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Original Research

Timing of CSF-1/CSF-1R signaling blockade is critical to improving responses to CTLA-4 based immunotherapy

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Article: e1151595 | Received 21 Dec 2015, Accepted 03 Feb 2016, Published online: 23 Jun 2016

References

  • Royal RE, Levy C, Turner K, Mathur A, Hughes M, Kammula US, Sherry RM, Topalian SL, Yang JC, Lowy I, Rosenberg SA. Phase 2 trial of single agent Ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother (2010); 33(8):828-33; PMID:20842054; http://dx.doi.org/10.1097/CJI.0b013e3181eec14c
  • Le DT, Lutz E, Uram JN, Sugar EA, Onners B, Solt S, Zheng L, Diaz LA Jr, Donehower RC, Jaffee EM et al. Evaluation of ipilimumab in combination with allogeneic pancreatic tumor cells transfected with a GM-CSF gene in previously treated pancreatic cancer. J Immunother (2013); 36(7):382-9; PMID:23924790; http://dx.doi.org/10.1097/CJI.0b013e31829fb7a2
  • Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med (2010); 363(8):711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
  • Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med (2011); 364(26):2517-26; PMID:21639810; http://dx.doi.org/10.1056/NEJMoa1104621
  • Phan GQ, Yang JC, Sherry RM, Hwu P, Topalian SL, Schwartzentruber DJ, Restifo NP, Haworth LR, Seipp CA, Freezer LJ et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci U S A (2003); 100(14):8372-7; PMID:12826605; http://dx.doi.org/10.1073/pnas.1533209100
  • Hodi FS, Mihm MC, Soiffer RJ, Haluska FG, Butler M, Seiden MV, Davis T, Henry-Spires R, MacRae S, Willman A et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A (2003); 100(8):4712-7; PMID:12682289; http://dx.doi.org/10.1073/pnas.0830997100
  • Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol (2009); 9(3):162-74; PMID:19197294; http://dx.doi.org/10.1038/nri2506
  • Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol (2008); 181(8):5791-802; PMID:18832739; http://dx.doi.org/10.4049/jimmunol.181.8.5791
  • Umemura N, Saio M, Suwa T, Kitoh Y, Bai J, Nonaka K, Ouyang GF, Okada M, Balazs M, Adany R et al. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J Leukoc Biol (2008); 83(5):1136-44; PMID:18285406; http://dx.doi.org/10.1189/jlb.0907611
  • Sawanobori Y, Ueha S, Kurachi M, Shimaoka T, Talmadge JE, Abe J, Shono Y, Kitabatake M, Kakimi K, Mukaida N et al. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood (2008); 111(12):5457-66; PMID:18375791; http://dx.doi.org/10.1182/blood-2008-01-136895
  • Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med (2001); 193(6):727-40; PMID:11257139; http://dx.doi.org/10.1084/jem.193.6.727
  • Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood (2002); 99(1):111-20; PMID:11756160; http://dx.doi.org/10.1182/blood.V99.1.111
  • Li F, Xiang Y, Potter J, Dinavahi R, Dang CV, Lee LA. Conditional deletion of c-myc does not impair liver regeneration. Cancer Res (2006); 66(11):5608-12; PMID:16740696; http://dx.doi.org/10.1158/0008-5472.CAN-05-4242
  • Richardsen E, Uglehus RD, Johnsen SH, Busund LT, Macrophage-Colony Stimulating Factor (CSF1) Predicts Breast Cancer Progression and Mortality. Anticancer research (2015); 35(2):865-74; PMID:25667468
  • Zhu XD, Zhang JB, Zhuang PY, Zhu HG, Zhang W, Xiong YQ, Wu WZ, Wang L, Tang ZY, Sun HC. High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol (2008); 26(16):2707-16; PMID:18509183; http://dx.doi.org/10.1200/JCO.2007.15.6521
  • Priceman SJ, Sung JL, Shaposhnik Z, Burton JB, Torres-Collado AX, Moughon DL, Johnson M, Lusis AJ, Cohen DA, Iruela-Arispe ML et al. Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: combating tumor evasion of antiangiogenic therapy. Blood (2010); 115(7):1461-71; PMID:20008303; http://dx.doi.org/10.1182/blood-2009-08-237412
  • Tarhini AA, Butterfield LH, Shuai Y, Gooding WE, Kalinski P, Kirkwood JM. Differing patterns of circulating regulatory T cells and myeloid-derived suppressor cells in metastatic melanoma patients receiving anti-CTLA4 antibody and interferon-alpha or TLR-9 agonist and GM-CSF with peptide vaccination. J Immunother (2012); 35(9):702-10; PMID:23090079; http://dx.doi.org/10.1097/CJI.0b013e318272569b
  • Zhu Y, Knolhoff BL, Meyer MA, Nywening TM, West BL, Luo J, Wang-Gillam A, Goedegebuure SP, Linehan DC, DeNardo DG. CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res (2014); 74(18):5057-69; PMID:25082815; http://dx.doi.org/10.1158/0008-5472.CAN-13-3723
  • Manthey CL, Johnson DL, Illig CR, Tuman RW, Zhou Z, Baker JF, Chaikin MA, Donatelli RR, Franks CF, Zeng L et al. JNJ-28312141, a novel orally active colony-stimulating factor-1 receptor/FMS-related receptor tyrosine kinase-3 receptor tyrosine kinase inhibitor with potential utility in solid tumors, bone metastases, and acute myeloid leukemia. Mol Cancer Ther (2009); 8(11):3151-61; PMID:19887542; http://dx.doi.org/10.1158/1535-7163.MCT-09-0255
  • Patel S, Player MR. Colony-stimulating factor-1 receptor inhibitors for the treatment of cancer and inflammatory disease. Current topics in medicinal chemistry (2009); 9(7):599-610; PMID:19689368; http://dx.doi.org/10.2174/156802609789007327
  • Chitu V, Nacu V, Charles JF, Henne WM, McMahon HT, Nandi S, Ketchum H, Harris R, Nakamura MC, Stanley ER. PSTPIP2 deficiency in mice causes osteopenia and increased differentiation of multipotent myeloid precursors into osteoclasts. Blood (2012); 120(15):3126-35; PMID:22923495; http://dx.doi.org/10.1182/blood-2012-04-425595
  • Xu J, Escamilla J, Mok S, David J, Priceman S, West B, Bollag G, McBride W, Wu L. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res (2013); 73(9):2782-94; PMID:23418320; http://dx.doi.org/10.1158/0008-5472.CAN-12-3981
  • Mok S, Koya RC, Tsui C, Xu J, Robert L, Wu L, Graeber TG, West BL, Bollag G, Ribas A. Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res (2014); 74(1):153-61; PMID:24247719; http://dx.doi.org/10.1158/0008-5472.CAN-13-1816
  • Coniglio SJ, Eugenin E, Dobrenis K, Stanley ER, West BL, Symons MH, Segall JE. Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol Med (2012); 18:519-27; PMID:22294205; http://dx.doi.org/10.2119/molmed.2011.00217
  • DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov (2011); 1(1):54-67; PMID:22039576; http://dx.doi.org/10.1158/2159-8274.CD-10-0028
  • Ries CH, Hoves S, Cannarile MA, Ruttinger D. CSF-1/CSF-1R targeting agents in clinical development for cancer therapy. Curr Opin Pharmacol (2015); 23:45-51; PMID:26051995; http://dx.doi.org/10.1016/j.coph.2015.05.008
  • Tarhini AA, Iqbal F. CTLA-4 blockade: therapeutic potential in cancer treatments. Onco Targets Ther (2010); 3:15-25; PMID:20616954; http://dx.doi.org/10.2147/OTT.S4833
  • Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol (2012); 12(4):253-68; PMID:22437938; http://dx.doi.org/10.1038/nri3175
  • Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med (2015); 373(1):23-34; PMID:26027431; http://dx.doi.org/10.1056/NEJMoa1504030
  • Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, McDermott D, Linette GP, Meyer N, Giguere JK, Agarwala SS et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med (2015); 372(21):2006-17; PMID:25891304; http://dx.doi.org/10.1056/NEJMoa1414428
  • Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med (2013); 369(2):134-44; PMID:23724846; http://dx.doi.org/10.1056/NEJMoa1305133
  • Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med (2013); 369(2):122-33; PMID:23724867; http://dx.doi.org/10.1056/NEJMoa1302369
  • Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, Belaygorod L, Carpenter D, Collins L, Piwnica-Worms D et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res (2013); 73(3):1128-41; PMID:23221383; http://dx.doi.org/10.1158/0008-5472.CAN-12-2731
  • Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med (2013); 19(10):1264-72; PMID:24056773; http://dx.doi.org/10.1038/nm.3337
  • Strachan DC, Ruffell B, Oei Y, Bissell MJ, Coussens LM, Pryer N, Daniel D. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8 T cells. Oncoimmunology (2013); 2(12):e26968; PMID:24498562; http://dx.doi.org/10.4161/onci.26968
  • Sluijter M, van der Sluis TC, van der Velden PA, Versluis M, West BL, van der Burg SH, van Hall T. Inhibition of CSF-1R supports T-cell mediated melanoma therapy. PLoS One (2014); 9(8):e104230; PMID:25110953; http://dx.doi.org/10.1371/journal.pone.0104230
  • Paulus P, Stanley ER, Schafer R, Abraham D, Aharinejad S. Colony-stimulating factor-1 antibody reverses chemoresistance in human MCF-7 breast cancer xenografts. Cancer Res (2006); 66(8):4349-56; PMID:16618760; http://dx.doi.org/10.1158/0008-5472.CAN-05-3523
  • Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, De Baetselier P, Van Ginderachter JA. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood (2008); 111(8):4233-44; PMID:18272812; http://dx.doi.org/10.1182/blood-2007-07-099226
  • Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, Divino CM, Chen SH. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res (2006); 66(2):1123-31; PMID:16424049; http://dx.doi.org/10.1158/0008-5472.CAN-05-1299
  • Srivastava MK, Zhu L, Harris-White M, Kar UK, Huang M, Johnson MF, Lee JM, Elashoff D, Strieter R, Dubinett S et al. Myeloid suppressor cell depletion augments antitumor activity in lung cancer. PLoS One (2012); 7(7):e40677; PMID:22815789; http://dx.doi.org/10.1371/journal.pone.0040677
  • Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ, McCauley LK. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res (2009); 69(4):1685-92; PMID:19176388; http://dx.doi.org/10.1158/0008-5472.CAN-08-2164
  • Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science (2008); 320(5877):807-11; PMID:18467591; http://dx.doi.org/10.1126/science.1154370
  • Wei S, Nandi S, Chitu V, Yeung YG, Yu W, Huang M, Williams LT, Lin H, Stanley ER. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells. J Leukoc Biol (2010); 88(3):495-505; PMID:20504948; http://dx.doi.org/10.1189/jlb.1209822
  • Fleetwood AJ, Lawrence T, Hamilton JA, Cook AD. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J Immunol (2007); 178(8):5245-52; PMID:17404308; http://dx.doi.org/10.4049/jimmunol.178.8.5245
  • Anagnostopoulos GK, Sakorafas GH, Kostopoulos P, Margantinis G, Tsiakos S, Terpos E, Pavlakis G, Fortun P, Arvanitidis D. Disseminated colon cancer with severe peripheral blood eosinophilia and elevated serum levels of interleukine-2, interleukine-3, interleukine-5, and GM-CSF. Surg Oncol (2005); 89(4):273-5; PMID:15726608; http://dx.doi.org/10.1002/jso.20173
  • Wu QD, Wang JH, Bouchier-Hayes D, Redmond HP. Neutrophil-induced transmigration of tumour cells treated with tumour-conditioned medium is facilitated by granulocyte-macrophage colony-stimulating factor. Eur J Surg (2000); 166(5):361-6; PMID:10881945; http://dx.doi.org/10.3109/110241500750008899
  • Jubinsky PT, Short MK, Mutema G, Morris RE, Ciraolo GM, Li M. Magmas expression in neoplastic human prostate. J Mol Histol (2005); 36(1–2):69-75; PMID:15704001; http://dx.doi.org/10.1007/s10735-004-3840-8
  • Chavey C, Bibeau F, Gourgou-Bourgade S, Burlinchon S, Boissière F, Laune D, Roques S, Lazennec G. Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast cancer research : BCR (2007); 9(1):R15; PMID:17261184; http://dx.doi.org/10.1186/bcr1648
  • Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer cell (2009); 16(3):183-94; PMID:19732719; http://dx.doi.org/10.1016/j.ccr.2009.06.017
  • Holmgaard RB, Zamarin D, Munn DH, Wolchok JD, Allison JP. Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med (2013); 210(7):1389-402; PMID:23752227; http://dx.doi.org/10.1084/jem.20130066
  • Holmgaard RB, D Zamarin, Y Li, B Gasmi, DH Munn, JP Allison, T Merghoub, JD Wolchok. Tumor-Expressed IDO Recruits and Activates MDSCs in a Treg-Dependent Manner. Cell reports 2015; 13:412-4; PMID:26411680; http://dx.doi.org/10.1016/j.celrep.2015.08.077
  • Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP, “GenePattern 2.0” Nature Genetics (2006); 38 no. 5: 500-501; http://dx.doi.org/10.1038/ng0506-500
  • Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med Jun (2015); 25;372(26):2521-32; PMID:25891173; http://dx.doi.org/10.1056/NEJMoa1503093
  • Garon EB1, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med May (2015); 21;372(21):2018-28; PMID:25891174; http://dx.doi.org/10.1056/NEJMoa1501824
  • Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER et al. Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma. N Engl J Med Nov 5(2015); 373(19):1803-13; PMID:26406148; http://dx.doi.org/10.1056/NEJMoa1510665

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