Toll-like receptor agonist therapy can profoundly augment the antitumor activity of adoptively transferred CD8+ T cells without host preconditioning

Journal for ImmunoTherapy of Cancer

Volumn 4, Issue 1, 2016, Pages

  Nelson, Michelle H ^a   Bowers, Jacob S ^a   Bailey, Stefanie R ^a   Diven, Marshall A ^a   Fugle, Caroline W ^a   Kaiser, Andrew D M ^b   Wrzesinski, Claudia ^b   Liu, Bei ^a   Restifo, Nicholas P ^b   Paulos, Chrystal M ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Adoptive immunotherapy; CD8+ T lymphocytes; Innate immunity; Total body Irradiation

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GLYCOPROTEIN GP 100; INTERLEUKIN 2; LIPOPOLYSACCHARIDE; MELANOCYTE PROTEIN PMEL 17; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHORYL LIPID A; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FLOW CYTOMETRY; FUNCTIONS OF THE HEMIC, LYMPHATIC AND RETICULOENDOTHELIAL SYSTEMS; INNATE IMMUNITY; IRRADIATION; LYMPHODEPLETION; MELANOMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPLEEN CELL; TREATMENT OUTCOME; TUMOR GROWTH; TUMOR VOLUME; VACCINATION;

EID: 84997719834     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-016-0110-8     Document Type: Article

References (57)

1. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915-20.
2. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003;361(9356):512-9.
3. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science. 2001;291(5505):881-4.
4. McFall-Ngai MJ, Ruby EG. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science. 1991;254(5037):1491-4.
5. Nelson MH, Diven MA, Huff LW, Paulos CM. Harnessing the Microbiome to Enhance Cancer Immunotherapy. J Immunol Res. 2015;2015:368736.
6. Berg RD. The indigenous gastrointestinal microflora. Trends Microbiol. 1996;4(11):430-5.
7. Savage DC. Microorganisms associated with epithelial surfaces and stability of the indigenous gastrointestinal microflora. Nahrung. 1987;31(5-6):383-95.
8. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12(12):1365-71.
9. Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res. 2000;6(3):205-14.
10. Hill GR, Ferrara JL. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 2000;95(9):2754-9.
11. Paulos CM, Wrzesinski C, Kaiser A, Hinrichs CS, Chieppa M, Cassard L, et al. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J Clin Invest. 2007;117(8):2197-204.
12. Viaud S, Daillere R, Boneca IG, Lepage P, Langella P, Chamaillard M, et al. Gut microbiome and anticancer immune response: really hot Sh*t! Cell Death Differ. 2015;22(2):199-214.
13. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342(6161):967-70.
14. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342(6161):971-6.
15. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 2005;23(10):2346-57.
16. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol. 2008;26(32):5233-9.
17. Stevanovic S, Draper LM, Langhan MM, Campbell TE, Kwong ML, Wunderlich JR, et al. Complete regression of metastatic cervical cancer after treatment with human papillomavirus-targeted tumor-infiltrating T cells. J Clin Oncol. 2015;33(14):1543-50.
18. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):177ra38.
19. Brentjens RJ, Riviere I, Park JH, Davila ML, Wang X, Stefanski J, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118(18):4817-28.
20. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116(20):4099-102.
21. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509-18.
22. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725-33.
23. Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science. 2014;344(6184):641-5.
24. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med. 2005;202(7):907-12.
25. Turk MJ, Guevara-Patino JA, Rizzuto GA, Engelhorn ME, Sakaguchi S, Houghton AN. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med. 2004;200(6):771-82.
26. Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol. 2005;5(8):641-54.
27. Antony PA, Piccirillo CA, Akpinarli A, Finkelstein SE, Speiss PJ, Surman DR, et al. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol. 2005;174(5):2591-601.
28. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050-9.
29. Wrzesinski C, Paulos CM, Gattinoni L, Palmer DC, Kaiser A, Yu Z, et al. Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J Clin Invest. 2007;117(2):492-501.
30. Zhang Y, Louboutin JP, Zhu J, Rivera AJ, Emerson SG. Preterminal host dendritic cells in irradiated mice prime CD8+ T cell-mediated acute graft-versus-host disease. J Clin Invest. 2002;109(10):1335-44.
31. Kawai T, Akira S. TLR signaling. Cell Death Differ. 2006;13(5):816-25.
32. Bowers J, Nelson M, Kundimi S, Bailey S, Huff L, Schwartz K, et al. Dendritic cells in irradiated mice trigger the functional plasticity and antitumor activity of adoptively transferred Tc17 cells via IL-12 signaling. Clinical Cancer Res. 2015;21(11):2546-57.
33. Rapoport AP, Aqui NA, Stadtmauer EA, Vogl DT, Xu YY, Kalos M, et al. Combination immunotherapy after ASCT for multiple myeloma using MAGE-A3/Poly-ICLC immunizations followed by adoptive transfer of vaccine-primed and costimulated autologous T cells. Clin Cancer Res. 2014;20(5):1355-65.
34. Rapoport AP, Aqui NA, Stadtmauer EA, Vogl DT, Fang HB, Cai L, et al. Combination immunotherapy using adoptive T-cell transfer and tumor antigen vaccination on the basis of hTERT and survivin after ASCT for myeloma. Blood. 2011;117(3):788-97.
35. Brody JD, Ai WZ, Czerwinski DK, Torchia JA, Levy M, Advani RH, et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J Clin Oncol. 2010;28(28):4324-32.
36. Manegold C, Gravenor D, Woytowitz D, Mezger J, Hirsh V, Albert G, et al. Randomized phase II trial of a toll-like receptor 9 agonist oligodeoxynucleotide, PF-3512676, in combination with first-line taxane plus platinum chemotherapy for advanced-stage non-small-cell lung cancer. J Clin Oncol. 2008;26(24):3979-86.
37. Ayari C, Bergeron A, LaRue H, Menard C, Fradet Y. Toll-like receptors in normal and malignant human bladders. J Urol. 2011;185(5):1915-21.
38. Speiser DE, Lienard D, Rufer N, Rubio-Godoy V, Rimoldi D, Lejeune F, et al. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest. 2005;115(3):739-46.
39. Paulos CM, Kaiser A, Wrzesinski C, Hinrichs CS, Cassard L, Boni A, et al. Toll-like receptors in tumor immunotherapy. Clin Cancer Res. 2007;13(18 Pt 1):5280-9.
40. Klebanoff CA, Khong HT, Antony PA, Palmer DC, Restifo NP. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol. 2005;26(2):111-7.
41. Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res. 1991;262:3-11.
42. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science. 2002;298(5594):850-4.
43. Su EW, Moore CJ, Suriano S, Johnson CB, Songalia N, Patterson A, et al. IL-2Ralpha mediates temporal regulation of IL-2 signaling and enhances immunotherapy. Sci Transl Med. 2015;7(311):311ra170.
44. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408(6813):740-5.
45. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, et al. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol. 2002;168(9):4531-7.
46. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med. 2001;194(6):863-9.
47. Hamilton SE, Jameson SC. The nature of the lymphopenic environment dictates protective function of homeostatic-memory CD8+ T cells. Proc Natl Acad Sci U S A. 2008;105(47):18484-9.
48. Appay V, Jandus C, Voelter V, Reynard S, Coupland SE, Rimoldi D, et al. New generation vaccine induces effective melanoma-specific CD8+ T cells in the circulation but not in the tumor site. J Immunol. 2006;177(3):1670-8.
49. Restifo NP. Building better vaccines: how apoptotic cell death can induce inflammation and activate innate and adaptive immunity. Curr Opin Immunol. 2000;12(5):597-603.
50. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 2006;314(5796):126-9.
51. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, Carroll RG, et al. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med. 2008;14(12):1390-5.
52. Woo SR, Corrales L, Gajewski TF. Innate immune recognition of cancer. Annu Rev Immunol. 2015;33:445-74.
53. Zitvogel L, Galluzzi L, Viaud S, Vetizou M, Daillere R, Merad M, et al. Cancer and the gut microbiota: an unexpected link. Sci Transl Med. 2015;7(271):271ps1.
54. Atkins M. Immunotherapy Combinations With Checkpoint Inhibitors in Metastatic Melanoma: Current Approaches and Future Directions. Semin Oncol. 2015;42 Suppl 3:S12-9.
55. Daud A. Current and Emerging Perspectives on Immunotherapy for Melanoma. Semin Oncol. 2015;42 Suppl 3:S3-11.
56. Derer A, Frey B, Fietkau R, Gaipl US. Immune-modulating properties of ionizing radiation: rationale for the treatment of cancer by combination radiotherapy and immune checkpoint inhibitors. Cancer Immunol Immunother. 2015.
57. Sathyanarayanan V, Neelapu SS. Cancer immunotherapy: Strategies for personalization and combinatorial approaches. Mol Oncol. 2015;9(10):2043-53.