicate that vaccinia abortively infects DCs, blocks their maturation, and induces delayed apoptosis. These data suggest new mechanisms by which vaccinia may evade the immune response.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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RPMI 1640 with 10 mM HEPES, 5 mM L-glutamine, 20 µg/ml gentamicin supplemented with 1% human plasma, 5% heat-inactivated human serum, or 10% FCS was used throughout these studies.
Mononuclear subsets
PBMCs. PBMCs were prepared from buffy coat fractions by isolation over Ficoll-Hypaque (Pharmacia, Upjohn, Kalamazoo, MI), and separated into T cell-enriched or T cell-depleted fractions by rosetting with SRBC (15, 16).
DCs. Immature DCs were derived from monocyte-enriched T cell-depleted fractions by plating in complete medium containing 1% human plasma for 6 to 8 days supplemented with 1000 U/ml of human rIL-4 (Schering-Plough, Madison, NJ) and 1000 U/ml of human rGM-CSF (Immunex, Seattle, WA). Mature DCs were generated by transferring the nonadherent cell fraction to new plates on day 6 to 8 and incubation for 1 to 2 days in monocyte-conditioned medium (50% v/v), as previously described (15, 16).
B-LCL. B-lymphoblastoid cell lines (B-LCL) were generated from PBMC by transformation with EBV supernatants, and maintained in RPMI containing 10% FCS (R10).
Virus stocks
The following recombinant WR vaccinia viruses were used: vP1170 parental vector, and vP1287, vP1288, vP1218-containing HIV-gag, pol and nef encoding genes, respectively, provided by Drs. James Tartaglia and William I. Cox (Virogenetics, Troy, NY).
Infection of APCs.
APCs were brought up to 1 x 107 cells/ml and infected with vaccinia stocks at MOIs of 1–2.5 in 0.1–0.3 ml for 1 h at 37°C. Following infection, cells were washed twice and cultured at 0.3 x 106 cells/ml in 1-ml vol in 24-well plates.
Cytofluorography
mAbs. The VV1-4G9, VV1-2F10, and VV1-6B6 anti-vaccinia mAbs reacting with the proteins D8L, A56R, and an early 29-kDa protein were kindly provided by Dr. Alan Schmaljohn (USAMRIID, Frederick, MD). The mAbs 183 against HIV p24 protein and to the lysosomal DC-LAMP were kindly provided by Dr. Melissa Pope (The Rockefeller University, New York, NY) and Dr. Serge Lebecque (Schering-Plough), respectively. HLA-DR-PE, CD25-PE, and isotype controls were purchased from Becton Dickinson (San Jose, CA), CD86-PE from PharMingen (San Diego, CA), and CD83 from Coulter (Palo Alto, CA). PE-conjugated goat anti-mouse IgG (Sigma Biosciences) was used as a secondary reagent.
Surface staining. Cells were phenotyped with the panel of mAbs, fixed in 1% formaldehyde, and analyzed on a FACScan.
Intracellular staining. Cells were fixed with 4% paraformaldehyde and permeabilized with 1% saponin, as previously described (17). Cells were exposed to primary Abs and secondary reagent for 30 min and analyzed on a FACScan.
Viability
The percentage of viable cells was assessed by trypan blue exclusion. Apoptosis and necrosis were assessed by staining with FITC-annexin V/propidium iodide (PI) using the Early Apoptosis detection kit (Kamiya Biomedical, Thousand Oaks, CA), according to the manufacturer’s instructions.
T cell responses
The allogeneic MLR was used to monitor DC function. DCs were added in graded doses to 2 x 105 allogeneic T cells in 96-well flat-bottom plates (Costar, Cambridge, MA) in triplicate. Proliferation was determined on day 5 with the addition of 4 µCi/ml of [3H]TdR for 12–16 h (mean cpm). In the superantigen-dependent T cell proliferation assays, graded doses of DCs were added to syngeneic T cells in the presence of 0.01–0.1 ng/ml of staphylococcal enterotoxin A. Proliferation was determined as above on day 3.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Vaccinia is highly cytopathic in several cells (4). We therefore analyzed immature and mature DCs for cytopathic effects following infection with vaccinia. Immature DCs were generated from T cell-depleted blood mononuclear cells by incubation with GM-CSF and IL-4 for 6 to 8 days (15). They were induced to mature by the addition of 50% (v/v) monocyte-conditioned medium (MCM) for 1 to 2 days. Mature DCs can be distinguished by high levels of MHC and costimulatory molecules, the DC-restricted markers CD83 and DC-LAMP, and strong immunostimulatory activity (reviewed in Ref. 14). DCs were infected at MOIs of 1–2. Following infection, immature DCs were exposed to MCM immediately. Cells were analyzed for viability for up to 3 days after infection.
After 1 day of infection, the mean percentage of viable immature DCs
was 73%, as measured by trypan blue exclusion, and 84% in the case of
uninfected cells (Fig. 1
, A
and B). For mature DCs, the mean percentages were 92% and
84% for uninfected and infected cells, respectively. At later time
points, however, vaccinia-infected immature DCs died at higher rates
when compared with mature DCs. Three days after vaccinia infection, the
viability in immature DCs dropped from 76% to 46% (Fig. 1A). Vaccinia-infected monocytes and immature DCs that were
not exposed to MCM showed a similar decrease in viability (40–50%
viable cells on day 3 postinfection).
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B). From a
total of eight experiments, we determined that vaccinia infection of
immature DCs led to 21–30% reduction in viability compared with only
7–11% reduction in mature DCs. Therefore, immature DCs and monocytes
are more susceptible than mature DCs to the cytopathic effects of
vaccinia. Immature DCs infected with vaccinia die by delayed apoptosis
To determine whether immature DCs infected with vaccinia were
dying via apoptosis, we stained DCs with FITC-annexin V, which
binds to phosphatidylserine on the surface of cells undergoing early
apoptosis (18, 19). After 1 day of infection, no
significant differences were noted between uninfected and infected DCs.
By day 2, a significant number of apoptotic cells (33% Annexin
V+, PI-) and cells
undergoing secondary necrosis (12% Annexin V+
and PI+) were apparent in the immature DC
population (Fig. 2), coincident with the
time when viability drops by trypan blue exclusion (Fig. 1). By day 3,
more than half the DCs had undergone apoptosis and secondary necrosis.
In contrast, mature DCs were largely resistant to the induction of
apoptosis by vaccinia virus (Fig. 2, right panels). The data
indicate that vaccinia causes substantial cytopathic effects due to
apoptosis in immature DCs, albeit delayed.
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We next followed the life cycle of vaccinia in DCs and other APCs. mAbs reacting with early and late proteins were used to assess the vaccinia replication cycle in infected cells (4). The VV1-6B6 Ab detects an early intracellular protein of 29 kDa. The VV1-4G9 Ab reacts with the hemagglutinin protein (A56R), a late protein found on the surface of the extracellular virions, but also on the membranes of productively infected cells (4, 20). The VV1-2F10 Ab detects D8L, a late protein found on the surface of the intracellular immature virions, and the surfaces of productively infected cells (21, 22).
One day after vaccinia infection, the majority of B-LCLs expressed the
29-kDa early Ag, the hemagglutinin, and the D8L protein (Fig. 3), confirming earlier data regarding the
permissiveness for vaccinia (23). Although few DCs
expressed late cycle Ags, they did express the early cycle 29-kDa Ag
(see arrows, Fig. 3). Thirty-five percent of mature DCs (range
22–46%, n = 3) and 67% of immature DCs (range
50–85%, n = 5) expressed the 29-kDa Ag, demonstrating
that the mature DCs are more resistant to infection, a feature that
correlates with the reduced cytopathic effects (Fig. 1). Similar data
were obtained regardless of the types of recombinant vaccinia
used.
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Vaccinia interferes with the maturation of DCs
Influenza infection of immature DCs induces maturation in
the absence of additional factors (24) (data not shown).
We therefore examined the effects of vaccinia infection on the
maturation of DCs. Three populations were analyzed: immature DCs,
immature DCs that were exposed to MCM following infection, and mature
DCs. Surprisingly, we found that vaccinia inhibited the expression of
many proteins known to be induced during DC maturation, including CD83,
a marker of DC maturation, CD86, DR, and CD25 (Fig. 4). The inhibition was most marked in
immature DCs that were infected and then exposed to MCM, but a similar
pattern was seen in the immature DC population to which no MCM was
added after infection. In the later case, the effects were probably in
a minor contaminating population of maturing DCs. On the other hand,
mature DCs were much less affected by vaccinia infection. CD83 and CD86
expression were slightly inhibited, but CD25 and DR levels were not
affected. The partial effect on mature DCs would appear to correlate
with their lesser susceptibility to infection.
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A). When MCM was added to
infected immature DCs, only the fraction that did not express viral Ag
was able to proceed to maturation (31%
VV1-6B6-, DC-LAMP+]. In
fact, of the total infected cell population (24% of total cells), only
4% were VV1-6B6+, DC-LAMP+
(1% of total cells), whereas 96% were VV1-6B6+,
DC-LAMP- (23% of total cells). Thus, 96% of
the infected (VV1-6B6+) cells actually failed to
proceed to maturation (Fig. 5A).
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gave similar results (not
shown). Thus, inhibition of maturation is a direct consequence of
vaccinia infection.
In contrast to immature DC populations, there was a significant
population of
VV1-6B6+/DC-LAMP+ cells in
infected mature DCs. In general, however, 
2-fold more immature
DC-LAMP-negative DCs were infected (mean 43%, range 21–64%,
n = 9) as compared with mature
DC-LAMP+ DCs (mean 17%, range 8–35%,
n = 6). To ascertain that infection blocks maturation
before cell death, we performed double labeling experiments. DC markers
were viewed in conjunction with PI staining. As Fig. 5B
shows, infected immature DCs exposed to MCM for 1 day showed a greater
than 4-fold inhibition in the up-regulation of CD25, a maturation
marker, without an increase in PI staining compared with uninfected
cells. As previously shown (Fig. 4), mature DCs retained CD25
expression.
Vaccinia infection impairs DC function
Because of the effects of vaccinia on DC viability and maturation,
we assessed DC function in the allogeneic MLR. Mature DCs are the most
powerful stimulators of T cell proliferation in this assay.
Vaccinia-infected immature DCs that were exposed to MCM were markedly
impaired in their stimulatory capacity (percentage of inhibition ranged
from 82–91% at DC:T cell ratios of 1:100–1:900). Infected mature DCs
were also less stimulatory, but the degree of inhibition was far less
impressive (range of 0–45% inhibition at DC:T cell ratios of
1:100–1:900) (Fig. 6, upper
panel). Similar results were observed in other assays of DC
function, e.g., superantigen-dependent T cell proliferation, in which
inhibition induced by infected immature DCs was 62–73% vs 3–30% by
mature DCs at DC:T cell ratios of 1:100–1:900 (Fig. 6, lower
panel). The loss of function in immature DCs is presumably
due to a combination of DC death and inhibition of maturation. Given
that mature DCs are far less affected both with respect to viability
and down-regulation of costimulatory molecules, it is not surprising
that their function is less compromised.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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, IFN-,ß, and IFN-
and inhibitors of the IFN
transduction pathway (4, 5). Our studies identify a novel
mechanism by which vaccinia can evade the immune response. Vaccinia
inhibits DC maturation within 1 day of infection (Figs. 4 and 5).
Infection in DCs is also characterized by abortive replication and
induction of apoptosis (Figs. 2 and 3). The effects are most pronounced
in immature DCs, which are more susceptible to vaccinia infection. As
far as we are aware, this is the first example of a viral pathogen that
interferes with DC maturation. While this study was under review, two
other reports appeared describing the inhibition of DC maturation by
protozoans. Plasmodium falciparum, the malaria
parasite, infects erythrocytes and induces the expression of surface
PfEMP-1 Ag. The modified erythrocytes bind immature DCs and inhibit
their maturation and function upon exposure to LPS (26).
In another study, Trypanosoma cruzi was found to produce
soluble factors that prevent DC maturation (27). In
contrast to these reports and our findings, other pathogens are known
to induce DC maturation following uptake, e.g., influenza virus
(13, 14, 24, 28). The advantage to the host in the latter
case is that Ag acquisition and processing of microbial Ags are
followed by efficient T cell stimulation. By inhibiting the maturation
pathway of DCs, and inducing their death, vaccinia can subvert the
development of efficient antiviral T cell immunity (Fig. 6). Pathologic
poxviruses, e.g., smallpox, may employ such mechanisms in their arsenal
of immune evasion tactics.
How might vaccinia inhibit maturation? MCM, the DC maturation stimulus
used in this study, contains IFN-, TNF-, and IL-1ß, which are
key cytokines in the induction of DC maturation (12, 13, 16, 29). Production of cytokine receptor homologues in the early
cycle by vaccinia, e.g., for IFN-, may account in part for the block
in DC maturation. Interestingly, the orf poxvirus encodes a
functional factor that inhibits the activity of GM-CSF
(30), which is requisite for generating DCs from
hemopoietic progenitors in culture (14).
Another consequence of vaccinia infection in DCs is an abortive
replication. Immature and mature human DCs, as well as monocytes,
permit the expression of early but not late cycle vaccinia proteins.
Our findings are in agreement with studies showing that murine and
human macrophages supported the expression of vaccinia early but not
late proteins (31, 32), while murine and human DCs
transcribed a reporter gene under the control of a vaccinia early
promoter, but not a late promoter (23). The block in
vaccinia viral replication in DCs is not understood at this time.
However, resistance to infection or inhibition of viral replication in
mature DCs, at least, is beginning to emerge as a common theme. For
example, mature DCs do not support influenza replication, yet still
efficiently present influenza Ags to T cells (17, 33). HIV
replication is also blocked in mature DCs, yet the DCs can still
transmit virus to T cells (34, 35). Mature DCs may acquire
mechanisms that inhibit virus entry or infection. An antiviral state
may be conferred as a consequence of maturation by type I IFNs, e.g.,
IFN- (16, 29). IFNs induce the expression of the Mx
proteins, the serine/threonine protein kinase, PKR, and 2'-5'
oligoadenylate synthetase (2-5A), all of which inhibit viral
replication (36, 37). In fact, a protein with 2'-5'
oligoadenylate-synthesizing activity was recently described in maturing
DCs (38). On the other hand, if vaccinia infects the DC
before maturation, synthesis of early viral proteins, e.g., E3L and K3L
(inhibitors of PKR and the 2-5A systems), may interfere with the
induction of the antiviral state.
Vaccinia infection led to delayed apoptosis in DCs, the effect more
evident and extensive in immature than mature DCs (Fig. 1 and data not
shown). The delay may be due to the production of apoptosis inhibitors,
e.g., SP-2 (39, 40). Mature DCs may be more resistant to
vaccinia’s apoptotic effect possibly because of higher levels of PKR
and 2-5A that inhibit the synthesis of proapoptotic products, e.g.,
dsRNA (Fig. 3 and Refs. 36, 37, 41). Furthermore,
maturation stimuli such as TNF- (a component of MCM) or CD40 ligand
promote viability of DCs via up-regulation of antiapoptotic proteins,
e.g., Bcl-xL (42, 43, 44, 45).
There is evidence that DCs are important in generating an immune response against poxviruses in vivo. In a mouse tumor model, only recombinant vaccinia vectors expressing a tumor-associated Ag under early promoters were capable of inducing protective and therapeutic immune responses (23). In functional assays, murine DCs infected with vaccinia-encoding Ag regulated by an early promoter activated Ag-specific CTL, while vaccinia vectors with late promoter-regulated genes did not. The recruitment of high numbers of DCs to the orf poxvirus skin lesion has also been described (30). Because DCs are the main initiators of immune responses and vaccinia inhibits their maturation, one important question is how the anti-vaccinia response is generated.
One possibility is that sufficient numbers of DCs survive vaccinia
infection to initiate T cell responses. Alternatively, DCs may mature
in vivo before infection. Poxvirus infections can induce the rapid and
systemic release of IL-1ß, IFN-, GM-CSF, and TNF- (4, 5, 30), all of which could affect the maturation of DCs from
precursors (12, 13, 16, 29). As shown in this study, a
significant fraction of mature DCs can be infected with vaccinia (Fig. 5A). These cells are far more resistant to apoptosis induced
by vaccinia, and retain the capacity to stimulate significant T cell
responses (Fig. 6 and Ref. 46). Another mechanism by which
the anti-vaccinia response may be generated is through
cross-presentation. Bystander DCs may ingest vaccinia-infected
apoptotic cells and present viral antigenic epitopes to T cells. We
have demonstrated that DCs phagocytose influenza virus-infected
apoptotic cells and cross-present influenza Ags to
CD8+ T cells (47, 48). This pathway
of representing Ags is highly efficient and may be the in vitro
equivalent of the in vivo phenomenon of cross-priming. Further studies
along these lines will be necessary to fathom how immunity to vaccinia
is generated.
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Acknowledgments |
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Footnotes |
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2 Address correspondence and reprint requests to Dr. Nina Bhardwaj, The Rockefeller University, 1230 York Avenue, New York, NY 10021. E-mail address:
3 Abbreviations used in this paper: DC, dendritic cell; B-LCL, B-lymphoblastoid cell line; LAMP, lysosome-associated membrane protein; MCM, monocyte-conditioned medium; MOI, multiplicity of infection; PI, propidium iodide; PKR, dsRNA-activated protein kinase.
Received for publication April 14, 1999. Accepted for publication September 28, 1999.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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M. Ostrowski, M. Vermeulen, O. Zabal, J. R. Geffner, A. M. Sadir, and O. J. Lopez Impairment of Thymus-Dependent Responses by Murine Dendritic Cells Infected with Foot-and-Mouth Disease Virus J. Immunol., September 15, 2005; 175(6): 3971 - 3979. [Abstract] [Full Text] [PDF]
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E. Flano, B. Kayhan, D. L. Woodland, and M. A. Blackman Infection of Dendritic Cells by a {gamma}2-Herpesvirus Induces Functional Modulation J. Immunol., September 1, 2005; 175(5): 3225 - 3234. [Abstract] [Full Text] [PDF]
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A. Chahroudi, R. Chavan, N. Koyzr, E. K. Waller, G. Silvestri, and M. B. Feinberg Vaccinia Virus Tropism for Primary Hematolymphoid Cells Is Determined by Restricted Expression of a Unique Virus Receptor J. Virol., August 15, 2005; 79(16): 10397 - 10407. [Abstract] [Full Text] [PDF]
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L. Liu, Z. Xu, R. C. Fuhlbrigge, V. Pena-Cruz, J. Lieberman, and T. S. Kupper Vaccinia Virus Induces Strong Immunoregulatory Cytokine Production in Healthy Human Epidermal Keratinocytes: a Novel Strategy for Immune Evasion J. Virol., June 15, 2005; 79(12): 7363 - 7370. [Abstract] [Full Text] [PDF]
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 J. G. Shannon, D. Howe, and R. A. Heinzen Virulent Coxiella burnetii does not activate human dendritic cells: Role of lipopolysaccharide as a shielding molecule PNAS, June 14, 2005; 102(24): 8722 - 8727. [Abstract] [Full Text] [PDF]
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A. T. Prechtel, N. M. Turza, D. J. Kobelt, J. I. Eisemann, R. S. Coffin, Y. McGrath, C. Hacker, X. Ju, M. Zenke, and A. Steinkasserer Infection of mature dendritic cells with herpes simplex virus type 1 dramatically reduces lymphoid chemokine-mediated migration J. Gen. Virol., June 1, 2005; 86(6): 1645 - 1657. [Abstract] [Full Text] [PDF]
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L. Bousarghin, P. Hubert, E. Franzen, N. Jacobs, J. Boniver, and P. Delvenne Human papillomavirus 16 virus-like particles use heparan sulfates to bind dendritic cells and colocalize with langerin in Langerhans cells J. Gen. Virol., May 1, 2005; 86(5): 1297 - 1305. [Abstract] [Full Text] [PDF]
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 S. Muraro, A. Bondanza, M. Bellone, P. D. Greenberg, and C. Bonini Molecular modification of idiotypes from B-cell lymphomas for expression in mature dendritic cells as a strategy to induce tumor-reactive CD4+ and CD8+ T-cell responses Blood, May 1, 2005; 105(9): 3596 - 3604. [Abstract] [Full Text] [PDF]
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P. Beuria, H. Chen, M. Timoney, and K. Sperber Impaired Accessory Cell Function in a Human Dendritic Cell Line after Human Immunodeficiency Virus Infection Clin. Vaccine Immunol., March 1, 2005; 12(3): 453 - 464. [Abstract] [Full Text] [PDF]
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M. Chen, C. Barnfield, T. I. Naslund, M. N. Fleeton, and P. Liljestrom MyD88 Expression Is Required for Efficient Cross-Presentation of Viral Antigens from Infected Cells J. Virol., March 1, 2005; 79(5): 2964 - 2972. [Abstract] [Full Text] [PDF]
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T. N. J. Bullock and H. Yagita Induction of CD70 on Dendritic Cells through CD40 or TLR Stimulation Contributes to the Development of CD8+ T Cell Responses in the Absence of CD4+ T Cells J. Immunol., January 15, 2005; 174(2): 710 - 717. [Abstract] [Full Text] [PDF]
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D. Wilflingseder, B. Mullauer, H. Schramek, Z. Banki, M. Pruenster, M. P. Dierich, and H. Stoiber HIV-1-Induced Migration of Monocyte-Derived Dendritic Cells Is Associated with Differential Activation of MAPK Pathways J. Immunol., December 15, 2004; 173(12): 7497 - 7505. [Abstract] [Full Text] [PDF]
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S. Tavakoli, W. Schwerin, A. Rohwer, S. Hoffmann, S. Weyer, R. Weth, H. Meisel, H. Diepolder, M. Geissler, P. R. Galle, et al. Phenotype and function of monocyte derived dendritic cells in chronic hepatitis B virus infection J. Gen. Virol., October 1, 2004; 85(10): 2829 - 2836. [Abstract] [Full Text] [PDF]
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L. Fantuzzi, C. Purificato, K. Donato, F. Belardelli, and S. Gessani Human Immunodeficiency Virus Type 1 gp120 Induces Abnormal Maturation and Functional Alterations of Dendritic Cells: a Novel Mechanism for AIDS Pathogenesis J. Virol., September 15, 2004; 78(18): 9763 - 9772. [Abstract] [Full Text] [PDF]
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J. A. Tobar, P. A. Gonzalez, and A. M. Kalergis Salmonella Escape from Antigen Presentation Can Be Overcome by Targeting Bacteria to Fc{gamma} Receptors on Dendritic Cells J. Immunol., September 15, 2004; 173(6): 4058 - 4065. [Abstract] [Full Text] [PDF]
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W. L. W. Chang, N. Baumgarth, D. Yu, and P. A. Barry Human Cytomegalovirus-Encoded Interleukin-10 Homolog Inhibits Maturation of Dendritic Cells and Alters Their Functionality J. Virol., August 15, 2004; 78(16): 8720 - 8731. [Abstract] [Full Text] [PDF]
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 E. Zinser, M. Lechmann, A. Golka, M. B. Lutz, and A. Steinkasserer Prevention and Treatment of Experimental Autoimmune Encephalomyelitis by Soluble CD83 J. Exp. Med., August 2, 2004; 200(3): 345 - 351. [Abstract] [Full Text] [PDF]
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R. Drillien, D. Spehner, and D. Hanau Modified vaccinia virus Ankara induces moderate activation of human dendritic cells J. Gen. Virol., August 1, 2004; 85(8): 2167 - 2175. [Abstract] [Full Text] [PDF]
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N. Teleshova, J. Kenney, J. Jones, J. Marshall, G. Van Nest, J. Dufour, R. Bohm, J. D. Lifson, A. Gettie, and M. Pope CpG-C Immunostimulatory Oligodeoxyribonucleotide Activation of Plasmacytoid Dendritic Cells in Rhesus Macaques to Augment the Activation of IFN-{gamma}-Secreting Simian Immunodeficiency Virus-Specific T Cells J. Immunol., August 1, 2004; 173(3): 1647 - 1657. [Abstract] [Full Text] [PDF]
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A. Granelli-Piperno, A. Golebiowska, C. Trumpfheller, F. P. Siegal, and R. M. Steinman HIV-1-infected monocyte-derived dendritic cells do not undergo maturation but can elicit IL-10 production and T cell regulation PNAS, May 18, 2004; 101(20): 7669 - 7674. [Abstract] [Full Text] [PDF]
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B. C. Turner, E. M. Hemmila, N. Beauchemin, and K. V. Holmes Receptor-Dependent Coronavirus Infection of Dendritic Cells J. Virol., May 15, 2004; 78(10): 5486 - 5490. [Abstract] [Full Text] [PDF]
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A. E. Gelman, J. Zhang, Y. Choi, and L. A. Turka Toll-Like Receptor Ligands Directly Promote Activated CD4+ T Cell Survival J. Immunol., May 15, 2004; 172(10): 6065 - 6073. [Abstract] [Full Text] [PDF]
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R. T. Semnani, M. Law, J. Kubofcik, and T. B. Nutman Filaria-Induced Immune Evasion: Suppression by the Infective Stage of Brugia malayi at the Earliest Host-Parasite Interface J. Immunol., May 15, 2004; 172(10): 6229 - 6238. [Abstract] [Full Text] [PDF]
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A. Tuettenberg, H. Jonuleit, T. Tuting, J. Bruck, V. Biermann, S. Kochanek, J. Knop, and A. H. Enk Early Adenoviral Gene Expression Mediates Immunosuppression by Transduced Dendritic Cell (DC): Implications for Immunotherapy Using Genetically Modified DC J. Immunol., February 1, 2004; 172(3): 1524 - 1530. [Abstract] [Full Text] [PDF]
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T. Kikuchi, T. Kobayashi, K. Gomi, T. Suzuki, Y. Tokue, A. Watanabe, and T. Nukiwa Dendritic Cells Pulsed with Live and Dead Legionella pneumophila Elicit Distinct Immune Responses J. Immunol., February 1, 2004; 172(3): 1727 - 1734. [Abstract] [Full Text] [PDF]
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G. S. Taylor, T. A. Haigh, N. H. Gudgeon, R. J. Phelps, S. P. Lee, N. M. Steven, and A. B. Rickinson Dual Stimulation of Epstein-Barr Virus (EBV)-Specific CD4+- and CD8+-T-Cell Responses by a Chimeric Antigen Construct: Potential Therapeutic Vaccine for EBV-Positive Nasopharyngeal Carcinoma J. Virol., January 15, 2004; 78(2): 768 - 778. [Abstract] [Full Text] [PDF]
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I. E. Vincent, C. P. Carrasco, B. Herrmann, B. M. Meehan, G. M. Allan, A. Summerfield, and K. C. McCullough Dendritic Cells Harbor Infectious Porcine Circovirus Type 2 in the Absence of Apparent Cell Modulation or Replication of the Virus J. Virol., December 15, 2003; 77(24): 13288 - 13300. [Abstract] [Full Text] [PDF]
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J. F. Fonteneau, D. G. Kavanagh, M. Lirvall, C. Sanders, T. L. Cover, N. Bhardwaj, and M. Larsson Characterization of the MHC class I cross-presentation pathway for cell-associated antigens by human dendritic cells Blood, December 15, 2003; 102(13): 4448 - 4455. [Abstract] [Full Text] [PDF]
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P. Sarobe, J. J. Lasarte, A. Zabaleta, L. Arribillaga, A. Arina, I. Melero, F. Borras-Cuesta, and J. Prieto Hepatitis C Virus Structural Proteins Impair Dendritic Cell Maturation and Inhibit In Vivo Induction of Cellular Immune Responses J. Virol., October 15, 2003; 77(20): 10862 - 10871. [Abstract] [Full Text] [PDF]
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S. Gredmark and C. Soderberg-Naucler Human Cytomegalovirus Inhibits Differentiation of Monocytes into Dendritic Cells with the Consequence of Depressed Immunological Functions J. Virol., October 15, 2003; 77(20): 10943 - 10956. [Abstract] [Full Text] [PDF]
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X. Wang, M. Messerle, R. Sapinoro, K. Santos, P. K. Hocknell, X. Jin, and S. Dewhurst Murine Cytomegalovirus Abortively Infects Human Dendritic Cells, Leading to Expression and Presentation of Virally Vectored Genes J. Virol., July 1, 2003; 77(13): 7182 - 7192. [Abstract] [Full Text] [PDF]
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V. Vezys and L. Lefrancois Cutting Edge: Inflammatory Signals Drive Organ-Specific Autoimmunity to Normally Cross-Tolerizing Endogenous Antigen J. Immunol., December 15, 2002; 169(12): 6677 - 6680. [Abstract] [Full Text] [PDF]
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Z. Humlova, M. Vokurka, M. Esteban, and Z. Melkova Vaccinia virus induces apoptosis of infected macrophages J. Gen. Virol., November 1, 2002; 83(11): 2821 - 2832. [Abstract] [Full Text] [PDF]
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Z. Hel, J. Nacsa, E. Tryniszewska, W.-P. Tsai, R. W. Parks, D. C. Montefiori, B. K. Felber, J. Tartaglia, G. N. Pavlakis, and G. Franchini Containment of Simian Immunodeficiency Virus Infection in Vaccinated Macaques: Correlation with the Magnitude of Virus-Specific Pre- and Postchallenge CD4+ and CD8+ T Cell Responses J. Immunol., November 1, 2002; 169(9): 4778 - 4787. [Abstract] [Full Text] [PDF]
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L. V. Overtvelt, M. Andrieu, V. Verhasselt, F. Connan, J. Choppin, V. Vercruysse, M. Goldman, A. Hosmalin, and B. Vray Trypanosoma cruzi down-regulates lipopolysaccharide-induced MHC class I on human dendritic cells and impairs antigen presentation to specific CD8+ T lymphocytes Int. Immunol., October 1, 2002; 14(10): 1135 - 1144. [Abstract] [Full Text] [PDF]
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S. C. Fausch, D. M. Da Silva, M. P. Rudolf, and W. M. Kast Human Papillomavirus Virus-Like Particles Do Not Activate Langerhans Cells: A Possible Immune Escape Mechanism Used by Human Papillomaviruses J. Immunol., September 15, 2002; 169(6): 3242 - 3249. [Abstract] [Full Text] [PDF]
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M. Kakimoto, A. Hasegawa, S. Fujita, and M. Yasukawa Phenotypic and Functional Alterations of Dendritic Cells Induced by Human Herpesvirus 6 Infection J. Virol., September 11, 2002; 76(20): 10338 - 10345. [Abstract] [Full Text] [PDF]
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L. Li, D. Liu, L. Hutt-Fletcher, A. Morgan, M. G. Masucci, and V. Levitsky Epstein-Barr virus inhibits the development of dendritic cells by promoting apoptosis of their monocyte precursors in the presence of granulocyte macrophage-colony-stimulating factor and interleukin-4 Blood, May 15, 2002; 99(10): 3725 - 3734. [Abstract] [Full Text] [PDF]
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J. R. Currier, M. deSouza, P. Chanbancherd, W. Bernstein, D. L. Birx, and J. H. Cox Comprehensive Screening for Human Immunodeficiency Virus Type 1 Subtype-Specific CD8 Cytotoxic T Lymphocytes and Definition of Degenerate Epitopes Restricted by HLA-A0207 and -CW0304 Alleles J. Virol., April 16, 2002; 76(10): 4971 - 4986. [Abstract] [Full Text] [PDF]
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P. Sarobe, J. J. Lasarte, N. Casares, A. Lopez-Diaz de Cerio, E. Baixeras, P. Labarga, N. Garcia, F. Borras-Cuesta, and J. Prieto Abnormal Priming of CD4+ T Cells by Dendritic Cells Expressing Hepatitis C Virus Core and E1 Proteins J. Virol., April 16, 2002; 76(10): 5062 - 5070. [Abstract] [Full Text] [PDF]
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M. Moutaftsi, A. M. Mehl, L. K. Borysiewicz, and Z. Tabi Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells Blood, April 15, 2002; 99(8): 2913 - 2921. [Abstract] [Full Text] [PDF]
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M. Lechmann, D. J.E.B. Krooshoop, D. Dudziak, E. Kremmer, C. Kuhnt, C. G. Figdor, G. Schuler, and A. Steinkasserer The Extracellular Domain of CD83 Inhibits Dendritic Cell-mediated T Cell Stimulation and Binds to a Ligand on Dendritic Cells J. Exp. Med., December 17, 2001; 194(12): 1813 - 1821. [Abstract] [Full Text] [PDF]
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Z. Hel, W.-P. Tsai, A. Thornton, J. Nacsa, L. Giuliani, E. Tryniszewska, M. Poudyal, D. Venzon, X. Wang, J. Altman, et al. Potentiation of Simian Immunodeficiency Virus (SIV)-Specific CD4+ and CD8+ T Cell Responses by a DNA-SIV and NYVAC-SIV Prime/Boost Regimen J. Immunol., December 15, 2001; 167(12): 7180 - 7191. [Abstract] [Full Text] [PDF]
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 C. W. Cutler, R. Jotwani, and B. Pulendran Dendritic Cells: Immune Saviors or Achilles' Heel? Infect. Immun., August 1, 2001; 69(8): 4703 - 4708. [Full Text] [PDF]
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Z. Mikloska, L. Bosnjak, and A. L. Cunningham Immature Monocyte-Derived Dendritic Cells Are Productively Infected with Herpes Simplex Virus Type 1 J. Virol., July 1, 2001; 75(13): 5958 - 5964. [Abstract] [Full Text] [PDF]
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M. P. Rudolf, S. C. Fausch, D. M. Da Silva, and W. M. Kast Human Dendritic Cells Are Activated by Chimeric Human Papillomavirus Type-16 Virus-Like Particles and Induce Epitope-Specific Human T Cell Responses In Vitro J. Immunol., May 15, 2001; 166(10): 5917 - 5924. [Abstract] [Full Text] [PDF]
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P. Lenz, P. M. Day, Y.-Y. S. Pang, S. A. Frye, P. N. Jensen, D. R. Lowy, and J. T. Schiller Papillomavirus-Like Particles Induce Acute Activation of Dendritic Cells J. Immunol., May 1, 2001; 166(9): 5346 - 5355. [Abstract] [Full Text] [PDF]
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C. Bonini, S. P. Lee, S. R. Riddell, and P. D. Greenberg Targeting Antigen in Mature Dendritic Cells for Simultaneous Stimulation of CD4+ and CD8+ T Cells J. Immunol., April 15, 2001; 166(8): 5250 - 5257. [Abstract] [Full Text] [PDF]
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J. Engelmayer, M. Larsson, A. Lee, M. Lee, W. I. Cox, R. M. Steinman, and N. Bhardwaj Mature Dendritic Cells Infected with Canarypox Virus Elicit Strong Anti-Human Immunodeficiency Virus CD8+ and CD4+ T-Cell Responses from Chronically Infected Individuals J. Virol., March 1, 2001; 75(5): 2142 - 2153. [Abstract] [Full Text]
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L.-J. Ho, J.-J. Wang, M.-F. Shaio, C.-L. Kao, D.-M. Chang, S.-W. Han, and J.-H. Lai Infection of Human Dendritic Cells by Dengue Virus Causes Cell Maturation and Cytokine Production J. Immunol., February 1, 2001; 166(3): 1499 - 1506. [Abstract] [Full Text] [PDF]
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J. P. Gardner, I. Frolov, S. Perri, Y. Ji, M. L. MacKichan, J. zur Megede, M. Chen, B. A. Belli, D. A. Driver, S. Sherrill, et al. Infection of Human Dendritic Cells by a Sindbis Virus Replicon Vector Is Determined by a Single Amino Acid Substitution in the E2 Glycoprotein J. Virol., December 15, 2000; 74(24): 11849 - 11857. [Abstract] [Full Text]
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R. Ignatius, M. Marovich, E. Mehlhop, L. Villamide, K. Mahnke, W. I. Cox, F. Isdell, S. S. Frankel, J. R. Mascola, R. M. Steinman, et al. Canarypox Virus-Induced Maturation of Dendritic Cells Is Mediated by Apoptotic Cell Death and Tumor Necrosis Factor Alpha Secretion J. Virol., December 1, 2000; 74(23): 11329 - 11338. [Abstract] [Full Text]
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A. Granelli-Piperno, L. Zhong, P. Haslett, J. Jacobson, and R. M. Steinman Dendritic Cells, Infected with Vesicular Stomatitis Virus-Pseudotyped HIV-1, Present Viral Antigens to CD4+ and CD8+ T Cells from HIV-1-Infected Individuals J. Immunol., December 1, 2000; 165(11): 6620 - 6626. [Abstract] [Full Text] [PDF]
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C. Meyer zum Buschenfelde, N. Nicklisch, S. Rose-John, C. Peschel, and H. Bernhard Generation of Tumor-Reactive CTL Against the Tumor-Associated Antigen HER2 Using Retrovirally Transduced Dendritic Cells Derived from CD34+ Hemopoietic Progenitor Cells J. Immunol., October 1, 2000; 165(7): 4133 - 4140. [Abstract] [Full Text] [PDF]
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M. Kruse, O. Rosorius, F. Krätzer, G. Stelz, C. Kuhnt, G. Schuler, J. Hauber, and A. Steinkasserer Mature Dendritic Cells Infected with Herpes Simplex Virus Type 1 Exhibit Inhibited T-Cell Stimulatory Capacity J. Virol., August 1, 2000; 74(15): 7127 - 7136. [Abstract] [Full Text]
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C. S. Subauste and M. Wessendarp Human Dendritic Cells Discriminate Between Viable and Killed Toxoplasma gondii Tachyzoites: Dendritic Cell Activation After Infection with Viable Parasites Results in CD28 and CD40 Ligand Signaling That Controls IL-12-Dependent and -Independent T Cell Production of IFN-{gamma} J. Immunol., August 1, 2000; 165(3): 1498 - 1505. [Abstract] [Full Text] [PDF]
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C. Munz, K. L. Bickham, M. Subklewe, M. L. Tsang, A. Chahroudi, M. G. Kurilla, D. Zhang, M. O'Donnell, and R. M. Steinman Human Cd4+ T Lymphocytes Consistently Respond to the Latent Epstein-Barr Virus Nuclear Antigen Ebna1 J. Exp. Med., May 15, 2000; 191(10): 1649 - 1660. [Abstract] [Full Text] [PDF]
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 B. Berwin, R. C. Reed, and C. V. Nicchitta Virally Induced Lytic Cell Death Elicits the Release of Immunogenic GRP94/gp96 J. Biol. Chem., June 8, 2001; 276(24): 21083 - 21088. [Abstract] [Full Text] [PDF]
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