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The interplay between the immune system and chemotherapy: emerging methods for optimizing therapy

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References

  • Rasmussen L, Arvin A. Chemotherapy-induced immunosuppression. Environ. Health Perspect. 43, 21–25 (1982).
  • Schwartz RS. Are immunosuppressive anticancer drugs self-defeating? Cancer Res. 28(7), 1452–1454 (1968).
  • Schwartz R. Immunosuppressive drug therapy. In: Human Transplantation. Rappaport F, Dausset J ( Eds). Grune and Stratton, Inc., New York, NY, USA 440–471 (1968).
  • Weinblatt ME, Coblyn JS, Fox DA et al. Efficacy of low-dose methotrexate in rheumatoid arthritis. N. Engl. J. Med. 312(13), 818–822 (1985).
  • Hauser SL, Dawson DM, Lehrich JR et al. Intensive immunosuppression in progressive multiple sclerosis. A randomized, three-arm study of high-dose intravenous cyclophosphamide, plasma exchange, and ACTH. N. Engl. J. Med. 308(4), 173–180 (1983).
  • Chan JA, Stuart K, Earle CC et al. Prospective study of bevacizumab plus temozolomide in patients with advanced neuroendocrine tumors. J. Clin. Oncol. 30(24), 2963–2968 (2012).
  • Tarnowski GS, Faanes RB, Ralph P, Williams N. Suppression and restoration of cytotoxic T-cell activity during chemotherapy of a mouse T-cell lymphoma and a macrophage tumor. Cancer Res. 38(12), 4540–4545 (1978).
  • Schwartz HS, Grindey GB. Adriamycin and daunorubicin: a comparison of antitumor activities and tissue uptake in mice following immunosuppression. Cancer Res. 33(8), 1837–1844 (1973).
  • Zagozdzon R, Golab J, Stoklosa T et al. Effective chemo-immunotherapy of L1210 leukemia in vivo using interleukin-12 combined with doxorubicin but not with cyclophosphamide, paclitaxel or cisplatin. Int. J. Cancer 77(5), 720–727 (1998).
  • Apetoh L, Ghiringhelli F, Tesniere A et al. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol. Rev. 220, 47–59 (2007).
  • Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8(1), 59–73 (2008).
  • Lake RA, Robinson BW. Immunotherapy and chemotherapy--a practical partnership. Nat. Rev. Cancer 5(5), 397–405 (2005).
  • Pages F, Berger A, Camus M et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353(25), 2654–2666 (2005).
  • Bindea G, Mlecnik B, Tosolini M et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39(4), 782–795 (2013).
  • Ladoire S, Mignot G, Dabakuyo S et al. In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival. J. Pathol. 224(3), 389–400 (2011).
  • Casares N, Pequignot MO, Tesniere A et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med. 202(12), 1691–1701 (2005).
  • Obeid M, Tesniere A, Ghiringhelli F et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13(1), 54–61 (2007).
  • Panaretakis T, Joza N, Modjtahedi N et al. The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ. 15(9), 1499–1509 (2008).
  • Apetoh L, Ghiringhelli F, Tesniere A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13(9), 1050–1059 (2007).
  • Apetoh L, Mignot G, Panaretakis T, Kroemer G, Zitvogel L. Immunogenicity of anthracyclines: moving towards more personalized medicine. Trends Mol. Med. 14(4), 141–151 (2008).
  • Ghiringhelli F, Apetoh L, Tesniere A et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 15(10), 1170–1178 (2009).
  • Ma Y, Adjemian S, Mattarollo SR et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38(4), 729–741 (2013).
  • Michaud M, Martins I, Sukkurwala AQ et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 334(6062), 1573–1577 (2011).
  • Ma Y, Yamazaki T, Yang H et al. Tumor necrosis factor is dispensable for the success of immunogenic anticancer chemotherapy. Oncoimmunology 2(6), e24786 (2013).
  • Menger L, Vacchelli E, Adjemian S et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci. Transl. Med. 4(143), 143ra199 (2012).
  • Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319(6055), 675–678 (1986).
  • Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436(7054), 1186–1190 (2005).
  • Fine JH, Chen P, Mesci A et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res. 70(18), 7102–7113 (2010).
  • Ugurel S, Paschen A, Becker JC. Dacarbazine in melanoma: from a chemotherapeutic drug to an immunomodulating agent. J. Invest. Dermatol. 133(2), 289–292 (2013).
  • Hervieu A, Rebe C, Vegran F et al. Dacarbazine-mediated upregulation of NKG2D ligands on tumor cells activates NK and CD8 T cells and restrains melanoma growth. J. Invest. Dermatol. 133(2), 499–508 (2013).
  • Lesterhuis WJ, Punt CJ, Hato SV et al. Platinum-based drugs disrupt STAT6-mediated suppression of immune responses against cancer in humans and mice. J. Clin. Invest. 121(8), 3100–3108 (2011).
  • Latchman Y, Wood CR, Chernova T et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2(3), 261–268 (2001).
  • Berendt MJ, North RJ. T-cell-mediated suppression of anti-tumor immunity. An explanation for progressive growth of an immunogenic tumor. J. Exp. Med. 151(1), 69–80 (1980).
  • Curiel TJ, Coukos G, Zou L et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10(9), 942–949 (2004).
  • Sonabend AM, Rolle CE, Lesniak MS. The role of regulatory T cells in malignant glioma. Anticancer Res. 28(2B), 1143–1150 (2008).
  • Di Paolo NC, Tuve S, Ni S, Hellstrom KE, Hellstrom I, Lieber A. Effect of adenovirus-mediated heat shock protein expression and oncolysis in combination with low-dose cyclophosphamide treatment on antitumor immune responses. Cancer Res. 66(2), 960–969 (2006).
  • Rico MJ, Rozados VR, Mainetti LE, Zacarias Fluck MF, Matar P, Scharovsky OG. Regulatory T cells but not NKT I cells are modulated by a single low-dose cyclophosphamide in a B cell lymphoma tumor-model. Exp. Oncol. 34(1), 38–42 (2012).
  • Roux S, Apetoh L, Chalmin F et al. CD4+CD25+ Tregs control the TRAIL-dependent cytotoxicity of tumor-infiltrating DCs in rodent models of colon cancer. J. Clin. Invest. 118(11), 3751–3761 (2008).
  • Kasprowicz DJ, Droin N, Soper DM, Ramsdell F, Green DR, Ziegler SF. Dynamic regulation of FoxP3 expression controls the balance between CD4+ T cell activation and cell death. Eur. J. Immunol. 35(12), 3424–3432 (2005).
  • Zhao J, Cao Y, Lei Z, Yang Z, Zhang B, Huang B. Selective depletion of CD4+CD25+Foxp3+ regulatory T cells by low-dose cyclophosphamide is explained by reduced intracellular ATP levels. Cancer Res. 70(12), 4850–4858 (2010).
  • Ghiringhelli F, Menard C, Puig PE et al. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother. 56(5), 641–648 (2007).
  • Ge Y, Domschke C, Stoiber N et al. Metronomic cyclophosphamide treatment in metastasized breast cancer patients: immunological effects and clinical outcome. Cancer Immunol. Immunother. 61(3), 353–362 (2012).
  • Viaud S, Flament C, Zoubir M et al. Cyclophosphamide induces differentiation of Th17 cells in cancer patients. Cancer Res. 71(3), 661–665 (2011).
  • Moschella F, Valentini M, Arico E et al. Unraveling cancer chemoimmunotherapy mechanisms by gene and protein expression profiling of responses to cyclophosphamide. Cancer Res. 71(10), 3528–3539 (2011).
  • Moschella F, Torelli GF, Valentini M et al. Cyclophosphamide induces a type I interferon-associated sterile inflammatory response signature in cancer patients’ blood cells: implications for cancer chemoimmunotherapy. Clin. Cancer Res. 19(15), 4249–4261 (2013).
  • Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9(3), 162–174 (2009).
  • Ugel S, Delpozzo F, Desantis G et al. Therapeutic targeting of myeloid-derived suppressor cells. Curr. Opin. Pharmacol. 9(4), 470–481 (2009).
  • Le HK, Graham L, Cha E, Morales JK, Manjili MH, Bear HD. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int. Immunopharmacol. 9(7–8), 900–909 (2009).
  • Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11(18), 6713–6721 (2005).
  • 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. 70(8), 3052–3061 (2010).
  • Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6(4), 443–446 (2000).
  • Park S, Jiang Z, Mortenson ED et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 18(2), 160–170 (2010).
  • Beano A, Signorino E, Evangelista A et al. Correlation between NK function and response to trastuzumab in metastatic breast cancer patients. J. Transl Med. 6, 25 (2008).
  • Borg C, Terme M, Taieb J et al. Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J. Clin. Invest. 114(3), 379–388 (2004).
  • Menard C, Blay JY, Borg C et al. Natural killer cell IFN-gamma levels predict long-term survival with imatinib mesylate therapy in gastrointestinal stromal tumor-bearing patients. Cancer Res. 69(8), 3563–3569 (2009).
  • Ozao-Choy J, Ma G, Kao J et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 69(6), 2514–2522 (2009).
  • Ko JS, Rayman P, Ireland J et al. Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res. 70(9), 3526–3536 (2010).
  • Xin H, Zhang C, Herrmann A, Du Y, Figlin R, Yu H. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 69(6), 2506–2513 (2009).
  • Kapanadze T, Gamrekelashvili J, Ma C et al. Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J. Hepatol. 59(5), 1007–1013 (2013).
  • Cao M, Xu Y, Youn JI et al. Kinase inhibitor Sorafenib modulates immunosuppressive cell populations in a murine liver cancer model. Lab. Invest. 91(4), 598–608 (2011).
  • Schilling B, Sucker A, Griewank K et al. Vemurafenib reverses immunosuppression by myeloid derived suppressor cells. Int. J. Cancer 133(7), 1653–1663 (2013).
  • Ko JS, Zea AH, Rini BI et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 15(6), 2148–2157 (2009).
  • Sevko A, Sade-Feldman M, Kanterman J et al. Cyclophosphamide promotes chronic inflammation-dependent immunosuppression and prevents antitumor response in melanoma. J. Invest. Dermatol. 133(6), 1610–1619 (2013).
  • Malvicini M, Ingolotti M, Piccioni F et al. Reversal of gastrointestinal carcinoma-induced immunosuppression and induction of antitumoural immunity by a combination of cyclophosphamide and gene transfer of IL-12. Mol. Oncol. 5(3), 242–255 (2011).
  • Petersen CC, Diernaes JE, Skovbo A, Hvid M, Deleuran B, Hokland M. Interleukin-21 restrains tumor growth and induces a substantial increase in the number of circulating tumor-specific T cells in a murine model of malignant melanoma. Cytokine 49(1), 80–88 (2010).
  • Chalmin F, Ladoire S, Mignot G et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 120(2), 457–471 (2010).
  • Bruchard M, Mignot G, Derangere V et al. Chemotherapy-triggered cathepsin B release in myeloid-derived suppressor cells activates the Nlrp3 inflammasome and promotes tumor growth. Nat. Med. 19(1), 57–64 (2013).
  • Ghiringhelli F, Bruchard M, Apetoh L. Immune effects of 5-fluorouracil: Ambivalence matters. Oncoimmunology 2(3), e23139 (2013).
  • Zhang JP, Yan J, Xu J et al. Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J. Hepatol. 50(5), 980–989 (2009).
  • Chen X, Wan J, Liu J et al. Increased IL-17-producing cells correlate with poor survival and lymphangiogenesis in NSCLC patients. Lung Cancer 69(3), 348–354 (2010).
  • Tosolini M, Kirilovsky A, Mlecnik B et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 71(4), 1263–1271 (2011).
  • Liu J, Duan Y, Cheng X et al. IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma. Biochem. Biophys. Res. Commun. 407(2), 348–354 (2011).
  • Berger H, Vegran F, Chikh M et al. SOCS3 transactivation by PPARgamma prevents IL-17-driven cancer growth. Cancer Res. 73(12), 3578–3590 (2013).
  • Chung AS, Wu X, Zhuang G et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat. Med. 19(9), 1114–1123 (2013).
  • Kantoff PW, Higano CS, Shore ND et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J. Med. 363(5), 411–422 (2010).
  • Machiels JP, Reilly RT, Emens LA et al. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res. 61(9), 3689–3697 (2001).
  • Arlen PM, Gulley JL, Parker C et al. A randomized phase II study of concurrent docetaxel plus vaccine versus vaccine alone in metastatic androgen-independent prostate cancer. Clin. Cancer Res. 12(4), 1260–1269 (2006).
  • Antonia SJ, Mirza N, Fricke I et al. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer. Clin. Cancer Res. 12(3 Pt 1), 878–887 (2006).
  • Wheeler CJ, Das A, Liu G, Yu JS, Black KL. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin. Cancer Res. 10(16), 5316–5326 (2004).
  • Quoix E, Ramlau R, Westeel V et al. Therapeutic vaccination with TG4010 and first-line chemotherapy in advanced non-small-cell lung cancer: a controlled phase 2B trial. Lancet Oncol. 12(12), 1125–1133 (2011).
  • Shankaran V, Ikeda H, Bruce AT et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410(6832), 1107–1111 (2001).
  • Allison JP, Krummel MF. The Yin and Yang of T cell costimulation. Science 270(5238), 932–933 (1995).
  • Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271(5256), 1734–1736 (1996).
  • Hodi FS, Butler M, Oble DA et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc. Natl Acad. Sci. USA 105(8), 3005–3010 (2008).
  • Zha Y, Blank C, Gajewski TF. Negative regulation of T-cell function by PD-1. Crit. Rev. Immunol. 24(4), 229–237 (2004).
  • Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl Acad. Sci. USA 99(19), 12293–12297 (2002).
  • Freeman GJ, Long AJ, Iwai Y et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192(7), 1027–1034 (2000).
  • Dong H, Strome SE, Salomao DR et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8(8), 793–800 (2002).
  • Zhu C, Anderson AC, Schubart A et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6(12), 1245–1252 (2005).
  • Anderson AC. Tim-3, a negative regulator of anti-tumor immunity. Curr. Opin. Immunol. 24(2), 213–216 (2012).
  • Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 207(10), 2187–2194 (2010).
  • Ding ZC, Huang L, Blazar BR et al. Polyfunctional CD4(+) T cells are essential for eradicating advanced B-cell lymphoma after chemotherapy. Blood 120(11), 2229–2239 (2012).
  • Hodi FS, O’Day SJ, McDermott DF et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363(8), 711–723 (2010).
  • Robert C, Thomas L, Bondarenko I et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364(26), 2517–2526 (2011).
  • Wolchok JD, Kluger H, Callahan MK et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369(2), 122–133 (2013).

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