IL-2 therapy promotes suppressive ICOS+ Treg expansion in melanoma patients

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 99-110

  Sim, Geok Choo ^a   Martin Orozco, Natalia ^b   Jin, Lei ^a   Yang, Yan ^a   Wu, Sheng ^a   Washington, Edwina ^a   Sanders, Deborah ^a   Lacey, Carol ^a   Wang, Yijun ^a   Vence, Luis ^a   Hwu, Patrick ^a   Radvanyi, Laszlo ^a  

^a Department of Melanoma Medical Oncology ^*  (United States)

^b Bellicum Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; CD14 ANTIGEN; CD16 ANTIGEN; CD19 ANTIGEN; CD27 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD39 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; CD56 ANTIGEN; CD57 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; GRANZYME B; INDUCIBLE T CELL COSTIMULATOR; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; KI 67 ANTIGEN; L SELECTIN; NATURAL KILLER CELL RECEPTOR NKG2D; RECOMBINANT INTERLEUKIN 2; RECOMBINANT MAGE A3 VACCINE; RECOMBINANT VACCINE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR VACCINE; UNCLASSIFIED DRUG;

ADULT; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER PATIENT; CELL EXPANSION; CELL LINEAGE; CLINICAL ARTICLE; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; METASTATIC MELANOMA; MULTIPLE CYCLE TREATMENT; NATURAL KILLER CELL; OUTCOME ASSESSMENT; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84892920498     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI46266     Document Type: Article

References (66)

1. Atkins MB, 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(7):2105-2116.
2. Dutcher J. Current status of interleukin-2 therapy for metastatic renal cell carcinoma and metastatic melanoma. Oncology (Williston Park). 2002; 16(11 suppl 13):4-10.
3. Kirkwood JM, et al. Next generation of immunotherapy for melanoma. J Clin Oncol. 2008; 26(20):3445-3455.
4. Whittington R, Faulds D. Interleukin-2. A review of its pharmacological properties and therapeutic use in patients with cancer. Drugs. 1993;46(3):446-514.
5. Fyfe G, et al. Results of treatment of 255 patients with metastatic renal cell carcinoma who received high-dose recombinant interleukin-2 therapy. J Clin Oncol. 1995;13(3):688-696.
6. Dudley ME, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol. 2008;26(32):5233-5239.
7. Huang J, et al. Survival, persistence, and progressive differentiation of adoptively transferred tumorreactive T cells associated with tumor regression. J Immunother. 2005;28(3):258-267.
8. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol. 2009;21(2):233-240.
9. Schwartzentruber DJ, et al. gp100 peptide vaccine interleukin-2 in patients with advanced melanoma. N Engl J Med. 2011;364(22):2119-2127.
10. DiSanto JP. Cytokines: shared receptors, distinct functions. Curr Biol. 1997;7(7):R424-R426.
11. Imada K, et al. Stat5b is essential for natural killer cell-mediated proliferation cytolytic activity. J Exp Med. 1998;188(11):2067-2074.
12. Moriggl R, et al. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity. 1999;10(2):249-259.
13. Harlin H, et al. Tumor progression despite massive influx of activated CD8(+) T cells in a patient with malignant melanoma ascites. Cancer Immunol Immunother. 2006;55(10):1185-1197.
14. Letsch A, et al. High frequencies of circulating melanoma-reactive CD8+ T cells in patients with advanced melanoma. Int J Cancer. 2000; 87(5):659-664.
15. McMannis JD, et al. In vivo effects of recombinant IL-2. I. Isolation of circulating Leu-19+ lymphokine- activated killer effector cells from cancer patients receiving recombinant IL-2. J Immunol. 1988;140(4):1335-1340.
16. Ahmadzadeh M, Rosenberg SA. IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood. 2006;107(6):2409-2414.
17. Cesana GC, 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(7):1169-1177.
18. Wei S, et al. Interleukin-2 administration alters the CD4+FOXP3+ T-cell pool tumor trafficking in patients with ovarian carcinoma. Cancer Res. 2007; 67(15):7487-7494.
19. Brandenburg S, et al. IL-2 induces in vivo suppression by CD4(+)CD25(+)Foxp3(+) regulatory T cells. Eur J Immunol. 2008;38(6):1643-1653.
20. Antony PA, Restifo NP. CD4+CD25+ T regulatory cells, immunotherapy of cancer, interleukin-2. J Immunother. 2005;28(2):120-128.
21. Chaput N, et al. Regulatory T cells prevent CD8 T cell maturation by inhibiting CD4 Th cells at tumor sites. J Immunol. 2007;179(8):4969-4978.
22. Linehan DC, Goedegebuure PS. CD25+ CD4+ regulatory T-cells in cancer. Immunol Res. 2005; 32(1-3):155-168.
23. Ghiringhelli F, Menard C, Martin F, Zitvogel L. The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunol Rev. 2006;214:229-238.
24. Curotto de Lafaille MA, Lafaille JJ. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity. 2009; 30(5):626-635.
25. Curiel, TJ. Regulatory T cells and treatment of cancer. Curr Opin Immunol. 2008;20(2):241-246.
26. Royal RE, et al. Correlates of response to IL-2 therapy in patients treated for metastatic renal cancer melanoma. Cancer J Sci Am. 1996;2(2):91-98.
27. Phan GQ, et al. Factors associated with response to high-dose interleukin-2 in patients with metastatic melanoma. J Clin Oncol. 2001;19(15):3477-3482.
28. Caligiuri MA, et al. Selective modulation of human natural killer cells in vivo after prolonged infusion of low dose recombinant interleukin 2. J Clin Invest. 1993;91(1):123-132.
29. Fehniger TA, et al. Potential mechanisms of human natural killer cell expansion in vivo during low-dose IL-2 therapy. J Clin Invest. 2000;106(1):117-124.
30. Lee SK, Gasser S. The role of natural killer cells in cancer therapy. Front Biosci (Elite Ed). 2010; 2:380-391.
31. Poli A, et al. CD56bright natural killer (NK) cells: an important NK cell subset. Immunology. 2009; 126(4):458-465.
32. Coquerelle C, et al. Anti-CTLA-4 treatment induces IL-10-producing ICOS+ regulatory T cells displaying IDO-dependent anti-inflammatory properties in a mouse model of colitis. Gut. 2009;58(10):1363-1373.
33. Herman AE, Freeman GJ, Mathis D, Benoist C. CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J Exp Med. 2004;199(11):1479-1489.
34. Vonderheide RH, et al. Tremelimumab in combination with exemestane in patients with advanced breast cancer and treatment-associated modulation of inducible costimulator expression on patient T cells. Clin Cancer Res. 2010;16(13):3485-3494.
35. Ito T, et al. Two functional subsets of FOXP3+ regulatory T cells in human thymus periphery. Immunity. 2008;28(6):870-880.
36. Strauss L, et al. Expression of ICOS on human melanoma-infiltrating CD4+CD25highFoxp3+ T regulatory cells: implications impact on tumormediated immune suppression. J Immunol. 2008; 180(5):2967-2980.
37. Vocanson M, et al. Inducible costimulator (ICOS) is a marker for highly suppressive antigen-specific T cells sharing features of T(h)17/T(h)1 and regulatory T cells. J Allergy Clin Immunol. 2010; 126(2):280-289.
38. Martin-Orozco N, et al. Melanoma cells express ICOS ligand to promote the activation and expansion of T-regulatory cells. Cancer Res. 2010;70(23): 9581-9590.
39. Wang J, et al. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol. 2007;37(1):129-138.
40. Ziegler SF. FOXP3: not just for regulatory T cells anymore. Eur J Immunol. 2007;37(1):21-23.
41. Miyara M, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30(6):899-911.
42. Sakaguchi S, Setoguchi R, Yagi H, Nomura T. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in self-tolerance autoimmune disease. Curr Top Microbiol Immunol. 2006;305:51-66.
43. Sakaguchi S, Wing K, Miyara M. Regulatory T cells - a brief history and perspective. Eur J Immunol. 2007;37(suppl 1):S116-S123.
44. Venken K, et al. Natural naive CD4+CD25+ CD127low regulatory T cell (Treg) development function are disturbed in multiple sclerosis patients: recovery of memory Treg homeostasis during disease progression. J Immunol. 2008;180(9):6411-6420.
45. Liu W, et al. CD127 expression inversely correlates with FoxP3 suppressive function of human CD4+ T reg cells. J Exp Med. 2006;203(7):1701- 1711.
46. Franceschini D, et al. PD-L1 negatively regulates CD4+CD25+Foxp3+ Tregs by limiting STAT-5 phosphorylation in patients chronically infected with HCV. J Clin Invest. 2009;119(3):551-564.
47. Radziewicz H, Dunham RM, Grakoui A. PD-1 tempers Tregs in chronic HCV infection. J Clin Invest. 2009; 119(3):450-453.
48. Borsellino G, et al. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP immune suppression. Blood. 2007; 110(4):1225-1232.
49. Fletcher JM, et al. CD39+Foxp3+ regulatory T Cells suppress pathogenic Th17 cells are impaired in multiple sclerosis. J Immunol. 2009;183(11):7602- 7610.
50. Mandapathil M, Lang S, Gorelik E, Whiteside TL. Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J Immunol Methods. 2009; 346(1-2):55-63.
51. Kryczek I, et al. FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res. 2009;69(9):3995-4000.
52. Sabatino M, et al. Serum vascular endothelial growth factor and fibronectin predict clinical response to high-dose interleukin-2 therapy. J Clin Oncol. 2009;27(16):2645-2652.
53. Liakou CI, et al. CTLA-4 blockade increases IFN©-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc Natl Acad Sci U S A. 2008;105(39):14987-14992.
54. Jin D, et al. CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res. 2010; 70(6):2245-2255.
55. Zhang B. CD73: a novel target for cancer immunotherapy. Cancer Res. 2010;70(16):6407-6411.
56. Dwyer KM, et al. CD39 and control of cellular immune responses. Purinergic Signal. 2007; 3(1-2):171-180.
57. Akimova T, et al. Helios expression is a marker of T cell activation and proliferation. PLoS One. 2011; 6(8):e24226.
58. Schulze Zur Wiesch J, et al. Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of Foxp3+ T regulatory cells correlates with progressive disease. J Virol. 2011;85(3):1287-1297
59. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25high regulatory cells in human peripheral blood. J Immunol. 2001;167(3):1245-1253.
60. Conrad C, et al. Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via ICOS costimulation of Foxp3(+) T-regulatory cells. Cancer Res. 2012;72(20):5240-5249.
61. Faget J, et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res. 2012; 72(23):6130-6141.
62. Eckerstorfer P, et al. Proximal human FOXP3 promoter transactivated by NF-kappaB negatively controlled by feedback loop SP3. Mol Immunol. 2010; 47(11-12):2094-2102.
63. Liao W, Lin JX, Leonard WJ. Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity. 2013;38(1):13-25.
64. Ito T, et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med. 2007;204(1):105-115.
65. Janke M, et al. Eminent role of ICOS costimulation for T cells interacting with plasmacytoid dendritic cells. Immunology. 2006;118(3):353-360.
66. Eisenhauer EA, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228-247.