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Transient Complement Inhibition Promotes a Tumor-Specific Immune Response through the Implication of Natural Killer Cells

Valérie Janelle, Marie-Pierre Langlois, Esther Tarrab, Pascal Lapierre, Laurent Poliquin and Alain Lamarre
Valérie Janelle
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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Marie-Pierre Langlois
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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Esther Tarrab
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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Pascal Lapierre
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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Laurent Poliquin
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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Alain Lamarre
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
1Immunovirology Laboratory, Institut national de la recherche scientifique, INRS-Institut Armand-Frappier, Laval; and 2Biomed Research Center, Department of Biology, Université du Québec à Montréal, Montréal, Québec, Canada
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DOI: 10.1158/2326-6066.CIR-13-0173 Published March 2014
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    Figure 1.

    Effect of CVF treatment on B16 tumor growth and immune cell infiltration. C57BL/6 mice were injected s.c. with B16 (day 0) and CVF was administered by i.p. injection on day 6. A, tumor growth was measured at indicated time points. Data show the mean ± SEM and are representative of two independent experiments. **, P < 0.01. B, 9 days following CVF treatment, tumors and spleens were harvested and total tumor CD45+ cell numbers were determined; C, immune cell subpopulation proportions of CD4+ T cells (CD4+CD25−), Tregs (CD4+CD25+), CD8+ T cells, B cells (B220+), NK (NKp46+), MDSC (Gr1+CD11b+), neutrophils (Gr1+CD11b−), dendritic cells (Gr1−CD11b+CD11c+), and macrophages (Gr1−CD11b+F4/80+) were determined. DC, dendritic cells; MDSC, myeloid-derived suppressor cells; NT, not treated.

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    Figure 2.

    Decomplementation increases NK cell availability without affecting their effector function. B16gp33-bearing mice were treated or not with CVF. On day 9 following treatment, spleens and tumors were harvested. A, percentage of NK cells among CD45+ cells. Mean ± SEM are shown (n = 9). ***, P < 0.001. B, NK degranulation assay in YAC-1 cocultures (10:1 effector–target ratio) with or without PMA–ionomycin. Data are the mean ± SEM of three independent experiments (n = 9). NT, not treated.

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    Figure 3.

    Increased systemic T-cell activation following CVF treatment. A, spleens and draining lymph nodes were harvested 9 days following CVF treatment, and dendritic cell activation was assessed by CD11c and CD86 staining. Data are the mean ± SEM of two independent experiments (n = 6). B, T-cell activation was assessed by CD62L and CD44 staining on spleens and tumors. Naïve (CD62L+CD44−), effector/effector memory (CD62L−), and central memory T cells (CD62L+CD44+) are shown. Data are the mean ± SEM of three independent experiments (n = 9). *, P < 0.05; **, P < 0.01. NT, not treated.

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    Figure 4.

    Influence of NK cells on CVF therapy. A, C57BL/6 mice were injected s.c. with B16 cells (n = 6–8), NK depleted or not at day 4 and treated or not with CVF at day 6. Tumor growth was measured at indicated time points. Data show the mean ± SEM and are representative of two independent experiments. *, P < 0.05; **, P < 0.01. B, C57BL/6 mice were injected s.c. with B16gp33 cells, NK depleted or not at day 4 and treated or not with CVF at day 6. Nine days following CVF treatment, spleens were harvested and an ex vivo stimulation with the gp33 (KAVYNFATC) peptide was performed to analyze cytokine secretion and C, degranulation. Data are the mean ± SEM of two independent experiments (n = 6). D, the proposed model for the influence of complement proteins and NK cells in the B16 melanoma model. Inhibition of the complement system by CVF allows for increased NK cell availability in tumor tissues. This expanded proportion of NK cells leads to increased tumor cell lysis and antigen release, thus facilitating the activation of tumor-specific CD8+ T lymphocytes. Inhibition of complement proteins also acts on MDSC and limits the immunosuppressive tumor microenvironment, leading to increased CTL activation. iDC, immature dendritic cell; mDC, mature dendritic cell; NT, not treated.

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    • Supplementary Figure Legend - PDF file - 86K
    • Supplementary Figure 1 - PDF file - 24K, Supplementary Figure 1. Complement system inhibition by CVF.
    • Supplementary Figure 2 - PDF file - 26K, Supplemental Figure 2. MDSC proportions following CVF treatment.
    • Supplementary Figure 3 - PDF file - 135K, Supplementary Figure 3. Effectiveness of NK cell depletion.
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Cancer Immunology Research: 2 (3)
March 2014
Volume 2, Issue 3
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Transient Complement Inhibition Promotes a Tumor-Specific Immune Response through the Implication of Natural Killer Cells
Valérie Janelle, Marie-Pierre Langlois, Esther Tarrab, Pascal Lapierre, Laurent Poliquin and Alain Lamarre
Cancer Immunol Res March 1 2014 (2) (3) 200-206; DOI: 10.1158/2326-6066.CIR-13-0173

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Transient Complement Inhibition Promotes a Tumor-Specific Immune Response through the Implication of Natural Killer Cells
Valérie Janelle, Marie-Pierre Langlois, Esther Tarrab, Pascal Lapierre, Laurent Poliquin and Alain Lamarre
Cancer Immunol Res March 1 2014 (2) (3) 200-206; DOI: 10.1158/2326-6066.CIR-13-0173
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