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Original Research

CCL3 augments tumor rejection and enhances CD8+ T cell infiltration through NK and CD103+ dendritic cell recruitment via IFNγ

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Article: e1393598 | Received 06 Sep 2017, Accepted 13 Oct 2017, Published online: 20 Nov 2017

References

  • Dunn GP, Old LJ, Schreiber RD The three Es of cancer immunoediting. Annu Rev Immunol. 2004;22:329–360. doi:10.1146/annurev.immunol.22.012703.104803. PMID:15032581.
  • Nakashima E et al. A candidate for cancer gene therapy: MIP-1 alpha gene transfer to an adenocarcinoma cell line reduced tumorigenicity and induced protective immunity in immunocompetent mice. Pharm Res. 1996;13:1896–1901. doi:10.1023/A:1016057830271. PMID:8987092.
  • He S, Wang L, Wu Y, Li D, Zhang Y CCL3 and CCL20-recruited dendritic cells modified by melanoma antigen gene-1 induce anti-tumor immunity against gastric cancer ex vivo and in vivo. J Exp Clin Cancer Res. 2010;29:37. doi:10.1186/1756-9966-29-37. PMID:20420712.
  • Spranger S, Bao R, Gajewski TF Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity. Nature. 2015;523:231–235. doi:10.1038/nature14404. PMID:25970248.
  • Harlin H et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69:3077–3085. doi:10.1158/0008-5472.CAN-08-2281. PMID:19293190.
  • Castellino F et al. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature. 2006;440:890–895. doi:10.1038/nature04651. PMID:16612374.
  • Hugues S et al. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat Immunol. 2007;8:921–930. doi:10.1038/ni1495. PMID:17660821.
  • Askew D et al. Transient surface CCR5 expression by naive CD8(+) T cells within inflamed Lymph Nodes is dependent on high Endothelial Venule interaction and augments Th cell-dependent memory response. Journal of Immunology. 2016;196:3653–3664. doi:10.4049/jimmunol.1501176.
  • Menten P, Wuyts A, Van Damme J Macrophage inflammatory protein-1. Cytokine Growth Factor Rev. 2002;13:455–481. doi:10.1016/S1359-6101(02)00045-X. PMID:12401480.
  • Shiraishi K et al. Enhancement of antitumor radiation efficacy and consistent induction of the abscopal effect in mice by ECI301, an active variant of macrophage inflammatory protein-1alpha. Clin Cancer Res. 2008;14:1159–1166. doi:10.1158/1078-0432.CCR-07-4485. PMID:18281550.
  • Corbett TH, Griswold DP, Jr., Roberts BJ, Peckham JC, Schabel FM, Jr. Tumor induction relationships in development of transplantable cancers of the colon in mice for chemotherapy assays, with a note on carcinogen structure. Cancer Res. 1975;35:2434–2439. PMID:1149045.
  • Huang AY et al. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc Natl Acad Sci U S A. 1996;93:9730–9735. doi:10.1073/pnas.93.18.9730. PMID:8790399.
  • Cambien B et al. CCL5 neutralization restricts cancer growth and potentiates the targeting of PDGFRbeta in colorectal carcinoma. PLoS One. 2011;6:e28842. doi:10.1371/journal.pone.0028842. PMID:22205974.
  • Chang LY et al. Tumor-derived chemokine CCL5 enhances TGF-beta-mediated killing of CD8(+) T cells in colon cancer by T-regulatory cells. Cancer Res. 2012;72:1092–1102. doi:10.1158/0008-5472.CAN-11-2493. PMID:22282655.
  • Mocellin S et al. Use of quantitative real-time PCR to determine immune cell density and cytokine gene profile in the tumor microenvironment. J Immunol Methods. 2003;280:1–11. doi:10.1016/S0022-1759(03)00274-6. PMID:12972183.
  • Li Z et al. Cross-talk between T cells and innate immune cells is crucial for IFN-gamma-dependent tumor rejection. J Immunol. 2007;179:1568–1576. doi:10.4049/jimmunol.179.3.1568. PMID:17641023.
  • Cacalano NA Regulation of natural killer cell function by STAT3. Front Immunol. 2016;7:128. doi:10.3389/fimmu.2016.00128. PMID:27148255.
  • Carter SL, Muller M, Manders PM, Campbell IL Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia. 2007;55:1728–1739. doi:10.1002/glia.20587. PMID:17902170.
  • Lantier L et al. Intestinal CD103+ dendritic cells are key players in the innate immune control of Cryptosporidium parvum infection in neonatal mice. PLoS Pathog. 2013;9:e1003801. doi:10.1371/journal.ppat.1003801. PMID:24367259.
  • Fahey TJ, 3rd et al. Macrophage inflammatory protein 1 modulates macrophage function. J Immunol. 1992;148:2764–2769. PMID:1573267.
  • Mikucki ME et al. Non-redundant requirement for CXCR3 signalling during tumoricidal T-cell trafficking across tumour vascular checkpoints. Nat Commun. 2015;6:7458. doi:10.1038/ncomms8458. PMID:26109379.
  • Castle JC et al. Immunomic, genomic and transcriptomic characterization of CT26 colorectal carcinoma. BMC Genomics. 2014;15:190. doi:10.1186/1471-2164-15-190. PMID:24621249.
  • Oderup C, LaJevic M, Butcher EC Canonical and noncanonical Wnt proteins program dendritic cell responses for tolerance. J Immunol. 2013;190:6126–6134. doi:10.4049/jimmunol.1203002. PMID:23677472.
  • Ma B, Hottiger MO Crosstalk between Wnt/beta-Catenin and NF-kappaB Signaling Pathway during inflammation. Front Immunol. 2016;7:378. doi:10.3389/fimmu.2016.00378. PMID:27713747.
  • Yasuhara R et al. The beta-catenin signaling pathway induces aggressive potential in breast cancer by up-regulating the chemokine CCL5. Exp Cell Res. 2015;338:22–31. doi:10.1016/j.yexcr.2015.09.003. PMID:26363360.
  • Budi EH, Duan D, Derynck R Transforming growth Factor-beta Receptors and Smads: Regulatory complexity and functional versatility. Trends Cell Biol. 2017;27:658–672. doi:10.1016/j.tcb.2017.04.005. PMID:28552280.
  • Sabat R et al. Biology of interleukin-10. Cytokine Growth Factor Rev. 2010;21:331–344. doi:10.1016/j.cytogfr.2010.09.002. PMID:21115385.
  • Monteagudo C, Martin JM, Jorda E, Llombart-Bosch A CXCR3 chemokine receptor immunoreactivity in primary cutaneous malignant melanoma: correlation with clinicopathological prognostic factors. J Clin Pathol. 2007;60:596–599. doi:10.1136/jcp.2005.032144. PMID:16522748.
  • Groom JR, Luster AD CXCR3 in T cell function. Exp Cell Res. 2011;317:620–631. doi:10.1016/j.yexcr.2010.12.017. PMID:21376175.
  • Nakajima C et al. A role of interferon-gamma (IFN-gamma) in tumor immunity: T cells with the capacity to reject tumor cells are generated but fail to migrate to tumor sites in IFN-gamma-deficient mice. Cancer Res. 2001;61:3399–3405. PMID:11309299.
  • Dorner BG et al. MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc Natl Acad Sci U S A. 2002;99:6181–6186. doi:10.1073/pnas.092141999. PMID:11972057.
  • Zhang N et al. Type 1 T-cell responses in chlamydial lung infections are associated with local MIP-1alpha response. Cell Mol Immunol. 2010;7:355–360. doi:10.1038/cmi.2010.32. PMID:20622889.
  • Martin-Fontecha A et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol. 2004;5:1260–1265. doi:10.1038/ni1138. PMID:15531883.
  • Sercan O, Stoycheva D, Hammerling GJ, Arnold B, Schuler T IFN-gamma receptor signaling regulates memory CD8+ T cell differentiation. J Immunol. 2010;184:2855–2862. doi:10.4049/jimmunol.0902708. PMID:20164422.
  • Whitmire JK, Tan JT, Whitton JL Interferon-gamma acts directly on CD8(+) T cells to increase their abundance during virus infection. Journal of Experimental Medicine. 2005;201:1053–1059. doi:10.1084/jem.20041463. PMID:15809350.
  • Golgher D, Jones E, Powrie F, Elliott T, Gallimore A Depletion of CD25+ regulatory cells uncovers immune responses to shared murine tumor rejection antigens. Eur J Immunol. 2002;32:3267–3275. doi:10.1002/1521-4141(200211)32:11%3c3267::AID-IMMU3267%3e3.0.CO;2-1. PMID:12555672.
  • Van der Jeught K. et al. Targeting the tumor microenvironment to enhance antitumor immune responses. Oncotarget. 2015;6:1359–1381. doi:10.18632/oncotarget.3204. PMID:25682197.
  • Bernardini G et al. CCL3 and CXCL12 regulate trafficking of mouse bone marrow NK cell subsets. Blood. 2008;111:3626–3634. doi:10.1182/blood-2007-08-106203. PMID:18227348.
  • Charmoy M et al. Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS Pathog. 2010;6:e1000755. doi:10.1371/journal.ppat.1000755. PMID:20140197.
  • Coca S et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer. 1997;79:2320–2328. doi:10.1002/(SICI)1097-0142(19970615)79:12%3c2320::AID-CNCR5%3e3.0.CO;2-P. PMID:9191519.
  • Roda JM et al. Natural killer cells produce T cell-recruiting chemokines in response to antibody-coated tumor cells. Cancer Res. 2006;66:517–526. doi:10.1158/0008-5472.CAN-05-2429. PMID:16397268.
  • Tomayko MM, Reynolds CP Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol. 1989;24:148–154. doi:10.1007/BF00300234. PMID:2544306.

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