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Vaccines and Antiviral Agents

Antibodies to gp120 and PD-1 Expression on Virus-Specific CD8+ T Cells in Protection from Simian AIDS

Monica Vaccari, Rabih Halwani, L. Jean Patterson, Adriano Boasso, Jennifer Beal, Elzbieta Tryniszewska, Anna Hryniewicz, David Venzon, Elias K. Haddad, Mohamed El-Far, Margherita Rosati, George N. Pavlakis, Barbara K. Felber, Saleh Al-Muhsen, Marjorie Robert-Guroff, Rafick-Pierre Sekaly, Genoveffa Franchini
Monica Vaccari
aAnimal Models & Retroviral Vaccines Section, National Cancer Institute, Bethesda, Maryland, USA
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Rabih Halwani
bPrince Naif Center for Immunology Research and Department of Pediatrics, College of Medicine, King Saud University, Riyadh, Saudi Arabia
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L. Jean Patterson
cImmune Biology of Retroviral Infection Section, National Cancer Institute, Bethesda, Maryland, USA
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Adriano Boasso
dImmunology Section, Imperial College London, Chelsea and Westminster Hospital, London, United Kingdom
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Jennifer Beal
cImmune Biology of Retroviral Infection Section, National Cancer Institute, Bethesda, Maryland, USA
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Elzbieta Tryniszewska
aAnimal Models & Retroviral Vaccines Section, National Cancer Institute, Bethesda, Maryland, USA
eDepartment of Microbiology Diagnostics, Medical University of Bialystok, Bialystok, Poland
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Anna Hryniewicz
aAnimal Models & Retroviral Vaccines Section, National Cancer Institute, Bethesda, Maryland, USA
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David Venzon
gBiostatistics and Data Management Section, National Cancer Institute, Bethesda, Maryland, USA
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Elias K. Haddad
fVaccine & Gene Therapy Institute of Florida, Port St. Lucie, Florida, USA
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Mohamed El-Far
bPrince Naif Center for Immunology Research and Department of Pediatrics, College of Medicine, King Saud University, Riyadh, Saudi Arabia
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Margherita Rosati
hHuman Retrovirus Section, Vaccine Branch, Center for Cancer Research, Frederick National Laboratory for Cancer Research, Frederick, Maryland, USA
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George N. Pavlakis
hHuman Retrovirus Section, Vaccine Branch, Center for Cancer Research, Frederick National Laboratory for Cancer Research, Frederick, Maryland, USA
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Barbara K. Felber
iHuman Retrovirus Pathogenesis Section, Vaccine Branch, Center for Cancer Research, Frederick National Laboratory for Cancer Research, Frederick, Maryland, USA
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Saleh Al-Muhsen
bPrince Naif Center for Immunology Research and Department of Pediatrics, College of Medicine, King Saud University, Riyadh, Saudi Arabia
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Marjorie Robert-Guroff
cImmune Biology of Retroviral Infection Section, National Cancer Institute, Bethesda, Maryland, USA
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Rafick-Pierre Sekaly
fVaccine & Gene Therapy Institute of Florida, Port St. Lucie, Florida, USA
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Genoveffa Franchini
aAnimal Models & Retroviral Vaccines Section, National Cancer Institute, Bethesda, Maryland, USA
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DOI: 10.1128/JVI.02686-12
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    Fig 1

    Clinical and virological outcome of vaccinations. (A) Schematic representation of the immunization regimens. The arrows indicate times of immunizations and of challenge exposure to SIVmac251, performed by the intrarectal route at week 74 in all animals and at week 52 in the 1 × MVA group. (B, C, D, E) Plasma virus levels are presented for each animal. *, identified Mamu-A*01+ macaques. (F, G, H) Comparison of mean virus load in plasma in macaques from the different groups.

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    Fig 2

    Antibody titers and kinetics of CD8+CM9+ T-cell response in the vaccinated macaques. Endpoint antibody titers to p27 Gag (A) and gp120 (B) in the sera of the immunized monkeys. (C) Correlative analysis between the titers of the gp120-binding antibodies in all the vaccinated animals and plasma viral loads at week 6 postinfection. (D to G) Frequency and kinetics of CM9+CD8+ T cells in blood of the macaques during immunization and following challenge exposure to SIVmac251. (H to K) Relative frequency of CD95+CD28− (effector memory [EM] in solid black bars) and CD95+CD28+ (central memory [CM] in white bars) CM9+CD8+ T cells in blood of vaccinated and control macaques following challenge exposure to SIVmac251. The data are shown as means for each group, calculated using the individual frequency of EM or CM on the total Gag-CM9+ memory population.

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    Fig 3

    PD-1 expression on CD8+CM9+ T-cell response in the vaccinated macaques. (A) CFSE gating strategy and mean fluorescence intensity (MFI) of PD-1 expression on nonproliferating CFSEhi CM9+CD8+ T cells from representative macaques. (B to D) PD-1 level of expression on CFSElo or CFSEhi CM9+ CD8+ T cells from animals from the 2 × MVA and 1 × MVA/Ad5 groups were analyzed at week 74 (before challenge) and at weeks 7 and 24 after challenge exposure to SIVmac251. (E) PD-1 expression levels on low and high proliferating CD8+CM9+ T cells in the two groups of vaccinated animals at all time points. The plot includes all the data points, and each dot represents one macaque. (F and G) Frequency of Gag-specific T cells 5 days following stimulation with Gag peptides in the presence (or absence) of anti-PD-L1 blocking antibody; CD8+ T cells (F) and CD4+ T cells (G) are gated on CFSElow cells. (H to J) PD-L1 expression on human mDCs (H) and on pDCs (J) and CD86 expression on human mDCs (I) following in vitro infection with Ad5 or MVA.

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    Fig 4

    Heat map representation of gene expression within CM9+ CD8+ T cells at 24 weeks following challenge. (Upper panel) Genes from representative pathways analyzed with GSEA and displayed as a heat map to demonstrate differential expression between Adv CM9+ and MVA CM9+ cells. Each pathway comprising selected top upregulated genes is represented by a different color. The false color expression in log2 scale is depicted on the right side of the figure. The heat map shows the expression level of each gene (red, upregulated; blue, downregulated). Eight significant pathways are shown (P values < 0.05) (6 upregulated in Ad5 CM9+ samples and 2 upregulated in MVA CM9+ cells), as is a subset of 30 most up- and downregulated genes (22 upregulated in Ad5 CM9+ samples and 8 upregulated in MVA CM9+ samples). (Lower panel) Genes upregulated and downregulated in antigen presentation pathways.

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  • Table 1

    Definition of pathways and genes differentially expressed in Adv versus MVA Tet+ cells

    Pathway or gene nameFunction or description
    Pathways
        HSA04010_MAPK_SIGNALING_PATHWAYGenes involved in MAPK signaling pathway
        HSA04540_GAP_JUNCTIONGenes involved in gap junction
        M_2.9_ERK_TRANSACTIVATION_CYTOSKELETAL_MAPK_JNKProgressively downregulated through 12 h following treatment of WS1 human skin fibroblasts with UVC at a high dose
        UVC_HIGH_D4_DNDownregulated at any time point following treatment of XPB/CS fibroblasts with 3 J/m2 UVC
        UVC_XPCS_ALL_DNDownregulated at 4 h following treatment of XPB/CS fibroblasts with 3 J/m2 UVC (genes involved in apoptosis)
        UVC_XPCS_4HR_DNUpregulated in mouse hematopoietic stem cells
        HSC_HSCANDPROGENITORS_FETALGenes involved in antigen processing and presentation
        HSA04612_ANTIGEN_PROCESSING_AND_PRESENTATIONGenes involved in MAPK signaling pathway
    Genes
        Upregulated in Tet+ MVA compared to Tet+ Adv
            TAPBPRequired for MHC formation
            CIITAInvolved in transcription of HLA class II and important for antigen presentation
            HLA-DQB1Involved in transcription of HLA class II and important for antigen presentation
            HLA-DMBHelps to load HLA class II
            IRAK1
            IGBP1B-cell activation
            PSMC5Important for MHC-I processing
            CCND2Important for cell division
        Uppregulated in Tet+ Adv compared to Tet+ MVA
            MAP3K4Apoptosis
            JUNApoptosis
            ATF4Apoptosis
            ATF2Apoptosis
            RAP1APlays a role in apoptosis
            DUSP5Apoptosis
            TAOK1Apoptosis
            PTENTumor suppressor
            ITPR1Apoptotic gene
            TUBB2B
            PRKACBApoptosis
            PRKCB1Apoptotic gene
            SOS1Differential role
            UBE2G1Ubiquitination
            POGZGene suppressor
            ARID5BGene repression
            PPP2R5CNegative control of cell division
            TRIM33Gene repression
            SPENGene transcription repression
            CDYLOncogene repression
            CNOT4Transcription repression
            CBLBAnti-inflammatory

Additional Files

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    Files in this Data Supplement:

    • Supplemental file 1 -

      Fig. S1 (Proliferative responses to the SIVmac251 gp120 Env and p27 Gag proteins before SIV challenge in the 2xMVA and 1xMVA/Ad5 groups; γ-ELISPOT responses measured in blood using the peptide pool derived from the entire SIVmac239 Gag, Env, and Nef proteins; intracellular cytokine production (IFN-γ or IL-2) in PBMCs at 2 weeks following the last immunization with MVA or Ad5 in CD8+ and CD4+ T-cells; plasma virus levels presented for each animal in Mamu-A*01+ macaques for each group.)

      Fig. S2 (Upregulation and downregulation of genes involved in T-cell signaling in NFAT and CD28 cells.)

      PDF, 835K

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Antibodies to gp120 and PD-1 Expression on Virus-Specific CD8+ T Cells in Protection from Simian AIDS
Monica Vaccari, Rabih Halwani, L. Jean Patterson, Adriano Boasso, Jennifer Beal, Elzbieta Tryniszewska, Anna Hryniewicz, David Venzon, Elias K. Haddad, Mohamed El-Far, Margherita Rosati, George N. Pavlakis, Barbara K. Felber, Saleh Al-Muhsen, Marjorie Robert-Guroff, Rafick-Pierre Sekaly, Genoveffa Franchini
Journal of Virology Feb 2013, 87 (6) 3526-3537; DOI: 10.1128/JVI.02686-12

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Antibodies to gp120 and PD-1 Expression on Virus-Specific CD8+ T Cells in Protection from Simian AIDS
Monica Vaccari, Rabih Halwani, L. Jean Patterson, Adriano Boasso, Jennifer Beal, Elzbieta Tryniszewska, Anna Hryniewicz, David Venzon, Elias K. Haddad, Mohamed El-Far, Margherita Rosati, George N. Pavlakis, Barbara K. Felber, Saleh Al-Muhsen, Marjorie Robert-Guroff, Rafick-Pierre Sekaly, Genoveffa Franchini
Journal of Virology Feb 2013, 87 (6) 3526-3537; DOI: 10.1128/JVI.02686-12
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