Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer

Frontiers in Oncology

Volumn 3 MAR, Issue , 2013, Pages

  Najjar, Yana G ^a   Finke, James H ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Cancer; Combination therapy; Immune evasion; MDSC; Targeted therapy

Indexed keywords

ACETYLSALICYLIC ACID 3 (NITROXYMETHYL) PHENYL ESTER; AXITINIB; BARDOXOLONE METHYL; BEVACIZUMAB; CYCLOOXYGENASE 2 INHIBITOR; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; FLUOROURACIL; GEMCITABINE; INTERFERON; INTERLEUKIN 6; PHOSPHODIESTERASE V INHIBITOR; RETINOIC ACID; SUNITINIB; UNCLASSIFIED DRUG; VITAMIN D;

ARTICLE; CANCER PROGNOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; HUMAN; INFLAMMATION; KIDNEY CARCINOMA; MYELOID DERIVED SUPPRESSOR CELL; MYELOID PROGENITOR CELL; NEOPLASM; NONHUMAN; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 3 CLINICAL TRIAL (TOPIC); SUPPRESSOR CELL; TUMOR MICROENVIRONMENT;

EID: 84880948301     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00049     Document Type: Article

References (70)

1. Amato, R. J., Hawkins, R. E., Kaufman, H. L., Thompson, J. A., Tomczak, P., Szczylik, C., et al. (2010). Vaccination of metastatic renal cancer patients with MVA-5T4: a randomized, double-blind, placebo-controlled phase III study. Clin. Cancer Res. 16, 5539-5547.
2. Bose, A., Taylor, J. L., Alber, S., Watkins, S. C., Garcia, J. A., Rini, B. I., et al. (2010). Sunitinib facilitates the activation and recruitment of therapeutic anti-tumor immunity in concert with specific vaccination. Int. J. Cancer 129, 2158-2170.
3. Brandau, S., Trellakis, S., Bruderek, K., Schmaltz, D., Steller, G., Elian, M., et al. (2011). Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol. 89, 311-317.
4. Bunt, S. K., Sinha, P., Clements, V. K., Leips, J., and Ostrand-Rosenberg, S. (2006). Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176, 284-290.
5. Dallas, J., Imanirad, I., Rajani, R., Dagan, R., Subbiah, S., Gaa, R., et al. (2012). Response to sunitinib in combination with proton beam radiation in a patient with chondrosarcoma: a case report. J. Med. Case Reports 6, 41.
6. D'Amico, R., Lei, L., Kennedy, B. C., Sisti, J., Ebiana, V., Crisman, C., et al. (2012). The addition of sunitinib to radiation delays tumor growth in a murine model of glioblastoma. Neurol. Res. 34, 252-261.
7. De Santo, C., Serafini, P., Marigo, I., Dolcetti, L., Bolla, M., Del Soldato, P., et al. (2005). Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc. Natl. Acad. Sci. 102, 4185-4190.
8. Diaz-Montero, C. M., Salem, M. L., Nishimura, M. I., Garrett-Mayer, E., Cole, D. J., and Montero, A. J. (2009). Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 58, 49-59.
9. Farsaci, B., Higgins, J. P., and Hodge, J. W. (2012). Consequence of dose scheduling of sunitinib on host immune response elements and vaccine combination therapy. Int. J. Cancer 130, 1948-1959.
10. Filipazzi, P., Huber, V., and Rivoltini, L. (2012). Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol. Immunother. 61, 255-263.
11. Filipazzi, P., Valenti, R., Huber, V., Pilla, L., Canese, P., Iero, M., et al. (2007). Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J. Clin. Oncol. 25, 2546-2553.
12. Finke, J. H., Rini, B., Ireland, J., Rayman, P., Richmond, A., Golshayan, A., et al. (2008). Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin. Cancer Res. 14, 6674-6682.
13. Fujita, M., Kohanbash, G., Fellows-Mayle, W., Hamilton, R. L., Komohara, Y., Decker, S. A., et al. (2011). COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 71, 2664-2674.
14. Gabitass, R. F., Annels, N. E., Stocken, D. D., Pandha, H. A., and Middleton, G. W. (2011). Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13. Cancer Immunol. Immunother. 60, 1419-1430.
15. Gabrilovich, D. I., and Nagaraj, S. (2009). Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174.
16. Gabrilovich, D. I., Ostrand-Rosenberg, S., and Bronte, V. (2012). Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268.
17. Gabrilovich, D. I., Velders, M. P., Sotomayor, E. M., and Kast, W. M. (2001). Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol. 166, 5398-5406.
18. Hanson, E. M., Clements, V. K., Sinha, P., Ilkovitch, D., and Ostrand-Rosenberg, S. (2009). Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J. Immunol. 183, 937-944.
19. Hoechst, B., Ormandy, L. A., Ballmaier, M., Lehner, F., Kruger, C., Manns, M. P., et al. (2008). A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 135, 234-243.
20. Kao, J., Ko, E. C., Eisenstein, S., Sikora, A. G., Fu, S., and Chen, S. H. (2011). Targeting immune suppressing myeloid-derived suppressor cells in oncology. Crit. Rev. Oncol. Hematol. 77, 12-19.
21. Ko, H. J., Kim, Y. J., Kim, Y. S., Chang, W. S., Ko, S. Y., Chang, S. Y., et al. (2007). A combination of chemoimmunotherapies can efficiently break self-tolerance and induce antitumor immunity in a tolerogenic murine tumor model. Cancer Res. 67, 7477-7486.
22. Ko, J. S., Rayman, P., Ireland, J., Swaidani, S., Li, G., Bunting, K. D., et al. (2010). Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res. 70, 3526-3536.
23. Ko, J. S., Zea, A. H., Rini, B. I., Ireland, J. L., Elson, P., Cohen, P., et al. (2009). Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 15, 2148-2157.
24. Kodumudi, K. N., Woan, K., Gilvary, D. L., Sahakian, E., Wei, S., and Djeu, J. Y. (2010). A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin. Cancer Res. 16, 4583-4594.
25. Kujawski, M., Kortylewski, M., Lee, H., Herrmann, A., Kay, H., and Yu, H. (2008). Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J. Clin. Invest. 118, 3367-3377.
26. Kujawski, M., Zhang, C., Herrmann, A., Reckamp, K., Scuto, A., Jensen, M., et al. (2010). Targeting STAT3 in adoptively transferred T cells promotes their in vivo expansion and antitumor effects. Cancer Res. 70, 9599-9610.
27. Kusmartsev, S., Eruslanov, E., Kubler, H., Tseng, T., Sakai, Y., Su, Z., et al. (2008). Oxidative stress regulates expression of VEGFR1 in myeloid cells: link to tumor-induced immune suppression in renal cell carcinoma. J. Immunol. 181, 346-353.
28. Lathers, D. M., Clark, J. I., Achille, N. J., and Young, M. R. (2004). Phase 1B study to improve immune responses in head and neck cancer patients using escalating doses of 25-hydroxyvitamin D3. Cancer Immunol. Immunother. 53, 422-430.
29. Le, H. K., Graham, L., Cha, E., Morales, J. K., Manjili, M. H., and Bear, H. D. (2009). Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int. Immunopharmacol. 9, 900-909.
30. Mandruzzato, S., Solito, S., Falisi, E., Francescato, S., Chiarion-Sileni, V., Mocellin, S., et al. (2009). IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 182, 6562-6568.
31. Meyer, C., Sevko, A., Ramacher, M., Bazhin, A. V., Falk, C. S., Osen, W., et al. (2011). Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc. Natl. Acad. Sci. U.S.A. 108, 17111-17116.
32. Mirza, N., Fishman, M., Fricke, I., Dunn, M., Neuger, A. M., Frost, T. J., et al. (2006). All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res. 66, 9299-9307.
33. Montero, A. J., Diaz-Montero, C. M., Kyriakopoulos, C. E., Bronte, V., and Mandruzzato, S. (2012). Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J. Immunother. 35, 107-115.
34. Motzer, R. J., Bacik, J., Murphy, B. A., Russo, P., and Mazumdar, M. (2002). Interferon-alfa as a comparative treatment for clinical trials of new therapies against advanced renal cell carcinoma. J. Clin. Oncol. 20, 289-296.
35. Motzer, R. J., Hutson, T. E., Tomczak, P., Michaelson, M. D., Bukowski, R. M., Oudard, S., et al. (2009). Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 27, 3584-3590.
36. Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R., Gysemans, C., Beschin, A., et al. (2008). Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111, 4233-4244.
37. Nagaraj, S., Gupta, K., Pisarev, V., Kinarsky, L., Sherman, S., Kang, L., et al. (2007). Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13, 828-835.
38. Nagaraj, S., Youn, J. I., Weber, H., Iclozan, C., Lu, L., Cotter, M. J., et al. (2010). Anti-inflammatory triterpenoid blocks immune suppressive function of MDSCs and improves immune response in cancer. Clin. Cancer Res. 16, 1812-1823.
39. Nefedova, Y., Fishman, M., Sherman, S., Wang, X., Beg, A. A., and Gabrilovich, D. I. (2007). Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res. 67, 11021-11028.
40. Obermajer, N., Muthuswamy, R., Odunsi, K., Edwards, R. P., and Kalinski, P. (2011). PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res. 71, 7463-7470.
41. Ostrand-Rosenberg, S. (2010). Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol. Immunother. 59, 1593-1600.
42. Ozao-Choy, J., Ma, G., Kao, J., Wang, G. X., Meseck, M., Sung, M., et al. (2009). The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 69, 2514-2522.
43. Poschke, I., Mougiakakos, D., Hansson, J., Masucci, G. V., and Kiessling, R. (2010). Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res. 70, 4335-4345.
44. Raychaudhuri, B., Rayman, P., Ireland, J., Ko, J., Rini, B., Borden, E. C., et al. (2011). Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro-oncology 13, 591-599.
45. Rodriguez, P. C., Ernstoff, M. S., Hernandez, C., Atkins, M., Zabaleta, J., Sierra, R., et al. (2009). Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 69, 1553-1560.
46. Rodriguez, P. C., Hernandez, C. P., Quiceno, D., Dubinett, S. M., Zabaleta, J., Ochoa, J. B., et al. (2005). Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med. 202, 931-939.
47. Schmielau, J., and Finn, O. J. (2001). Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 61, 4756-4760.
48. Serafini, P., Borrello, I., and Bronte, V. (2006a). Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol. 16, 53-65.
49. Serafini, P., Meckel, K., Kelso, M., Noonan, K., Califano, J., Koch, W., et al. (2006b). Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J. Exp. Med. 203, 2691-2702.
50. Serafini, P., Mgebroff, S., Noonan, K., and Borrello, I. (2008). Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 68, 5439-5449.
51. Sinha, P., Clements, V. K., Bunt, S. K., Albelda, S. M., and Ostrand-Rosenberg, S. (2007a). Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179, 977-983.
52. Sinha, P., Clements, V. K., Fulton, A. M., and Ostrand-Rosenberg, S. (2007b). Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 67, 4507-4513.
53. Sinha, P., Clements, V. K., and Ostrand-Rosenberg, S. (2005). Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 174, 636-645.
54. Sinha, P., Okoro, C., Foell, D., Freeze, H. H., Ostrand-Rosenberg, S., and Srikrishna, G. (2008). Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J. Immunol. 181, 4666-4675.
55. Sippel, T. R., White, J., Nag, K., Tsvankin, V., Klaassen, M., Kleinschmidt-DeMasters, B. K., et al. (2011). Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin. Cancer Res. 17, 6992-7002.
56. Solito, S., Falisi, E., Diaz-Montero, C. M., Doni, A., Pinton, L., Rosato, A., et al. (2011). A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 118, 2254-2265.
57. Song, X., Krelin, Y., Dvorkin, T., Bjorkdahl, O., Segal, S., Dinarello, C. A., et al. (2005). CD11b+/Gr-1+ immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells. J. Immunol. 175, 8200-8208.
58. Srivastava, M. K., Sinha, P., Clements, V. K., Rodriguez, P., and Ostrand-Rosenberg, S. (2010). Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res. 70, 68-77.
59. Suzuki, E., Kapoor, V., Jassar, A. S., Kaiser, L. R., and Albelda, S. M. (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.
60. Ugel, S., Delpozzo, F., Desantis, G., Papalini, F., Simonato, F., Sonda, N., et al. (2009). Therapeutic targeting of myeloid-derived suppressor cells. Curr. Opin. Pharmacol. 9, 470-481.
61. Umansky, V., and Sevko, A. (2012). Overcoming immunosuppression in the melanoma microenvironment induced by chronic inflammation. Cancer Immunol. Immunother. 61, 275-282.
62. van Cruijsen, H., van der Veldt, A. A., Vroling, L., Oosterhoff, D., Broxterman, H. J., Scheper, R. J., et al. (2008). Sunitinib-induced myeloid lineage redistribution in renal cell cancer patients: CD1c+ dendritic cell frequency predicts progression-free survival. Clin. Cancer Res. 14, 5884-5892.
63. Venton, G., Ducournau, A., Gross, E., Lechevallier, E., Rochwerger, A., Curvale, G., et al. (2012). Complete pathological response after sequential therapy with sunitinib and radiotherapy for metastatic clear cell renal carcinoma. Anticancer Res. 32, 701-705.
64. Vincent, J., Mignot, G., Chalmin, F., Ladoire, S., Bruchard, M., Chevriaux, A., et al. (2010). 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 70, 3052-3061.
65. Vuk-Pavlovic, S., Bulur, P. A., Lin, Y., Qin, R., Szumlanski, C. L., Zhao, X., et al. (2010). Immunosuppressive CD14+HLA-DRlow/-monocytes in prostate cancer. Prostate 70, 443-455.
66. Walter, S., Weinschenk, T., Stenzl, A., Zdrojowy, R., Pluzanska, A., Szczylik, C., et al. (2012). Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat. Med. doi:10.1038/nm.2883. [Epub ahead of print].
67. Xin, H., Zhang, C., Herrmann, A., Du, Y., Figlin, R., and Yu, H. (2009). Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 69, 2506-2513.
68. Youn, J. I., Collazo, M., Shalova, I. N., Biswas, S. K., and Gabrilovich, D. I. (2012). Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J. Leukoc. Biol. 91, 167-181.
69. Youn, J. I., Nagaraj, S., Collazo, M., and Gabrilovich, D. I. (2008). Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181, 5791-5802.
70. Zea, A. H., Rodriguez, P. C., Atkins, M. B., Hernandez, C., Signoretti, S., Zabaleta, J., et al. (2005). Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65, 3044-3048.