Distinct myeloid suppressor cell subsets correlate with plasma IL-6 and IL-10 and reduced interferon-alpha signaling in CD4 + T cells from patients with GI malignancy

Cancer Immunology, Immunotherapy

Volumn 60, Issue 9, 2011, Pages 1269-1279

  Mundy Bosse, Bethany L ^a,b   Young, Gregory S ^a,b   Bauer, Todd ^b   Binkley, Elaine ^b   Bloomston, Mark ^a,b   Bill, Matthew A ^b   Bekaii Saab, Tanios ^b   Carson III, William E ^a,b   Lesinski, Gregory B ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Immune suppression; Interleukin 10; Interleukin 6; Myeloid derived suppressor cell

Indexed keywords

ALPHA INTERFERON; CD11B ANTIGEN; CD14 ANTIGEN; CD15 ANTIGEN; CD33 ANTIGEN; CD4 ANTIGEN; CYTOKINE; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 6; STAT1 PROTEIN;

ADULT; AGED; ARTICLE; BONE MARROW CELL; CANCER PATIENT; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; CORRELATION FUNCTION; DIGESTIVE SYSTEM CANCER; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION;

ADULT; AGED; AGED, 80 AND OVER; CD4-POSITIVE T-LYMPHOCYTES; GASTROINTESTINAL NEOPLASMS; HUMANS; INTERFERON-ALPHA; INTERLEUKIN-10; INTERLEUKIN-6; MALE; MIDDLE AGED; MYELOID CELLS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

EID: 80054711965     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1029-z     Document Type: Article

References (52)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics. CA Cancer J Clin 59:225-249
2. Chaudry MA, Sales K, Ruf P, Lindhofer H, Winslet MC (2007) EpCAM an immunotherapeutic target for gastrointestinal malignancy: current experience and future challenges. Br J Cancer 96:1013-1019 (Pubitemid 46608303)
3. Dougan M, Dranoff G (2009) Immune therapy for cancer. Annu Rev Immunol 27:83-117
4. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI (2001) Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 166:678-689 (Pubitemid 32038493)
5. Ugel S, Delpozzo F, Desantis G, Papalini F, Simonato F, Sonda N, Zilio S, Bronte V (2009) Therapeutic targeting of myeloidderived suppressor cells. Curr Opin Pharmacol 9:470-481
6. Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162-174
7. Tisdale MJ (2010) Cancer cachexia. Curr Opin Gastroenterol 26:146-151
8. Liao WC, Lin JT, Wu CY, Huang SP, Lin MT, Wu AS, Huang YJ, Wu MS (2008) Serum interleukin-6 level but not genotype predicts survival after resection in stages II and III gastric carcinoma. Clin Cancer Res 14:428-434 (Pubitemid 351226110)
9. Chung YC, Chang YF (2003) Serum interleukin-6 levels reflect the disease status of colorectal cancer. J Surg Oncol 83:222-226
10. De Vita F, Orditura M, Galizia G, Romano C, Infusino S, Auriemma A, Lieto E, Catalano G (1999) Serum interleukin-10 levels in patients with advanced gastrointestinal malignancies. Cancer 86:1936-1943
11. Karin M, Greten FR (2005) NF-kappa B: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5:749-759 (Pubitemid 41400849)
12. Stewart TJ, Greeneltch KM, Reid JE, Liewehr DJ, Steinberg SM, Liu K, Abrams SI (2009) Interferon regulatory factor-8 modulates the development of tumor-induced CD11bGr-1 myeloid cells. J Cell Mol Med
13. Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S (2007) Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 67:10019-10026 (Pubitemid 47621253)
14. Li H, Han Y, Guo Q, Zhang M, Cao X (2009) Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 182:240-249
15. Nagaraj S, Schrum AG, Cho HI, Celis E, Gabrilovich DI (2010) Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J Immunol 184:3106-3116
16. Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, Golshayan A, Rayman PA, Wood L, Garcia J, Dreicer R, Bukowski R, Finke JH (2009) Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 15:2148-2157
17. Ostrand-Rosenberg S Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother
18. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S (2010) Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res 70:68-77
19. Mazzoni A, Bronte V, Visintin A, Spitzer JH, Apolloni E, Serafini P, Zanovello P, Segal DM (2001) Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J Immunol 168:689-695 (Pubitemid 34049569)
20. Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182:4499-4506
21. Morales JK, Kmieciak M, Graham L, Feldmesser M, Bear HD, Manjili MH (2009) Adoptive transfer of HER2/neu-specific T cells expanded with alternating gamma chain cytokines mediate tumor regression when combined with the depletion of myeloidderived suppressor cells. Cancer Immunol Immunother 58:941-953
22. Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S (2007) Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 179:977-983
23. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S (2007) Prostaglandin E2 promotes tumor progression by inducing myeloid- derived suppressor cells. Cancer Res 67:4507-4513 (Pubitemid 46815102)
24. Sinha P, Clements VK, 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 (Pubitemid 40094255)
25. Kusmartsev S, Gabrilovich DI (2005) STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J Immunol 174:4880-4891
26. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI (2008) Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 181:5791-5802
27. Nagaraj S, Youn JI, Weber H, Iclozan C, Lu L, Cotter MJ, Meyer C, Becerra CR, Fishman M, Antonia S, Sporn MB, Liby KT, Rawal B, Lee JH, Gabrilovich DI (2010) Anti-inflammatory triterpenoid blocks immune suppressive function of MDSCs and improves immune response in cancer. Clin Cancer Res 16:1812-1823
28. De Santo C, Salio M, Masri SH, Lee LY, Dong T, Speak AO, Porubsky S, Booth S, Veerapen N, Besra GS, Grone HJ, Platt FM, Zambon M, Cerundolo V (2008) Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid- derived suppressor cells in mice and humans. J Clin Invest 118:4036-4048
29. Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, Castelli C, Mariani L, Parmiani G, Rivoltini L (2007) Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocytemacrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol 25:2546-2553 (Pubitemid 47041228)
30. Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O'Neill A, Mier J, Ochoa AC (2005) Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 65:3044-3048 (Pubitemid 40524582)
31. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ (2009) Increased circulating myeloidderived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58:49-59
32. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, De Baetselier P, Van Ginderachter JA (2008) Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111:4233-4244
33. + HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res 70:4335-4345
34. Hoechst B, Ormandy LA, Ballmaier M, Lehner F, Kruger C, Manns MP, Greten TF, Korangy F (2008) A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(?)CD25(?)Foxp3(?) T cells. Gastroenterology 135:234-243 (Pubitemid 351899008)
35. Gordon IO, Freedman RS (2006) Defective antitumor function of monocyte-derived macrophages from epithelial ovarian cancer patients. Clin Cancer Res 12:1515-1524
36. Ugurel S, Uhlig D, Pfohler C, Tilgen W, Schadendorf D, Reinhold U (2004) Down-regulation of HLA class II and costimulatory CD86/B7-2 on circulating monocytes from melanoma patients. Cancer Immunol Immunother 53:551-559 (Pubitemid 38680262)
37. Brassard DL, Grace MJ, Bordens RW (2002) Interferon-alpha as an immunotherapeutic protein. J Leukoc Biol 71:565-581
38. Biron CA (2001) Interferons alpha and beta as immune regulators- a new look. Immunity 14:661-664 (Pubitemid 32592413)
39. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali- Krishna K (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202:637-650 (Pubitemid 41248415)
40. Le Bon A, Durand V, Kamphuis E, Thompson C, Bulfone-Paus S, Rossmann C, Kalinke U, Tough DF (2006) Direct stimulation of T cells by type I IFN enhances the CD8? T cell response during cross-priming. J Immunol 176:4682-4689
41. Lesinski GB, Anghelina M, Zimmerer J, Bakalakos T, Badgwell B, Parihar R, Hu Y, Becknell B, Abood G, Chaudhury AR, Magro C, Durbin J, Carson WE III (2003) The antitumor effects of IFN-αlpha are abrogated in a STAT1-deficient mouse. J Clin Invest 112:170-180 (Pubitemid 38056353)
42. Lesinski GB, Kondadasula SV, Crespin T, Shen L, Kendra K, Walker M, Carson WE III (2004) Multiparametric flow cytometric analysis of inter-patient variation in STAT1 phosphorylation following interferon Alfa immunotherapy. J Natl Cancer Inst 96:1331-1342 (Pubitemid 39264122)
43. Critchley-Thorne RJ, Yan N, Nacu S, Weber J, Holmes SP, Lee PP (2007) Down-regulation of the interferon signaling pathway in T lymphocytes from patients with metastatic melanoma. PLoS Med 4:e176
44. Mundy BL (2010) Myeloid-derived suppressor cells and decreased interferon responsiveness in tumor-bearing mice. International Society for Biological Therapy of Cancer, Washington, DC
45. Lesinski GB, Trefry J, Brasdovich M, Kondadasula SV, Sackey K, Zimmerer JM, Chaudhury AR, Yu L, Zhang X, Crespin TR, Walker MJ, Carson WE III (2007) Melanoma cells exhibit variable signal transducer and activator of transcription 1 phosphorylation and a reduced response to IFN-αlpha compared with immune effector cells. Clin Cancer Res 13:5010-5019 (Pubitemid 47502065)
46. Lechner MG, Liebertz DJ, Epstein AL (2010) Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 185:2273-2284
47. Michael Kutner CN, Neter J, Li W (2004) Applied linear statistics model, 5th edn. McGraw-Hill, Irwin
48. Ko JS, Rayman P, Ireland J, Swaidani S, Li G, Bunting KD, Rini B, Finke JH, Cohen PA (2010) Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res 70:3526-3536
49. Strohlein MA, Heiss MM (2009) Intraperitoneal immunotherapy to prevent peritoneal carcinomatosis in patients with advanced gastrointestinal malignancies. J Surg Oncol 100:329-330
50. Jaffee EM, Hruban RH, Biedrzycki B, Laheru D, Schepers K, Sauter PR, Goemann M, Coleman J, Grochow L, Donehower RC, Lillemoe KD, O'Reilly S, Abrams RA, Pardoll DM, Cameron JL, Yeo CJ (2001) Novel allogeneic granulocyte- macrophage colony- stimulating factor-secreting tumor vaccine for pancreatic cancer: a phase I trial of safety and immune activation. J Clin Oncol 19:145-156 (Pubitemid 32063491)
51. Thomas AM, Santarsiero LM, Lutz ER, Armstrong TD, Chen YC, Huang LQ, Laheru DA, Goggins M, Hruban RH, Jaffee EM (2004) Mesothelin-specific CD8(?) T cell responses provide evidence of in vivo cross-priming by antigen-presenting cells in vaccinated pancreatic cancer patients. J Exp Med 200:297-306 (Pubitemid 39031249)
52. Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, Lehner F, Manns MP, Greten TF, Korangy F (2009) Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 50:799-807