Differential Regulation of T-cell mediated anti-tumor memory and cross-protection against the same tumor in lungs versus skin

References

• Beyer M, Kochanek M, Darabi K, Popov A, Jensen M, Endl E, Knolle PA, Thomas RK, von Bergwelt-Baildon M, Debey S, et al. Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 2005;106:2018–25. doi:10.1182/blood-2005-02-0642. PMID:15914560.
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, Chauffert B, Solary E, Bonnotte B, Martin F. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004;34:336–44. doi:10.1002/eji.200324181. PMID:14768038.
   PubMed Web of Science ®Google Scholar
• Golden EB, Chhabra A, Chachoua A, Adams S, Donach M, Fenton-Kerimian M, Friedman K, Ponzo F, Babb JS, Goldberg J, et al. Local radiotherapy and granulocyte-macrophage colony-stimulating factor to generate abscopal responses in patients with metastatic solid tumours: a proof-of-principle trial. Lancet Oncol 2015;16:795–803. doi:10.1016/S1470-2045(15)00054-6. PMID:26095785.
   PubMed Web of Science ®Google Scholar
• Rosenberg SA. Raising the bar: the curative potential of human cancer immunotherapy. Sci Transl Med 2012;4:127ps8. doi:10.1126/scitranslmed.3003634.
   Web of Science ®Google Scholar
• Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012;12:269–81. doi:10.1038/nri3191. PMID:22437939.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443–54. doi:10.1056/NEJMoa1200690. PMID:22658127.
   PubMed Web of Science ®Google Scholar
• Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014;515:568–71. doi:10.1038/nature13954. PMID:25428505.
   PubMed Web of Science ®Google Scholar
• Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002;2:389–400. doi:10.1038/nri821. PMID:12093005.
   PubMed Web of Science ®Google Scholar
• Thornton AM, Shevach EM. Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J Immunol 2000;164:183–90. doi:10.4049/jimmunol.164.1.183. PMID:10605010.
   PubMed Web of Science ®Google Scholar
• Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999;59:3128–33. PMID:10397255.
   PubMed Web of Science ®Google Scholar
• Knutson KL, Dang Y, Lu H, Lukas J, Almand B, Gad E, Azeke E, Disis ML. IL-2 immunotoxin therapy modulates tumor-associated regulatory T cells and leads to lasting immune-mediated rejection of breast cancers in neu-transgenic mice. J Immunol 2006;177:84–91. doi:10.4049/jimmunol.177.1.84. PMID:16785502.
   PubMed Web of Science ®Google Scholar
• Gritzapis AD, Voutsas IF, Baxevanis CN. Ontak reduces the immunosuppressive tumor environment and enhances successful therapeutic vaccination in HER-2/neu-tolerant mice. Cancer Immunol Immunother 2012;61:397–407. doi:10.1007/s00262-011-1113-4. PMID:21928125.
   PubMed Web of Science ®Google Scholar
• Litzinger MT, Fernando R, Curiel TJ, Grosenbach DW, Schlom J, Palena C. IL-2 immunotoxin denileukin diftitox reduces regulatory T cells and enhances vaccine-mediated T-cell immunity. Blood 2007;110:3192–201. doi:10.1182/blood-2007-06-094615. PMID:17616639.
   PubMed Web of Science ®Google Scholar
• Tanaka A, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Cell Res 2017;27:109–18. doi:10.1038/cr.2016.151. PMID:27995907.
   PubMed Web of Science ®Google Scholar
• Bos PD, Plitas G, Rudra D, Lee SY, Rudensky AY. Transient regulatory T cell ablation deters oncogene-driven breast cancer and enhances radiotherapy. J Exp Med 2013;210:2435–66. doi:10.1084/jem.20130762. PMID:24127486.
   PubMed Web of Science ®Google Scholar
• Godfrey DI, Hammond KJ, Poulton LD, Smyth MJ, Baxter AG. NKT cells: facts, functions and fallacies. Immunol Today 2000;21:573–83. doi:10.1016/S0167-5699(00)01735-7. PMID:11094262.
   PubMedGoogle Scholar
• Izhak L, Ambrosino E, Kato S, Parish ST, O'Konek JJ, Weber H, Xia Z, Venzon D, Berzofsky JA, Terabe M. Delicate balance among three types of T cells in concurrent regulation of tumor immunity. Cancer Res 2013;73:1514–23. doi:10.1158/0008-5472.CAN-12-2567. PMID:23319803.
   PubMed Web of Science ®Google Scholar
• Terabe M, Matsui S, Noben-Trauth N, Chen H, Watson C, Donaldson DD, Carbone DP, Paul WE, Berzofsky JA. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway. Nat Immunol 2000;1:515–20. doi:10.1038/82771. PMID:11101874.
   PubMed Web of Science ®Google Scholar
• Park JM, Terabe M, van den Broeke LT, Donaldson DD, Berzofsky JA. Unmasking immunosurveillance against a syngeneic colon cancer by elimination of CD4+ NKT regulatory cells and IL-13. Int J Cancer 2005;114:80–7. doi:10.1002/ijc.20669. PMID:15523692.
   PubMed Web of Science ®Google Scholar
• Terabe M, Swann J, Ambrosino E, Sinha P, Takaku S, Hayakawa Y, Godfrey DI, Ostrand-Rosenberg S, Smyth MJ, Berzofsky JA. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 2005;202:1627–33. doi:10.1084/jem.20051381. PMID:16365146.
   PubMed Web of Science ®Google Scholar
• Terabe M, Robertson FC, Clark K, De Ravin E, Bloom A, Venzon D, Kato S, Mirza A, Berzofsky JA. Blockade of only TGF-β 1 and 2 is sufficient to enhance the efficacy of vaccine and PD-1 checkpoint blockade immunotherapy. OncoImmunology 2017;6:e1308616. doi:10.1080/2162402X.2017.1308616. PMID:28638730.
   PubMed Web of Science ®Google Scholar
• Crowe NY, Coquet JM, Berzins SP, Kyparissoudis K, Keating R, Pellicci DG, Hayakawa Y, Godfrey DI, Smyth MJ. Differential antitumor immunity mediated by NKT cell subsets in vivo. J Exp Med 2005;202:1279–88. doi:10.1084/jem.20050953. PMID:16275765.
   PubMed Web of Science ®Google Scholar
• Izhak L, Ambrosino E, Kato S, Parish ST, O'Konek JJ, Weber H, Xia Z, Venzon D, Berzofsky JA, Terabe M. Delicate balance among three types of T cells in concurrent regulation of tumor immunity. Cancer Res 2013;73:1514–23. doi:10.1158/0008-5472.CAN-12-2567. PMID:23319803.
   PubMed Web of Science ®Google Scholar
• Mosely SI, Prime JE, Sainson RC, Koopmann JO, Wang DY, Greenawalt DM, Ahdesmaki MJ, Leyland R, Mullins S, Pacelli L. Rational selection of syngeneic preclinical tumor models for immunotherapeutic drug discovery. Cancer Immunol Res 2017;5:29–41. doi:10.1158/2326-6066.CIR-16-0114. PMID:27923825.
   PubMed Web of Science ®Google Scholar
• Llosa NJ, Cruise M, Tam A, Wicks EC, Hechenbleikner EM, Taube JM, Blosser RL, Fan H, Wang H, Luber BS, The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov 2015;5:43–51. doi:10.1158/2159-8290.CD-14-0863. PMID:25358689.
   PubMed Web of Science ®Google Scholar
• Devaud C, Westwood JA, John LB, Flynn JK, Paquet-Fifield S, Duong CP, Yong CS, Pegram HJ, Stacker SA, Achen MG, et al. Tissues in different anatomical sites can sculpt and vary the tumor microenvironment to affect responses to therapy. Mol Ther 2014;22:18–27. doi:10.1038/mt.2013.219. PMID:24048441.
   PubMed Web of Science ®Google Scholar
• Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, Clement O, Marcheteau E, Gey A, Fraisse G, et al. Mucosal imprinting of vaccine-induced CD8(+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med 2013;5:172ra20. doi:10.1126/scitranslmed.3004888.
   Web of Science ®Google Scholar
• Nizard M, Roussel H, Diniz MO, Karaki S, Tran T, Voron T, Dransart E, Sandoval F, Riquet M, Rance B, et al. Induction of resident memory T cells enhances the efficacy of cancer vaccine. Nat Commun 2017;8:15221. doi:10.1038/ncomms15221. PMID:28537262.
   PubMed Web of Science ®Google Scholar
• de Velasco G, Miao D, Voss MH, Hakimi AA, Hsieh JJ, Tannir NM, Tamboli P, Appleman LJ, Rathmell WK, Van Allen EM, et al. Tumor mutational load and immune parameters across metastatic renal cell carcinoma risk groups. Cancer Immunol Res 2016;4:820–2. doi:10.1158/2326-6066.CIR-16-0110. PMID:27538576.
   PubMed Web of Science ®Google Scholar
• Lam VC, Lanier LL. NK cells in host responses to viral infections. Curr Opin Immunol 2017;44:43–51. doi:10.1016/j.coi.2016.11.003. PMID:27984782.
   PubMed Web of Science ®Google Scholar
• Pal M, Schwab L, Yermakova A, Mace EM, Claus R, Krahl AC, Woiterski J, Hartwig UF, Orange JS, Handgretinger R, et al. Tumor-priming converts NK cells to memory-like NK cells. Oncoimmunology 2017;6:e1317411. doi:10.1080/2162402X.2017.1317411. PMID:28680749.
   PubMed Web of Science ®Google Scholar
• Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 2003;171:2366–73. doi:10.4049/jimmunol.171.5.2366. PMID:12928383.
   PubMed Web of Science ®Google Scholar
• Bouwer AL, Saunderson SC, Caldwell FJ, Damani TT, Pelham SJ, Dunn AC, Jack RW, Stoitzner P, McLellan AD. NK cells are required for dendritic cell-based immunotherapy at the time of tumor challenge. J Immunol 2014;192:2514–21. doi:10.4049/jimmunol.1202797. PMID:24477907.
   PubMed Web of Science ®Google Scholar
• Bakdash G, Vogelpoel LT, van Capel TM, Kapsenberg ML, de Jong EC. Retinoic acid primes human dendritic cells to induce gut-homing, IL-10-producing regulatory T cells. Mucosal Immunol 2015;8:265–78. doi:10.1038/mi.2014.64. PMID:25027601.
   PubMed Web of Science ®Google Scholar
• Dzutsev A, Hogg A, Sui Y, Solaymani–Mohammadi S, Yu H, Frey B, Wang Y, Berzofsky JA. 2017. Differential T cell homing to colon vs small intestine is imprinted by local CD11c+ antigen presenting cells that determine homing receptors. J. Leuk. Biol 2017;102:1381–1388. doi:10.1189/jlb.1A1116-463RR.
   Google Scholar