Myeloid-derived suppressor cells predict survival of patients with advanced melanoma: Comparison with regulatory T cells and NY-ESO-1- or melan-A-specific T cells

Clinical Cancer Research

Volumn 20, Issue 6, 2014, Pages 1601-1609

  Weide, Benjamin ^a,c   Martens, Alexander ^b   Zelba, Henning ^b   Stutz, Christina ^c   Derhovanessian, Evelyna ^b   Di Giacomo, Anna Maria ^e   Maio, Michele ^e   Sucker, Antje ^c,d   Schilling, Bastian ^c,d   Schadendorf, Dirk ^c,d   Buttner, Petra ^f   Garbe, Claus ^a   Pawelec, Graham ^c  

^a University Medical Centers Hamburg   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e UNIVERSITY HOSPITAL OF SIENA   (Italy)

^f JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD14 ANTIGEN; CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; MELAN A; TRANSCRIPTION FACTOR FOXP3; CTAG1B PROTEIN, HUMAN; MEMBRANE PROTEIN; MLANA PROTEIN, HUMAN; TUMOR ANTIGEN;

ADULT; ADVANCED CANCER; ANTIGEN SPECIFICITY; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CAUSAL ATTRIBUTION; CELL SPECIFICITY; COHORT ANALYSIS; DISTANT METASTASIS; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; MELANOMA; MYELOID DERIVED SUPPRESSOR CELL; OVERALL SURVIVAL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; SURVIVAL RATE; AGED; BONE MARROW CELL; COMPARATIVE STUDY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; T LYMPHOCYTE;

AGED; ANTIGENS, NEOPLASM; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNE TOLERANCE; KAPLAN-MEIER ESTIMATE; MALE; MART-1 ANTIGEN; MELANOMA; MEMBRANE PROTEINS; MIDDLE AGED; MYELOID CELLS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 84896523495     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2508     Document Type: Article

References (49)

1. Neuman HB, Patel A, Ishill N, Hanlon C, Brady MS, Halpern AC, et al. A single-institution validation of the AJCC staging system for stage IV melanoma. Ann Surg Oncol 2008;15:2034-41.
2. Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 2001;19:3635-48.
3. Weide B, Zelba H, Derhovanessian E, Pflugfelder A, Eigentler TK, Di Giacomo AM, et al. Functional T cells targeting NY-ESO-1 or Melan-A are predictive for survival of patients with distant melanoma metastasis. J Clin Oncol. 2012;30:1835-41.
4. McCarter MD, Baumgartner J, Escobar GA, Richter D, Lewis K, Robinson W, et al. Immunosuppressive dendritic and regulatory T cells are upregulated in melanoma patients. Ann Surg Oncol 2007;14:2854-60.
5. Baumgartner JM, Gonzalez R, Lewis KD, Robinson WA, Richter DA, Palmer BE, et al. Increased survival from stage IV melanoma associated with fewer regulatory T Cells. J Surg Res 2009;154:13-20.
6. Poschke I, Mougiakakos D, Hansson J, Masucci GV, Kiessling R. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res 2010;70:4335-45.
7. Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, et al. 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 2007;25:2546-53.
8. Atkins MB, Lotze MT, Dutcher JP, Fisher RI, Weiss G, Margolin K, et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999;17:2105-16.
9. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711-23.
10. Mandruzzato S, Solito S, Falisi E, Francescato S, Chiarion-Sileni V, Mocellin S, et al. IL4Ra+myeloid-derived suppressor cell expansion in cancer patients. J Immunol 2009;182:6562-8.
11. Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 2005;65:3044-8.
12. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
13. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 2012;12:253-68.
14. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin- cyclophosphamide chemotherapy. Cancer Immunol Immunother 2009;58:49-59.
15. Eruslanov E, Neuberger M, Daurkin I, Perrin GQ, Algood C, Dahm P, et al. Circulating and tumor-infiltrating myeloid cell subsets in patients with bladder cancer. Int J Cancer 2012;130:1109-19.
16. Yuan XK, Zhao XK, Xia YC, Zhu X, Xiao P. Increased circulating immunosuppressive CD14(+)HLA-DR(-/low) cells correlate with clinical cancer stage and pathological grade in patients with bladder carcinoma. J Int Med Res 2011;39:1381-91.
17. Schilling B, Sucker A, Griewank K, Zhao F, Weide B, Gorgens A, et al. Vemurafenib reverses immunosuppression by myeloid derived suppressor cells. Int J Cancer 2013;133:1653-63.
18. Solito S, Falisi E, Diaz-Montero CM, Doni A, Pinton L, Rosato A, et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 2011;118:2254-65.
19. Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012:18:1254-61.
20. Kalathil S, Lugade AA, Miller A, Iyer R, Thanavala Y. Higher frequencies of GARP+CTLA-4+Foxp3+ T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T-cell functionality. Cancer Res 2013;73:2435-44.
21. Filipazzi P, Pilla L, Mariani L, Patuzzo R, Castelli C, Camisaschi C, et al. Limited induction of tumor-cross-reactive t cells without ameasurable clinical benefit in early melanoma patients vaccinated with human leukocyte antigen-class i-modified peptides. Clin Cancer Res 2012;18: 6485-96.
22. Gros A, Turcotte S, Ahmadzadeh M, Wunderlich JR, Dudley ME, Rosenberg SA. Myeloid cells obtained from the blood but not from the tumor can suppress T cell proliferation in patients with melanoma. Clin Cancer Res 2012;18:5212-23.
23. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008;133:775-87.
24. Nicholaou T, Ebert LM, Davis ID, McArthur GA, Jackson H, Dimopoulos N, et al. Regulatory T-cell-mediated attenuation of T-cell responses to the NY-ESO-1 ISCOMATRIX vaccine in patients with advanced malignant melanoma. Clin Cancer Res 2009;15:2166-73.
25. Viguier M, Lemaitre F, Verola O, Cho MS, Gorochov G, Dubertret L, et al. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J Immunol 2004;173:1444-53.
26. Cesana GC, DeRaffele G, Cohen S, Moroziewicz D, Mitcham J, Stoutenburg J, et al. Characterization of CD4+CD25+ regulatory T cells in patients treated with high-dose interleukin-2 for metastatic melanoma or renal cell carcinoma. J Clin Oncol 2006;24:1169-77.
27. Gray CP, Arosio P, Hersey P. Association of increased levels of heavychain ferritin with increased CD4+ CD25+ regulatory T-cell levels in patients with melanoma. Clin Cancer Res 2003;9:2551-9.
28. Vence L, Palucka AK, Fay JW, Ito T, Liu YJ, Banchereau J, et al. Circulating tumor antigen-specific regulatory T cells in patients with metastatic melanoma. Proc Natl Acad Sci USA 2007;104:20884-9.
29. Jandus C, Bioley G, Speiser DE, Romero P. Selective accumulation of differentiated FOXP3(+) CD4(+) T cells in metastatic tumor lesions from melanoma patients compared to peripheral blood. Cancer Immunol Immunother 2008;57:1795-805.
30. Ahmadzadeh M, Felipe-Silva A, Heemskerk B, Powell DJJr., Wunderlich JR, Merino MJ, et al. FOXP3 expression accurately defines the population of intratumoral regulatory T cells that selectively accumulate in metastatic melanoma lesions. Blood 2008;112:4953-60.
31. Jacobs JF, Nierkens S, Figdor CG, de Vries IJ, Adema GJ. Regulatory T cells in melanoma: the final hurdle towards effective immunotherapy? Lancet Oncol 2012;13:e32-e42.
32. Filipazzi P, Huber V, Rivoltini L. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol Immunother 2012;61:255-63.
33. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-61.
34. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
35. Nagaraj S, Schrum AG, Cho HI, Celis E, Gabrilovich DI. Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J Immunol 2010;184:3106-16.
36. Nagaraj S, Nelson A, Youn JI, Cheng P, Quiceno D, Gabrilovich DI. Antigen-specific CD4(+) T cells regulate function of myeloid-derived suppressor cells in cancer via retrograde MHC class II signaling. Cancer Res 2012;72:928-38.
37. Poschke I, Mao Y, Adamson L, Salazar-Onfray F, Masucci G, Kiessling R. Myeloid-derived suppressor cells impair the quality of dendritic cell vaccines. Cancer Immunol Immunother 2012;61:827-38.
38. Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, et al. Altered recognition of antigen is a mechanism of CD8+T cell tolerance in cancer. Nat Med 2007;13:828-35.
39. DeSanto C, Serafini P, Marigo I, Dolcetti L, Bolla M, Del Soldato P, et al. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc Natl Acad Sci U S A 2005;102:4185-90.
40. Serafini P, Meckel K, Kelso M, Noonan K, Califano J, Koch W, et al. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006;203:2691-702.
41. Mao Y, Poschke I, Wennerberg E, Pico de Coana Y, Egyhazi Brage S, Schultz I, et al. Melanoma-educated CD14+ cells acquire a myeloidderived suppressor cell phenotype through COX-2-dependent mechanisms. Cancer Res 2013;73:3877-87.
42. Ahmadzadeh M, Rosenberg SA. IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood 2006; 107:2409-14.
43. Berntsen A, Brimnes MK, thor Straten P, Svane IM. Increase of circulating CD4+CD25highFoxp3 +regulatory T cells in patients with metastatic renal cell carcinoma during treatment with dendritic cell vaccination and low-dose interleukin-2. J Immunother 2010;33: 425-34.
44. Veltman JD, Lambers ME, van Nimwegen M, Hendriks RW, Hoogsteden HC, Aerts JG, et al. COX-2 inhibition improves immunotherapy and is associated with decreased numbers of myeloid-derived suppressor cells in mesothelioma. Celecoxib influences MDSC function. BMC Cancer 2010;10:464.
45. Obermajer N, Muthuswamy R, Lesnock J, Edwards RP, Kalinski P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 2011;118:5498-505.
46. Alhamarneh O, Agada F, Madden L, Stafford N, Greenman J. Serum IL10 and circulating CD4(+) CD25(high) regulatory T cell numbers as predictors of clinical outcome and survival in patients with head and neck squamous cell carcinoma. Head Neck 2011;33:415-23.
47. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10: 942-9.
48. Griffiths RW, Elkord E, Gilham DE, Ramani V, Clarke N, Stern PL, et al. Frequency of regulatory T cells in renal cell carcinoma patients and investigation of correlation with survival. Cancer Immunol Immunother 2007;56:1743-53.
49. Schwartzentruber DJ, Lawson DH, Richards JM, Conry RM, Miller DM, Treisman J, et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 2011;364:2119-27.