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

OncoImmunology

Volumn 5, Issue 7, 2016, Pages

  Holmgaard, Rikke B ^a   Brachfeld, Alexandra ^a   Gasmi, Billel ^a   Jones, David R ^a   Mattar, Marissa ^a   Doman, Thompson ^b   Murphy, Mary ^b   Schaer, David ^b   Wolchok, Jedd D ^a,c   Merghoub, Taha ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c Weill Graduate School of Medical Sciences of Cornell University   (United States)

Author keywords

CSF 1R; CTLA 4; immunotherapy; MDSCs; PD 1

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR; COLONY STIMULATING FACTOR RECEPTOR ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IPILIMUMAB; PROGRAMMED DEATH 1 RECEPTOR; RECEPTOR ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CANCER INFILTRATION; CELL CULTURE; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION ASSAY; HUMAN; HUMAN CELL; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; RECEPTOR BLOCKING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; TUMOR MODEL; TUMOR REGRESSION;

EID: 84976274337     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1151595     Document Type: Article

References (55)

1. R.E.Royal, C.Levy, K.Turner, A.Mathur, M.Hughes, U.S.Kammula, R.M.Sherry, S.L.Topalian, J.C.Yang, I.Lowy, S.A.Rosenberg. 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
2. D.T.Le, E.Lutz, J.N.Uram, E.A.Sugar, B.Onners, S.Solt, L.Zheng, L.A.Diaz Jr, R.C.Donehower, E.M.Jaffee 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
3. F.S.Hodi, S.J.O'Day, D.F.McDermott, R.W.Weber, J.A.Sosman, J.B.Haanen, R.Gonzalez, C.Robert, D.Schadendorf, J.C.Hassel 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
4. C.Robert, L.Thomas, I.Bondarenko, S.O'Day, J.Weber, C.Garbe, C.Lebbe, J.F.Baurain, A.Testori, J.J.Grob 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
5. G.Q.Phan, J.C.Yang, R.M.Sherry, P.Hwu, S.L.Topalian, D.J.Schwartzentruber, N.P.Restifo, L.R.Haworth, C.A.Seipp, L.J.Freezer 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
6. F.S.Hodi, M.C.Mihm, R.J.Soiffer, F.G.Haluska, M.Butler, M.V.Seiden, T.Davis, R.Henry-Spires, S.MacRae, A.Willman 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
7. D.I.Gabrilovich, S.Nagaraj. 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
8. J.I.Youn, S.Nagaraj, M.Collazo, D.I.Gabrilovich. 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
9. N.Umemura, M.Saio, T.Suwa, Y.Kitoh, J.Bai, K.Nonaka, G.F.Ouyang, M.Okada, M.Balazs, R.Adany 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
10. Y.Sawanobori, S.Ueha, M.Kurachi, T.Shimaoka, J.E.Talmadge, J.Abe, Y.Shono, M.Kitabatake, K.Kakimi, N.Mukaida 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
11. E.Y.Lin, A.V.Nguyen, R.G.Russell, J.W.Pollard. 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
12. X.M.Dai, G.R.Ryan, A.J.Hapel, M.G.Dominguez, R.G.Russell, S.Kapp, V.Sylvestre, E.R.Stanley. 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
13. F.Li, Y.Xiang, J.Potter, R.Dinavahi, C.V.Dang, L.A.Lee. 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
14. E.Richardsen, R.D.Uglehus, S.H.Johnsen, L.T.Busund, Macrophage-Colony Stimulating Factor (CSF1) Predicts Breast Cancer Progression and Mortality. Anticancer research (2015); 35(2):865-74; PMID:25667468
15. X.D.Zhu, J.B.Zhang, P.Y.Zhuang, H.G.Zhu, W.Zhang, Y.Q.Xiong, W.Z.Wu, L.Wang, Z.Y.Tang, H.C.Sun. 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
16. S.J.Priceman, J.L.Sung, Z.Shaposhnik, J.B.Burton, A.X.Torres-Collado, D.L.Moughon, M.Johnson, A.J.Lusis, D.A.Cohen, M.L.Iruela-Arispe 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
17. A.A.Tarhini, L.H.Butterfield, Y.Shuai, W.E.Gooding, P.Kalinski, J.M.Kirkwood. 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
18. Y.Zhu, B.L.Knolhoff, M.A.Meyer, T.M.Nywening, B.L.West, J.Luo, A.Wang-Gillam, S.P.Goedegebuure, D.C.Linehan, D.G.DeNardo. 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
19. C.L.Manthey, D.L.Johnson, C.R.Illig, R.W.Tuman, Z.Zhou, J.F.Baker, M.A.Chaikin, R.R.Donatelli, C.F.Franks, L.Zeng 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
20. S.Patel, M.R.Player. 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
21. V.Chitu, V.Nacu, J.F.Charles, W.M.Henne, H.T.McMahon, S.Nandi, H.Ketchum, R.Harris, M.C.Nakamura, E.R.Stanley. 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
22. J.Xu, J.Escamilla, S.Mok, J.David, S.Priceman, B.West, G.Bollag, W.McBride, L.Wu. 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
23. S.Mok, R.C.Koya, C.Tsui, J.Xu, L.Robert, L.Wu, T.G.Graeber, B.L.West, G.Bollag, A.Ribas. 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
24. S.J.Coniglio, E.Eugenin, K.Dobrenis, E.R.Stanley, B.L.West, M.H.Symons, J.E.Segall. 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
25. D.G.DeNardo, D.J.Brennan, E.Rexhepaj, B.Ruffell, S.L.Shiao, S.F.Madden, W.M.Gallagher, N.Wadhwani, S.D.Keil, S.A.Junaid 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
26. C.H.Ries, S.Hoves, M.A.Cannarile, D.Ruttinger. 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
27. A.A.Tarhini, F.Iqbal. 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
28. D.I.Gabrilovich, S.Ostrand-Rosenberg, V.Bronte. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol (2012); 12(4):253-68; PMID:22437938; http://dx.doi.org/10.1038/nri3175
29. J.Larkin, V.Chiarion-Sileni, R.Gonzalez, J.J.Grob, C.L.Cowey, C.D.Lao, D.Schadendorf, R.Dummer, M.Smylie, P.Rutkowski 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
30. M.A.Postow, J.Chesney, A.C.Pavlick, C.Robert, K.Grossmann, D.McDermott, G.P.Linette, N.Meyer, J.K.Giguere, S.S.Agarwala 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
31. O.Hamid, C.Robert, A.Daud, F.S.Hodi, W.J.Hwu, R.Kefford, J.D.Wolchok, P.Hersey, R.W.Joseph, J.S.Weber 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
32. J.D.Wolchok, H.Kluger, M.K.Callahan, M.A.Postow, N.A.Rizvi, A.M.Lesokhin, N.H.Segal, C.E.Ariyan, R.A.Gordon, K.Reed 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
33. J.B.Mitchem, D.J.Brennan, B.L.Knolhoff, B.A.Belt, Y.Zhu, D.E.Sanford, L.Belaygorod, D.Carpenter, L.Collins, D.Piwnica-Worms 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
34. S.M.Pyonteck, L.Akkari, A.J.Schuhmacher, R.L.Bowman, L.Sevenich, D.F.Quail, O.C.Olson, M.L.Quick, J.T.Huse, V.Teijeiro 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
35. D.C.Strachan, B.Ruffell, Y.Oei, M.J.Bissell, L.M.Coussens, N.Pryer, D.Daniel. 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
36. M.Sluijter, T.C.van der Sluis, P.A.van der Velden, M.Versluis, B.L.West, S.H.van der Burg, T.van Hall. 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
37. P.Paulus, E.R.Stanley, R.Schafer, D.Abraham, S.Aharinejad. 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
38. K.Movahedi, M.Guilliams, J.Van den Bossche, R.Van den Bergh, C.Gysemans, A.Beschin, P.De Baetselier, J.A.Van Ginderachter. 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
39. B.Huang, P.Y.Pan, Q.Li, A.I.Sato, D.E.Levy, J.Bromberg, C.M.Divino, S.H.Chen. 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
40. M.K.Srivastava, L.Zhu, M.Harris-White, U.K.Kar, M.Huang, M.F.Johnson, J.M.Lee, D.Elashoff, R.Strieter, S.Dubinett 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
41. X.Li, R.Loberg, J.Liao, C.Ying, L.A.Snyder, K.J.Pienta, L.K.McCauley. 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
42. H.Lin, E.Lee, K.Hestir, C.Leo, M.Huang, E.Bosch, R.Halenbeck, G.Wu, A.Zhou, D.Behrens 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
43. S.Wei, S.Nandi, V.Chitu, Y.G.Yeung, W.Yu, M.Huang, L.T.Williams, H.Lin, E.R.Stanley. 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
44. A.J.Fleetwood, T.Lawrence, J.A.Hamilton, A.D.Cook. 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
45. G.K.Anagnostopoulos, G.H.Sakorafas, P.Kostopoulos, G.Margantinis, S.Tsiakos, E.Terpos, G.Pavlakis, P.Fortun, D.Arvanitidis. 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
46. Q.D.Wu, J.H.Wang, D.Bouchier-Hayes, H.P.Redmond. 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
47. P.T.Jubinsky, M.K.Short, G.Mutema, R.E.Morris, G.M.Ciraolo, M.Li. 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
48. C.Chavey, F.Bibeau, S.Gourgou-Bourgade, S.Burlinchon, F.Boissière, D.Laune, S.Roques, G.Lazennec. 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
49. Z.G.Fridlender, J.Sun, S.Kim, V.Kapoor, G.Cheng, L.Ling, G.S.Worthen, S.M.Albelda. 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
50. R.B.Holmgaard, D.Zamarin, D.H.Munn, J.D.Wolchok, J.P.Allison. 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
51. R.B.Holmgaard, D.Zamarin, Y.Li, B.Gasmi, D.H.Munn, J.P.Allison, T.Merghoub, J.D.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
52. M.Reich, T.Liefeld, J.Gould, J.Lerner, P.Tamayo, J.P.Mesirov, “GenePattern 2.0” Nature Genetics (2006); 38 no. 5:500-501; http://dx.doi.org/10.1038/ng0506-500
53. C.Robert, J.Schachter, G.V.Long, A.Arance, J.J.Grob, L.Mortier, A.Daud, M.S.Carlino, C.McNeil, M.Lotem 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
54. E.B.1.Garon, N.A.Rizvi, R.Hui, N.Leighl, A.S.Balmanoukian, J.P.Eder, A.Patnaik, C.Aggarwal, M.Gubens, L.Horn 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
55. R.J.Motzer, B.Escudier, D.F.McDermott, S.George, H.J.Hammers, S.Srinivas, S.S.Tykodi, J.A.Sosman, G.Procopio, E.R.Plimack 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