A copper chelate selectively triggers apoptosis in myeloid-derived suppressor cells in a drug-resistant tumor model and enhances antitumor immune response

References

• DeNardo DG, Brennan DJ, Rexhepaj E, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1:54–67
   PubMed Web of Science ®Google Scholar
• Shiao SL, Ganesan AP, Rugo HS, Coussens LM. Immune microenvironments in solid tumors: new targets for therapy. Genes Dev 2011;25:2559–2572
   PubMed Web of Science ®Google Scholar
• Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263–274
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162–174
   PubMed Web of Science ®Google Scholar
• Pan PY, Wang GX, Yin B, et al. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 2008;111:219–228
   PubMed Web of Science ®Google Scholar
• Sinha P, Clements VK, Bunt SK, et al. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 2007;179:977–983
   PubMed Web of Science ®Google Scholar
• Hanson EM, Clements VK, Sinha P, et al. Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J Immunol 2009;183:937–944
   PubMed Web of Science ®Google Scholar
• Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007;117:1155–1166
   PubMed Web of Science ®Google Scholar
• Kao J, Ko EC, Sikora AT, et al. Targeting immune suppressing myeloid-derived suppressor cells in oncology. Crit Rev Oncol Hematol 2011;77:12–19
   PubMed Web of Science ®Google Scholar
• Kusmartsev S, Cheng F, Yu B, et al. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res 2003;63:4441–4449
   PubMed Web of Science ®Google Scholar
• Fricke I, Mirza N, Dupont J, et al. Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses. Clin Cancer Res 2007;13:4840–4848
   PubMed Web of Science ®Google Scholar
• Zhenga Y, Xub M, Li X, et al. Cimetidine suppresses lung tumor growth in mice through proapoptosis of myeloid-derived suppressor cells. Mol Immunol 2013;54:74–83
   PubMed Web of Science ®Google Scholar
• Suzuki E, Kapoor V, Jassar AS, et al. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 2005;11:6713–6721
   PubMed Web of Science ®Google Scholar
• Vincent J, Mignot G, Chalmin F, et al. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010;70:3052–3061
   PubMed Web of Science ®Google Scholar
• Terabe M, Matsui S, Park JM, et al. Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence. J Exp Med 2003;198:1741–1752
   PubMed Web of Science ®Google Scholar
• Talmadge JE, Hood KC, Zobel LC, et al. Chemoprevention by cyclooxygenase-2 inhibition reduces immature myeloid suppressor cell expansion. Int Immunopharmacol 2007;7:140–151
   PubMed Web of Science ®Google Scholar
• Zea AH, Rodriguez PC, Atkins MB, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 2005;65:3044–3048
   PubMed Web of Science ®Google Scholar
• Serafini P, Meckel K, Kelso M, et al. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006;203:2691–2702
   PubMed Web of Science ®Google Scholar
• De Santo C, Serafini P, Marigo I, et al. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc Natl Acad Sci USA 2005;102:4185–4190
   PubMed Web of Science ®Google Scholar
• Yu J, Du W, Yan F, et al. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol 2013;190:3783–3797
   PubMed Web of Science ®Google Scholar
• Majumder S, Panda GS, Kumar Choudhuri S. Synthesis, characterization and biological properties of a novel copper complex. Eur J Med Chem 2003;38:893–898
   PubMed Web of Science ®Google Scholar
• Mookerjee A, Mookerjee Basu J, Dutta P, et al. Overcoming drug-resistant cancer by a newly developed copper chelate through host-protective cytokine-mediated apoptosis. Clin Cancer Res 2006;12:4339–4349
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Mookerjee A, Basu JM, et al. A novel copper chelate modulates tumor associated macrophages to promote anti-tumor response of T cells. PLoS One 2009;4:e7048
   PubMed Web of Science ®Google Scholar
• Chakraborty P, Chatterjee S, Ganguly A, et al. Reprogramming of TAM toward proimmunogenic type through regulation of MAP kinases using a redox-active copper chelate. J Leukoc Biol 2012;91:609–619
   PubMed Web of Science ®Google Scholar
• Delano MJ, Scumpia PO, Weinstein JS, et al. MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J Exp Med 2007;204:1463–1474
   PubMed Web of Science ®Google Scholar
• Bronte V, Wang M, Overwijk WW, et al. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J Immunol 1998;161:5313–5320
   PubMed Web of Science ®Google Scholar
• Makarenkova VP, Bansal V, Matta BM, et al. CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J Immunol 2006;176:2085–2094
   PubMed Web of Science ®Google Scholar
• Zhu B, Bando Y, Xiao S, et al. CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J Immunol 2007;179:5228–5237
   PubMed Web of Science ®Google Scholar
• Friche E, Danks MK, Beck WT. Characterization of tumor cell resistance to 4′-deoxy-4′-iododoxorubicin developed in Ehrlich ascites cells in vivo. Cancer Res 1992;52:5701–5706
   PubMed Web of Science ®Google Scholar
• Choudhuri SK, Chatterjee A. Reversal of resistance against doxorubicin by a newly developed compound, oxalyl bis(N-phenyl)hydroxamic acid in vitro. Anticancer Drugs 1998;9:825–832
   PubMed Web of Science ®Google Scholar
• Majumder S, Dutta P, Mookerjee A, Choudhuri SK. The role of a novel copper complex in overcoming doxorubicin resistance in Ehrlich ascites carcinoma cells in vivo. Chem Biol Interact 2006;159:90–103
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Das S, Chakraborty P, et al. Myeloid derived suppressor cells (MDSCs) can induce the generation of Th17 response from naive CD4+ T cells. Immunobiology 2013;218:718–724
   PubMed Web of Science ®Google Scholar
• Ganguly A, Basu S, Banerjee K, et al. Redox active copper chelate overcomes multidrug resistance in T-lymphoblastic leukemia cell by triggering apoptosis. Mol Biosyst 2011;7:1701–1712
   PubMed Web of Science ®Google Scholar
• Sinha P, Chornoguz O, Clements VK, et al. Myeloid-derived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood 2011;117:5381–5390
   PubMed Web of Science ®Google Scholar
• Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770–776
   PubMed Web of Science ®Google Scholar
• Siegel RM, Chan FK, Chun HJ, Lenardo MJ. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat Immunol 2000;1:469–474
   PubMed Web of Science ®Google Scholar
• Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48–58
   PubMed Web of Science ®Google Scholar
• Joyce JA. Therapeutic targeting of the tumor microenvironment. Cancer Cell 2005;7:513–520
   PubMed Web of Science ®Google Scholar
• Ugel S, Delpozzo F, Desantis G, et al. Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol 2009;9:470–481
   PubMed Web of Science ®Google Scholar
• Liu Q, Zhang M, Jiang X, et al. miR-223 suppresses differentiation of tumor-induced CD11b(+) Gr1(+) myeloid-derived suppressor cells from bone marrow cells. Int J Cancer 2011;129:2662–2673
   PubMed Web of Science ®Google Scholar
• Lu B. The molecular mechanisms that control function and death of effector CD4+ T cells. Immunol Res 2006;36:275–282
   PubMed Web of Science ®Google Scholar
• Lu B, Zagouras P, Fischer JE, et al. Kinetic analysis of genomewide gene expression reveals molecule circuitries that control T cell activation and Th1/2 differentiation. Proc Natl Acad Sci USA 2004;101:3023–3028
   PubMed Web of Science ®Google Scholar
• Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007;25:267–296
   PubMed Web of Science ®Google Scholar
• Leary SC, Winge DR. The Janus face of copper: its expanding role in biology and the pathophysiology of disease. EMBO Rep 2007;8:224–227
   PubMed Web of Science ®Google Scholar
• Ganguly A, Chakraborty P, Banerjee K, Choudhuri SK. The role of a Schiff base scaffold, N-(2-hydroxy acetophenone) glycinate in overcoming multidrug resistance in cancer. Eur J Pharm Sci 2014;51:96–109
   PubMed Web of Science ®Google Scholar
• Spoerlein C, Mahal K, Schmidt H, Schobert R. Effects of chrysin, apigenin, genistein and their homoleptic copper(II) complexes on the growth and metastatic potential of cancer cells. J Inorg Biochem 2013;127:107–115
   PubMed Web of Science ®Google Scholar
• Sato TT, Machida S, Takahashi S, et al. Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mitochondrial permeability transition in Jurkat cells. J Immunol 2004;173:285–296
   PubMed Web of Science ®Google Scholar