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Microenvironment and Immunology

Chemotherapy Induces Intratumoral Expression of Chemokines in Cutaneous Melanoma, Favoring T-cell Infiltration and Tumor Control

Michelle Hong, Anne-Laure Puaux, Caleb Huang, Laure Loumagne, Charlene Tow, Charles Mackay, Masashi Kato, Armelle Prévost-Blondel, Marie-Françoise Avril, Alessandra Nardin and Jean-Pierre Abastado
Michelle Hong
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Anne-Laure Puaux
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Caleb Huang
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Laure Loumagne
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Charlene Tow
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Charles Mackay
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Masashi Kato
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Armelle Prévost-Blondel
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Marie-Françoise Avril
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Alessandra Nardin
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Jean-Pierre Abastado
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DOI: 10.1158/0008-5472.CAN-11-1466 Published November 2011
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    Figure 1.

    Low T-cell infiltration of RETAAD cutaneous metastasis. A, cutaneous (n = 22) and visceral (n = 4) tumors were collected from 9 RETAAD mice and analyzed for the presence of CD3+ cells by flow cytometry. Data represent the percentage of CD3+ cells among live CD45+ cells. Mann–Whitney U test, 2-tailed. B, immunofluorescence labeling of CD3 (pink) in RETAAD cutaneous (left) and reproductive tract (right) tumors. Scale bar, 50 μm. Quantification of tumor-infiltrating T cells detected by immunofluorescence in cutaneous (n = 4) and visceral (n = 6) tumors. Data represent the number of T cells per field of view (FOV). Mann–Whitney U test, 2-tailed. C, expression of T-cell markers (Cd3g, Cd4, and Cd8a) and effector molecules (Ifng, Prf1b, and Gzmb) was measured in cutaneous (n = 20) and visceral (n = 10) tumors. Unpaired t test, 2-tailed. D, inverse correlation between the percentages of CD3+, CD4+, and CD8+ T cells and cutaneous tumor weight (n = 12). Pearson correlation, 1-tailed. Statistical significance between groups is represented by *, P < 0.05; **, P < 0.01; ***, P < 0.001. Cut, cutaneous; Vis, visceral.

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    Figure 2.

    RETAAD T cells infiltrate exogenous B16 skin tumors. B16 cells were injected subcutaneously into the right flank of tumor-bearing RETAAD mice. Fourteen days after injection, transplanted B16 and autochthonous RETAAD skin tumors from the same mice were analyzed for T-cell infiltration. A, flow cytometric comparison of T-cell infiltrates in transplanted B16 (n = 4) and autochthonous RETAAD (n = 6) skin tumors from the same mice. Data show the percentages of CD3+, CD4+, and CD8+ T cells among total live cells [4′,6-diamidino-2-phenylindole (DAPI)-]. Mann–Whitney U test, 2-tailed. Statistical significance between groups is represented by **, P < 0.01. B, intratumoral expression of chemokine and chemokine receptor genes. Volcano plot shows fold change in gene expression in B16 skin tumors grown in RETAAD mice (n = 3) compared with autochthonous RETAAD skin tumors (n = 5). Open squares represent chemokine genes with greater than 2-fold differential expression and P < 0.05. Horizontal line shows P = 0.05. Vertical line represents 10-fold increase in B16 compared with RETAAD tumors. L2, L3, L4, L7, X5, X9, and X10 indicate the chemokine genes Ccl2, Ccl3, Ccl4, Ccl7, Cxcl5, Cxcl9, and Cxcl10, respectively. C, surface expression of chemokine receptors on CD4+ and CD8+ T cells was analyzed in peripheral blood collected from RETAAD mice. Data are representative of 8 mice analyzed. Isotype control, gray filled histograms; naive (CD44− CD62L+), black solid line; effector memory (CD44+ CD62L−), red solid line; central memory (CD44+ CD62L+), green solid line. D, percentages of CXCR3+ cells within CD4+ and CD8+ T cell subsets of RETAAD mice (n = 8). CM, central memory; EM, effector memory.

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    Figure 3.

    Chemokine induces T-cell infiltration in RETAAD cutaneous tumors and inhibits tumor growth. Cxcl9-encoding or control plasmids (5 μg) were injected into established RETAAD cutaneous tumors 3 times on alternate days. On day 6, tumors were analyzed for T-cell infiltration. A, the percentages of CD4+ and CD8+ T cells among total live cells in Cxcl9-treated tumors (n = 5) and control tumors (n = 7) were determined using flow cytometry. Mann–Whitney U test, 1-tailed. B, relative expression of several effector molecules, that is, Ifng, Gzma, and Gzmb in Cxcl9-treated (n = 8) and control tumors (n = 5). Unpaired t test, 1-tailed. C, percentage of dead tumor cells (CD45−DAPI+/CD45−) in Cxcl9-treated (n = 5) and control (n = 5) tumors. Mann–Whitney U test, 1-tailed. D–F, Melan-ret cells were transfected with a CXCL9-encoding plasmid and injected subcutaneously into both flanks of C57BL/6 mice (n = 5). D, tumor size was measured every 2 to 3 days. Statistical analysis was carried out using 2-way ANOVA, 2-tailed. At necropsy on day 16, Cxcl9-transfected tumors (n = 3) and control tumors (n = 5) were collected and weighed. Mann–Whitney U test, 1-tailed. E, the expression of Cxcl9 and Cd3g was measured by qRT-PCR in Cxcl9-transfected and control tumors. Unpaired t test, 2-tailed. F, tumor growth curves and tumor weights of Cxcl9-transfected (n = 5) and control (n = 5) tumors in Rag1−/− mice. Two-way ANOVA, 2-tailed and Mann–Whitney U test, 1-tailed. G and H, Ccl5 synergizes with Cxcl9 to recruit T cells. RETAAD cutaneous tumors were injected with 2.5 μg plasmid DNA encoding Ccl5 (n = 10) or Cxcl9 (n = 11), a combination of both plasmids (n = 15), or control plasmid (n = 9) on alternate days for 5 days. On day 6, tumors were analyzed for T-cell infiltration. G, the percentages of CD3+ T cells measured by flow cytometry were compared using Kruskal–Wallis test. The expression of Cd3g was compared by ANOVA and Bonferroni multiple comparison posttest. H, surface expression of CCR5 on CD4+ and CD8+ T cells in peripheral blood (n = 6) and TIL (n = 16). Mann–Whitney U test, 1-tailed. All data are representative of 3 independent experiments conducted. Statistical differences between groups are represented by ***, P < 0.001; **, P < 0.01; *, P < 0.05; ns, nonsignificant. C, control plasmid; Tr, tumors injected with the Cxcl9 plasmid; Tf, Melan-ret transfected with Cxcl9 plasmid.

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    Figure 4.

    Chemotherapeutic drugs induce chemokine expression in human melanoma cells in vitro. Temozolomide, cisplatin, and dacarbazine were tested on 5 different human melanoma cell lines (HTB-71, M88, M102, M131, and M134) for their effect on CCL5, CXCL9, and CXCL10 production. A, CCL5, CXCL9, and CXCL10 expression was measured by qRT-PCR in cells treated with either temozolomide (100 μg/mL), cisplatin (10 μg/mL), or dacarbazine (100 μg/mL) for 72 hours. Data show the fold change in chemokine expression in drug-treated cells over control cells. B, M102 cells were treated with increasing dose of temozolomide (0, 10, 20, 40, 60, 80, and 100 μg/mL) or cisplatin (0, 1.3, 2.5, 5, and 10 μg/mL) for 72 hours and the expression of CCL5, CXCL9, and CXCL10 was measured by qRT-PCR. Comparisons were done using 2-way ANOVA. C, kinetics of CCL5, CXCL9, and CXCL10 expression in M102 cells at 6, 12, 24, 48, and 72 hours after temozolomide (100 μg/mL) and cisplatin (10 μg/mL) treatment. Comparisons were done using 2-way ANOVA. D, concentrations of 40 different cytokines, chemokines, angiogenic factors, and growth factors in the supernatants of drug-treated and control cells were determined using multiplex immunobeads technology. Data are presented as fold change in protein production from drug-treated cells compared with control cells. Only cytokines/chemokines with 9-fold or more increase in secretion after drug treatment and P value lesser than 0.05 are represented from temozolomide treatment group. Mann–Whitney U test, 1-tailed.

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    Figure 5.

    Temozolomide induces intratumoral expression of chemokines and promotes T-cell infiltration. Tumor-bearing Rag1−/− mice were treated intraperitoneally with 2 mg temozolomide (TMZ; n = 10) or DMSO (n = 8) for 2 consecutive days and then injected intravenously with 107 in vitro activated T cells. A, intratumoral expression of chemokines was analyzed by qRT-PCR. Unpaired t test, 1-tailed. B, T-cell infiltration was measured in individual tumors by flow cytometry. Data show the percentage of CD3+ cells among live CD45+ cells. Mann–Whitney U test, 1-tailed. Temozolomide enhanced intratumoral T-cell infiltration. Anti-CXCR3 blocking antibody (TMZ + α-CXCR3) abolished chemotherapy-induced infiltration of T cells. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

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    Figure 6.

    Enhanced chemokine expression in human melanoma skin tumors after chemotherapy correlates with increased T-cell infiltration, tumor control, and patient survival. A total of 33 cutaneous melanoma tumors from 13 stage III or IV patients were collected before and after chemotherapy. Gene expression was measured by qRT-PCR. A, CD4 or CD8A expression correlates with CCL5, CXCL9, and CXCL10 expression in the tumors. Spearman correlation, 1-tailed with Bonferroni correction for multiple testing. B, the expression of CD4 and CD8A was compared between tumors with high or low expression of CCL5 and CXCR3 ligands. 0, CCL5lo CXCR3 ligandslo; 1, CCL5hi or CXCR3 ligandshi; 2/3, CCL5hi and CXCR3 ligandshi. One-way ANOVA. C and D, intratumoral expression of CCL5, CXCL9, and CXCR3 as well as CD4 and CD8A was compared between cutaneous tumors before (pre; n = 13) and after chemotherapy (post; n = 22). Tumors collected after treatment were divided into chemotherapy resistant (CT-R; n = 12) or chemotherapy sensitive (CT-S; n = 10). Differential gene expression between tumor samples collected before treatment and chemotherapy-sensitive tumors was assessed by 1-tailed t test on log-transformed expression values. E, Kaplan–Meier analysis of patient survival with high- or low- intratumoral chemokine expression after chemotherapy. Statistical significance between groups is presented as *, P < 0.05; **, P < 0.01; ***, P < 0.001.

Tables

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  • Table 1.

    Multiplex analysis of soluble factors secreted by M102 cell line after chemotherapeutic drug treatment

    AnalyteMean ± SD (pg/mL; temozolomide)Mean ± SD (pg/mL; DMSO)Fold increasePMean ± SD (pg/mL; cisplatin)Mean ± SD (pg/mL; DMF)Fold increaseP
    b-NGFNDNDNANANDNDNANA
    CTACKNDNDNANANDNDNANA
    Eotaxin42.1 ± 16.497.3 ± 89.80.430.2584.5 ± 101119.3 ± 133.60.710.35
    FGF basic41.5 ± 12.722.3 ± 18.71.860.1044.8 ± 16.742.9 ± 451.040.35
    G-CSFNDNDNANANDNDNANA
    GM-CSF100.1 ± 73.875 ± 81.51.330.2058.5 ± 58.7124.6 ± 166.80.470.50
    GROα3,776 ± 977.81,009 ± 377.13.740.05309.8 ± 87.4293.9 ± 198.71.050.35
    HGFNDNDNANANDNDNANA
    IFN-α2NDNDNANANDNDNANA
    IFNγ254 ± 199.3319.6 ± 276.40.790.3583.1 ± 42.4700.5 ± 776.80.120.10
    IL-1αNDNDNANANDNDNANA
    IL-1βNDNDNANANDNDNANA
    IL-1ra200.2 ± 162.1221.4 ± 184.10.90.41131.3 ± 118.1298 ± 256.40.460.35
    IL-2NDNDNANANDNDNANA
    IL-2raNDNDNANANDNDNANA
    IL-3NDNDNANANDNDNANA
    IL-4NDNDNANANDNDNANA
    IL-5NDNDNANANDNDNANA
    IL-6NDNDNANANDNDNANA
    IL-7NDNDNANANDNDNANA
    IL-8/CXCL883,229 ± 67,8107,869 ± 2,35410.580.0511,343 ± 1,8562,144 ± 1,2435.290.05
    IL-975.3 ± 50.971.5 ± 55.50.920.5010.2 ± 1.5113 ± 117.10.090.05
    IL-1019.4 ± 16.248.1 ± 29.40.40.1010.3 ± 765.8 ± 710.160.10
    IL-12p40NDNDNANANDNDNANA
    IL-12p7088 ± 87.891.6 ± 77.61.130.4123.4 ± 19.4143.6 ± 162.10.160.10
    IL-13NDNDNANANDNDNANA
    IL-15NDNDNANANDNDNANA
    IL-1640.8 ± 34.756.1 ± 62.30.730.5041.8 ± 35.1103 ± 123.30.410.35
    IL-17103.8 ± 97130.1 ± 147.40.80.50114.4 ± 125.8125.6 ± 109.80.910.50
    IL-18NDNDNANANDNDNANA
    IP-10/CXCL103,810 ± 1,122268.7 ± 268.814.180.05667.3 ± 215.3115.8 ± 100.25.760.05
    LIF13,478 ± 11,8436,288 ± 5,5082.140.25188.1 ± 16.42,258 ± 383.40.080.05
    MCP-1/CCL2522.8 ± 46.85.3 ± 1.698.290.04NDNDNANA
    MCP-3/CCL7NDNDNANANDNDNANA
    M-CSF86.7 ± 75.730.7 ± 35.72.920.17121.4 ± 103.627.7 ± 30.54.380.17
    MIF6,475 ± 522.8246.7 ± 54.926.250.0513,356 ± 3,597874.3 ± 236.815.280.05
    MIG/CXCL947 ± 1.45.1 ± 5.19.170.05NDNDNANA
    MIP-1α/CCL3NDNDNANANDNDNANA
    MIP-1β/CCL4NDNDNANANDNDNANA
    PDGF-bb65.7 ± 44.157 ± 671.150.3522.9 ± 14.493.3 ± 82.60.250.10
    RANTES/CCL5330.4 ± 12.128.7 ± 11.611.50.0529 ± 10.427.3 ± 22.71.060.35
    SCF40.6 ± 35.644.4 ± 40.10.910.5077.2 ± 66.920 ± 28.23.870.27
    SCGF-β1,025 ± 405.71,290 ± 431.50.790.20832.9 ± 226.92,916 ± 2,7900.290.05
    SDF-1αNDNDNANANDNDNANA
    TNF-αNDNDNANANDNDNANA
    TNF-βNDNDNANANDNDNANA
    TRAILNDNDNANANDNDNANA
    VEGF36,847 ± 6,11744,477 ± 33,9650.830.3516,688 ± 5,20655,394 ± 46,3100.30.35

    NOTE: Human melanoma cell line M102 was cultured with temozolomide (100 μg/mL) or cisplatin (10 μg/mL) for 3 days. Supernatants were collected and the concentrations of various soluble factors were analyzed using xMAP multiplex technology. Data show the production of cytokines, chemokines, angiogenic, and growth factors in pg/mL ± SD from the supernatant of drug-treated cells compared with control cells. Results are representative of 3 independent samples analyzed. Secreted factors that are significantly upregulated after drug treatment are indicated in bold.

    Abbreviations: ND, not detected; NA, not available. Mann–Whiney U test, 1-tailed.

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      • Supplementary Figure 1 - PDF file - 782K, CD8+ T cell depletion accelerates the development of visceral tumors but has no effect on cutaneous tumors in RETAAD mice.(A) Development of visceral metastases was followed by PET scan 4 weeks and 8 weeks after initiation of the depletion of CD8+ T cells n=10 as described in (Eyles et al., 2010). Control mice n=9 were injected with rat IgG control. Data shows the percentage of mice with visceral metastases in each group. (B) Skin tumors were detected at necropsy. Data shows the number of skin tumors (left) and the percentage of mice with skin tumors (right). All data represent means � SEM. Results are representative of two independent experiments. C= control group. D= CD8 depleted. Statistical analysis was performed using Mann-Whitney U test, one-tailed.
      • Supplementary Figure 2 - PDF file - 634K, Positive controls for antibody staining. Peripheral blood mononuclear cells were collected from 3 tumor-bearing RETAAD mice and were stained with antibodies against CCR1, CCR2, CCR3 and CCR5. Monocytes, eosinophils and macrophages were used as positive controls for the antibodies CCR1/CCR2, CCR3 and CCR5 respectively.
      • Supplementary Figure 3 - PDF file - 335K, Map of CCL5 and CXCL9 expressing plasmids. The sequences encoding the chemokines were cloned under the control of the CMV promoter (PCMV) upstream of the bovine growth hormone polyadenylation site (BGH pA).
      • Supplementary Figure 4 - PDF file - 436K, Plasmid transfection into cutaneous tumors. (A) Chemokine expression in vivo after Cxcl9 transfection into established RETAAD cutaneous tumors. The expression of Cxcl9 and as a negative control, Cxcl10, relative to Gapdh were analyzed by qRT-PCR in Cxcl9-treated tumors (n=5). Unpaired t-test, one-tailed. *** p < 0.001. C - Control; Tr - Treated. (B) Injection of control plasmid has no effect on T cell infiltration into tumors. Cd3g expression relative to Gapdh was compared between non-injected tumors (NI; n=5) and control plasmid-injected tumors (I; n=7) by qRT-PCR. Statistical analysis was performed using unpaired t-test, one-tailed.
      • Supplementary Figure 5 - PDF file - 487K, Cd3g expression correlates with Ccl5 expression in RETAAD tumors. A total of 37 cutaneous and visceral tumors were collected from 15 tumor-bearing RETAAD mice and analyzed for the expression of Cd3g and Ccl5 by qRT-PCR. Cd3g expression was strongly correlated with Ccl5 expression. Pearson correlation, one-tailed.
      • Supplementary Figure 6 - PDF file - 799K, Ccl5 synergizes with Cxcl9 to recruit T cells. (A) The relative expression of Cd3g analyzed by qRT-PCR in 45 tumors was correlated with the percentage of CD3+ T cells measured by flow cytometry. Pearson's correlation, one-tailed. (B) The percentages of CD4+ and CD8+ T cells over total live cells (DAPI-) were analyzed by flow cytometry in RETAAD cutaneous tumors injected with either control plasmid, plasmid expressing Ccl5, plasmid expressing Cxcl9, or a combination of both plasmids. Statistical analysis was performed using unpaired t-test, one-tailed.
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    Chemotherapy Induces Intratumoral Expression of Chemokines in Cutaneous Melanoma, Favoring T-cell Infiltration and Tumor Control
    Michelle Hong, Anne-Laure Puaux, Caleb Huang, Laure Loumagne, Charlene Tow, Charles Mackay, Masashi Kato, Armelle Prévost-Blondel, Marie-Françoise Avril, Alessandra Nardin and Jean-Pierre Abastado
    Cancer Res November 15 2011 (71) (22) 6997-7009; DOI: 10.1158/0008-5472.CAN-11-1466

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    Chemotherapy Induces Intratumoral Expression of Chemokines in Cutaneous Melanoma, Favoring T-cell Infiltration and Tumor Control
    Michelle Hong, Anne-Laure Puaux, Caleb Huang, Laure Loumagne, Charlene Tow, Charles Mackay, Masashi Kato, Armelle Prévost-Blondel, Marie-Françoise Avril, Alessandra Nardin and Jean-Pierre Abastado
    Cancer Res November 15 2011 (71) (22) 6997-7009; DOI: 10.1158/0008-5472.CAN-11-1466
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