Val-BoroPro Accelerates T Cell Priming via Modulation of Dendritic Cell Trafficking Resulting in Complete Regression of Established Murine Tumors

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Walsh, Meghaan P ^a   Duncan, Brynn ^a   Larabee, Shannon ^a   Krauss, Aviva ^a   Davis, Jessica P E ^a   Cui, Yongzhi ^a   Kim, Su Young ^a   Guimond, Martin ^b   Bachovchin, William ^c   Fry, Terry J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DENDRITIC CELL VACCINE; HY ANTIGEN; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 5; UNCLASSIFIED DRUG; VALINYLBOROPROLINE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL EXPANSION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IMMUNOCOMPETENT CELL; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN DEPLETION; RHABDOMYOSARCOMA; T LYMPHOCYTE SUBPOPULATION; TUMOR REGRESSION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BORONIC ACIDS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; DIPEPTIDES; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOTHERAPY, ADOPTIVE; LYMPH NODES; MALE; MICE; NEOPLASMS; REMISSION INDUCTION; T-LYMPHOCYTES;

EID: 84875019665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058860     Document Type: Article

References (52)

1. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ, (2011) Natural Innate and Adaptive Immunity to Cancer. Annu Rev Immunol 29: 235-271.
2. Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, et al. (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450: 903-907.
3. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD, (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3: 991-998.
4. Dunn GP, Old LJ, Schreiber RD, (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148.
5. Khong HT, Restifo NP, (2002) Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 3: 999-1005.
6. Zitvogel L, Tesniere A, Kroemer G, (2006) Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol 6: 715-727.
7. Mapara MY, Sykes M, (2004) Tolerance and cancer: mechanisms of tumor evasion and strategies for breaking tolerance. J Clin Oncol 22: 1136-1151.
8. Melchionda F, McKirdy MK, Medeiros F, Fry TJ, Mackall CL, (2004) Escape from immune surveillance does not result in tolerance to tumor-associated antigens. J Immunother (1997) 27: 329-338.
9. Gerner MY, Casey KA, Mescher MF, (2008) Defective MHC class II presentation by dendritic cells limits CD4 T cell help for antitumor CD8 T cell responses. J Immunol 181: 155-164.
10. Huang AY, Golumbek P, Ahmadzadeh M, Jaffee E, Pardoll D, et al. (1994) Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 264: 961-965.
11. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, et al. (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13: 1050-1059.
12. Murillo O, Dubrot J, Palazon A, Arina A, Azpilikueta A, et al. (2009) In vivo depletion of DC impairs the anti-tumor effect of agonistic anti-CD137 mAb. Eur J Immunol 39: 2424-2436.
13. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
14. Gerner MY, Mescher MF, (2009) Antigen processing and MHC-II presentation by dermal and tumor-infiltrating dendritic cells. J Immunol 182: 2726-2737.
15. Gabrilovich D, (2004) Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 4: 941-952.
16. Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, et al. (2010) Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med 16: 880-886.
17. Daud AI, Mirza N, Lenox B, Andrews S, Urbas P, et al. (2008) Phenotypic and functional analysis of dendritic cells and clinical outcome in patients with high-risk melanoma treated with adjuvant granulocyte macrophage colony-stimulating factor. J Clin Oncol 26: 3235-3241.
18. Aspord C, Pedroza-Gonzalez A, Gallegos M, Tindle S, Burton EC, et al. (2007) Breast cancer instructs dendritic cells to prime interleukin 13-secreting CD4+ T cells that facilitate tumor development. J Exp Med 204: 1037-1047.
19. Ghiringhelli F, Apetoh L, Housseau F, Kroemer G, Zitvogel L, (2007) Links between innate and cognate tumor immunity. Curr Opin Immunol 19: 224-231.
20. Adams S, Miller GT, Jesson MI, Watanabe T, Jones B, et al. (2004) PT-100, a small molecule dipeptidyl peptidase inhibitor, has potent antitumor effects and augments antibody-mediated cytotoxicity via a novel immune mechanism. Cancer Res 64: 5471-5480.
21. Peters A, (2010) Incretin-based therapies: review of current clinical trial data. Am J Med 123: S28-37.
22. Gorrell MD, (2005) Dipeptidyl peptidase IV and related enzymes in cell biology and liver disorders. Clin Sci (Lond) 108: 277-292.
23. Dolznig H, Schweifer N, Puri C, Kraut N, Rettig WJ, et al. (2005) Characterization of cancer stroma markers: in silico analysis of an mRNA expression database for fibroblast activation protein and endosialin. Cancer Immun 5: 10.
24. Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, et al. (2010) Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 330: 827-830.
25. Santos AM, Jung J, Aziz N, Kissil JL, Pure E, (2009) Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest 119: 3613-3625.
26. Lopez-Otin C, Matrisian LM, (2007) Emerging roles of proteases in tumour suppression. Nat Rev Cancer 7: 800-808.
27. Jones B, Adams S, Miller GT, Jesson MI, Watanabe T, et al. (2003) Hematopoietic stimulation by a dipeptidyl peptidase inhibitor reveals a novel regulatory mechanism and therapeutic treatment for blood cell deficiencies. Blood 102: 1641-1648.
28. Pennisi A, Li X, Ling W, Khan S, Gaddy D, et al. (2009) Inhibitor of DASH proteases affects expression of adhesion molecules in osteoclasts and reduces myeloma growth and bone disease. Br J Haematol 145: 775-787.
29. Lee JJ, Dimina D, Macias MP, Ochkur SI, McGarry MP, et al. (2004) Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305: 1773-1776.
30. Nakano H, Tamura T, Yoshimoto T, Yagita H, Miyasaka M, et al. (1997) Genetic defect in T lymphocyte-specific homing into peripheral lymph nodes. Eur J Immunol 27: 215-221.
31. Weigel BJ, Rodeberg DA, Krieg AM, Blazar BR, (2003) CpG oligodeoxynucleotides potentiate the antitumor effects of chemotherapy or tumor resection in an orthotopic murine model of rhabdomyosarcoma. Clin Cancer Res 9: 3105-3114.
32. Sharp R, Recio JA, Jhappan C, Otsuka T, Liu S, et al. (2002) Synergism between INK4a/ARF inactivation and aberrant HGF/SF signaling in rhabdomyosarcomagenesis. Nat Med 8: 1276-1280.
33. Meadors JL, Cui Y, Chen QR, Song YK, Khan J, et al. (2011) Murine rhabdomyosarcoma is immunogenic and responsive to T-cell-based immunotherapy. Pediatr Blood Cancer 57: 921-929.
34. Melchionda F, Fry TJ, Milliron MJ, McKirdy MA, Tagaya Y, et al. (2005) Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8+ memory cell pool. J Clin Invest 115: 1177-1187.
35. Fry TJ, Shand JL, Milliron M, Tasian SK, Mackall CL, (2009) Antigen loading of DCs with irradiated apoptotic tumor cells induces improved anti-tumor immunity compared to other approaches. Cancer Immunol Immunother 58: 1257-1264.
36. Mele DA, Sampson JF, Huber BT, (2011) Th17 differentiation is the default program for DPP2-deficient T-cell differentiation. Eur J Immunol 41: 1583-1593.
37. Forster R, Davalos-Misslitz AC, Rot A, (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8: 362-371.
38. Rosenberg SA, Dudley ME, Restifo NP, (2008) Cancer immunotherapy. N Engl J Med 359: 1072.
39. Porter DL, Levine BL, Kalos M, Bagg A, June CH, (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733.
40. Kusmartsev S, Vieweg J, (2009) Enhancing the efficacy of cancer vaccines in urologic oncology: new directions. Nat Rev Urol 6: 540-549.
41. Rosenberg SA, Yang JC, Restifo NP, (2004) Cancer immunotherapy: moving beyond current vaccines. Nat Med 10: 909-915.
42. Nemunaitis J, Vukelja SJ, Richards D, Cunningham C, Senzer N, et al. (2006) Phase I trial of PT-100 (PT-100), a cytokine-inducing small molecule, following chemotherapy for solid tumor malignancy. Cancer Invest 24: 553-561.
43. Meany H, Balis FM, Aikin A, Whitcomb P, Murphy RF, et al. (2010) Pediatric phase I trial design using maximum target inhibition as the primary endpoint. J Natl Cancer Inst 102: 909-912.
44. Eager RM, Cunningham CC, Senzer N, Richards DA, Raju RN, et al. (2009) Phase II trial of talabostat and docetaxel in advanced non-small cell lung cancer. Clin Oncol (R Coll Radiol) 21: 464-472.
45. Eager RM, Cunningham CC, Senzer NN, Stephenson J Jr, Anthony SP, et al. (2009) Phase II assessment of talabostat and cisplatin in second-line stage IV melanoma. BMC Cancer 9: 263.
46. Narra K, Mullins SR, Lee HO, Strzemkowski-Brun B, Magalong K, et al. (2007) Phase II trial of single agent Val-boroPro (Talabostat) inhibiting Fibroblast Activation Protein in patients with metastatic colorectal cancer. Cancer Biol Ther 6: 1691-1699.
47. Cristillo AD, Galmin L, Restrepo S, Hudacik L, Suschak J, et al. (2008) HIV-1 Env vaccine comprised of electroporated DNA and protein co-administered with Talabostat. Biochem Biophys Res Commun 370: 22-26.
48. Randolph GJ, Angeli V, Swartz MA, (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 5: 617-628.
49. MartIn-Fontecha A, Sebastiani S, Hopken UE, Uguccioni M, Lipp M, et al. (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198: 615-621.
50. Van Damme J, Struyf S, Wuyts A, Van Coillie E, Menten P, et al. (1999) The role of CD26/DPP IV in chemokine processing. Chem Immunol 72: 42-56.
51. Oravecz T, Pall M, Roderiquez G, Gorrell MD, Ditto M, et al. (1997) Regulation of the receptor specificity and function of the chemokine RANTES (regulated on activation, normal T cell expressed and secreted) by dipeptidyl peptidase IV (CD26)-mediated cleavage. J Exp Med 186: 1865-1872.
52. Rabinovich GA, Gabrilovich D, Sotomayor EM, (2007) Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25: 267-296.