Inhibition of tumor-induced myeloid-derived suppressor cell function by a nanoparticulated adjuvant

Journal of Immunology

Volumn 186, Issue 1, 2011, Pages 264-274

  Fernández, Audry ^a   Mesa, Circe ^a   Marigo, Ilaria ^b   Dolcetti, Luigi ^b,c   Clavell, Marilyn ^a   Oliver, Liliana ^a   Fernández, Luis E ^a   Bronte, Vincenzo ^b  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

^b VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^c VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; DENDRITIC CELL VACCINE; IMMUNOLOGICAL ADJUVANT; OVALBUMIN; UNCLASSIFIED DRUG; VERY SMALL SIZE PROTEOLIPOSOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; IMMUNE DEFICIENCY; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOMA; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; SPLENOMEGALY; SUPPRESSOR CELL; TUMOR IMMUNITY; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTINEOPLASTIC AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; CANCER VACCINES; CELL LINE, TUMOR; FEMALE; G(M3) GANGLIOSIDE; GROWTH INHIBITORS; LYMPHOMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID CELLS; NANOPARTICLES; NEISSERIA MENINGITIDIS; PROTEOLIPIDS; SARCOMA, EXPERIMENTAL;

EID: 79251551682     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001465     Document Type: Article

References (55)

1. Mocellin, S., S. Mandruzzato, V. Bronte, M. Lise, and D. Nitti. 2004. Part I: vaccines for solid tumours. Lancet Oncol. 5: 681-689.
2. Ostrand-Rosenberg, S. 2004. Animal models of tumor immunity, immunotherapy and cancer vaccines. Curr. Opin. Immunol. 16: 143-150.
3. Carr, A., Z. Mazorra, D. F. Alonso, C. Mesa, O. Valiente, D. E. Gomez, R. Perez, and L. E. Fernandez. 2001. A purified GM3 ganglioside conjugated vaccine induces specific, adjuvant-dependent and non-transient antitumour activity against B16 mouse melanoma in vitro and in vivo. Melanoma Res. 11: 219-227.
4. Gabri, M. R., Z. Mazorra, G. V. Ripoll, C. Mesa, L. E. Fernandez, D. E. Gomez, and D. F. Alonso. 2006. Complete antitumor protection by perioperative immunization with GM3/VSSP vaccine in a preclinical mouse melanoma model. Clin. Cancer Res. 12: 7092-7098.
5. Machiels, J. P., R. T. Reilly, L. A. Emens, A. M. Ercolini, R. Y. Lei, D. Weintraub, F. I. Okoye, and E. M. Jaffee. 2001. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage- colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res. 61: 3689-3697.
6. Tatsumi, T., T. Takehara, T. Kanto, T. Miyagi, N. Kuzushita, Y. Sugimoto, M. Jinushi, A. Kasahara, Y. Sasaki, M. Hori, and N. Hayashi. 2001. Administration of interleukin-12 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines in mouse hepatocellular carcinoma. Cancer Res. 61: 7563-7567.
7. Jonasch, E., C. Wood, P. Tamboli, L. C. Pagliaro, S. M. Tu, J. Kim, P. Srivastava, C. Perez, L. Isakov, and N. Tannir. 2008. Vaccination of metastatic renal cell carcinoma patients with autologous tumour-derived vitespen vaccine: clinical findings. Br. J. Cancer 98: 1336-1341.
8. Rosenberg, S. A., J. C. Yang, and N. P. Restifo. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10: 909-915.
9. Small, E. J., P. F. Schellhammer, C. S. Higano, C. H. Redfern, J. J. Nemunaitis, F. H. Valone, S. S. Verjee, L. A. Jones, and R. M. Hershberg. 2006. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J. Clin. Oncol. 24: 3089-3094.
10. Wood, C., P. Srivastava, R. Bukowski, L. Lacombe, A. I. Gorelov, S. Gorelov, P. Mulders, H. Zielinski, A. Hoos, F. Teofilovici, et al; C-100-12 RCC Study Group. 2008. An adjuvant autologous therapeutic vaccine (HSPPC-96; vitespen) versus observation alone for patients at high risk of recurrence after nephrectomy for renal cell carcinoma: a multicentre, open-label, randomised phase III trial. Lancet 372: 145-154.
11. Malmberg, K. J. 2004. Effective immunotherapy against cancer: a question of overcoming immune suppression and immune escape? Cancer Immunol. Immunother. 53: 879-892.
12. Sica, A., and V. Bronte. 2007. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 117: 1155-1166.
13. Sinha, P., V. K. Clements, S. K. Bunt, S. M. Albelda, and S. Ostrand-Rosenberg. 2007. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179: 977-983.
14. Zou, W. 2006. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6: 295-307.
15. Gallina, G., L. Dolcetti, P. Serafini, C. De Santo, I. Marigo, M. P. Colombo, G. Basso, F. Brombacher, I. Borrello, P. Zanovello, et al. 2006. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 116: 2777-2790.
16. Huang, B., P. Y. Pan, Q. Li, A. I. Sato, D. E. Levy, J. Bromberg, C. M. Divino, and S. H. Chen. 2006. 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. 66: 1123-1131.
17. Nagaraj, S., K. Gupta, V. Pisarev, L. Kinarsky, S. Sherman, L. Kang, D. L. Herber, J. Schneck, and D. I. Gabrilovich. 2007. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13: 828-835.
18. Serafini, P., C. De Santo, I. Marigo, S. Cingarlini, L. Dolcetti, G. Gallina, P. Zanovello, and V. Bronte. 2004. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol. Immunother. 53: 64-72.
19. Liu, C., S. Yu, J. Kappes, J. Wang, W. E. Grizzle, K. R. Zinn, and H. G. Zhang. 2007. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 109: 4336-4342.
20. Suzuki, E., V. Kapoor, A. S. Jassar, L. R. Kaiser, and S. M. Albelda. 2005. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11: 6713-6721.
21. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5: 641-654.
22. Gabrilovich, D. I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9: 162-174.
23. Estevez, F., A. Carr, L. Solorzano, O. Valiente, C. Mesa, O. Barroso, G. V. Sierra, and L. E. Fernandez. 1999. Enhancement of the immune response to poorly immunogenic gangliosides after incorporation into very small size proteoliposomes (VSSP). Vaccine 18: 190-197.
24. Carr, A., E. Rodríguez, Mdel. C. Arango, R. Camacho, M. Osorio, M. Gabri, G. Carrillo, Z. Valdés, Y. Bebelagua, R. Pérez, and L. E. Fernández. 2003. Immunotherapy of advanced breast cancer with a heterophilic ganglioside (NeuGcGM3) cancer vaccine. J. Clin. Oncol. 21: 1015-1021.
25. Ramírez, B. S., E. S. Pestana, G. G. Hidalgo, T. H. García, R. P. Rodríguez, A. Ullrich, and L. E. Férnandez. 2006. Active antimetastatic immunotherapy in Lewis lung carcinoma with self EGFR extracellular domain protein in VSSP adjuvant. Int. J. Cancer 119: 2190-2199.
26. Torréns, I., O. Mendoza, A. Batte, O. Reyes, L. E. Fernández, C. Mesa, and G. Guillén. 2005. Immunotherapy with CTL peptide and VSSP eradicated established human papillomavirus (HPV) type 16 E7-expressing tumors. Vaccine 23: 5768-5774.
27. Mesa, C., J. de León, and L. E. Fernández. 2006. Very small size proteoliposomes derived from Neisseria meningitidis: an effective adjuvant for generation of CTL responses to peptide and protein antigens. Vaccine 24: 2692-2699.
28. Mesa, C., J. De León, K. Rigley, and L. E. Fernández. 2004. Very small size proteoliposomes derived from Neisseria meningitidis: an effective adjuvant for Th1 induction and dendritic cell activation. Vaccine 22: 3045-3052.
29. Bronte, V., P. Serafini, C. De Santo, I. Marigo, V. Tosello, A. Mazzoni, D. M. Segal, C. Staib, M. Lowel, G. Sutter, et al. 2003. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J. Immunol. 170: 270-278.
30. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
31. Kusmartsev, S., S. Nagaraj, and D. I. Gabrilovich. 2005. Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J. Immunol. 175: 4583-4592.
32. Bronte, V., D. B. Chappell, E. Apolloni, A. Cabrelle, M. Wang, P. Hwu, and N. P. Restifo. 1999. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J. Immunol. 162: 5728-5737.
33. Kusmartsev, S., and D. I. Gabrilovich. 2005. STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J. Immunol. 174: 4880-4891.
34. Dolcetti, L., E. Peranzoni, S. Ugel, I. Marigo, A. Fernandez Gomez, C. Mesa, M. Geilich, G. Winkels, E. Traggiai, A. Casati, et al. 2010. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 40: 22-35.
35. Fujimoto, C., Y. Nakagawa, K. Ohara, and H. Takahashi. 2004. Polyriboinosinic polyribocytidylic acid [poly(I:C)]/TLR3 signaling allows class I processing of exogenous protein and induction of HIV-specific CD8+ cytotoxic T lymphocytes. Int. Immunol. 16: 55-63.
36. Ngoi, S. M., M. G. Tovey, and A. T. Vella. 2008. Targeting poly(I:C) to the TLR3-independent pathway boosts effector CD8 T cell differentiation through IFN-alpha/beta. J. Immunol. 181: 7670-7680.
37. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Heinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184: 1413-1424.
38. Luft, T., K. C. Pang, E. Thomas, P. Hertzog, D. N. Hart, J. Trapani, and J. Cebon. 1998. Type I IFNs enhance the terminal differentiation of dendritic cells. J. Immunol. 161: 1947-1953. (Pubitemid 28387618)
39. Kurts, C. 2008. CD11c: not merely a murine DC marker, but also a useful vaccination target. Eur. J. Immunol. 38: 2072-2075.
40. Parmiani, G., C. Castelli, L. Pilla, M. Santinami, M. P. Colombo, and L. Rivoltini. 2007. Opposite immune functions of GM-CSF administered as vaccine adjuvant in cancer patients. Ann. Oncol. 18: 226-232.
41. Serafini, P., R. Carbley, K. A. Noonan, G. Tan, V. Bronte, and I. Borrello. 2004. High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells. Cancer Res. 64: 6337-6343.
42. Almand, B., J. I. Clark, E. Nikitina, J. van Beynen, N. R. English, S. C. Knight, D. P. Carbone, and D. I. Gabrilovich. 2001. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 166: 678-689.
43. Nagaraj, S., and D. I. Gabrilovich. 2010. Myeloid-derived suppressor cells in human cancer. Cancer J. 16: 348-353.
44. Zea, A. H., P. C. Rodriguez, M. B. Atkins, C. Hernandez, S. Signoretti, J. Zabaleta, D. McDermott, D. Quiceno, A. Youmans, A. O'Neill, et al. 2005. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65: 3044-3048.
45. Brys, L., A. Beschin, G. Raes, G. H. Ghassabeh, W. Noël, J. Brandt, F. Brombacher, and P. De Baetselier. 2005. Reactive oxygen species and 12/15-lipoxygenase contribute to the antiproliferative capacity of alternatively activated myeloid cells elicited during helminth infection. J. Immunol. 174: 6095-6104.
46. Goñi, O., P. Alcaide, and M. Fresno. 2002. Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+ )immature myeloid suppressor cells. Int. Immunol. 14: 1125-1134.
47. Birklé, S., G. Zeng, L. Gao, R. K. Yu, and J. Aubry. 2003. Role of tumor-associated gangliosides in cancer progression. Biochimie 85: 455-463.
48. Shurin, G. V., M. R. Shurin, S. Bykovskaia, J. Shogan, M. T. Lotze, and E. M. Barksdale, Jr. 2001. Neuroblastoma-derived gangliosides inhibit dendritic cell generation and function. Cancer Res. 61: 363-369.
49. Bogdan, C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
50. Movahedi, K., M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, A. Beschin, P. De Baetselier, and J. A. Van Ginderachter. 2008. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111: 4233-4244.
51. Zhu, B., Y. Bando, S. Xiao, K. Yang, A. C. Anderson, V. K. Kuchroo, and S. J. Khoury. 2007. CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 179: 5228-5237.
52. Kusmartsev, S., and D. I. Gabrilovich. 2003. Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species. J. Leukoc. Biol. 74: 186-196.
53. De Santo, C., P. Serafini, I. Marigo, L. Dolcetti, M. Bolla, P. Del Soldato, C. Melani, C. Guiducci, M. P. Colombo, M. Iezzi, et al. 2005. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc. Natl. Acad. Sci. USA 102: 4185-4190.
54. Serafini, P., K. Meckel, M. Kelso, K. Noonan, J. Califano, W. Koch, L. Dolcetti, V. Bronte, and I. Borrello. 2006. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J. Exp. Med. 203: 2691-2702.
55. Morecki, S., Y. Gelfand, E. Yacovlev, O. Eizik, Y. Shabat, and S. Slavin. 2008. CpG-induced myeloid CD11b+Gr-1+ cells efficiently suppress T cell-mediated immunoreactivity and graft-versus-host disease in a murine model of allogeneic cell therapy. Biol. Blood Marrow Transplant. 14: 973-984.