Interleukin 15 provides relief to CTLs from regulatory T cell-mediated inhibition: Implications for adoptive T cell-based therapies for lymphoma

Clinical Cancer Research

Volumn 19, Issue 1, 2013, Pages 106-117

  Perna, Serena K ^a   De Angelis, Biagio ^a   Pagliara, Daria ^a   Hasan, Sayyeda T ^a   Zhang, Lan ^a   Mahendravada, Aruna ^a   Heslop, Helen E ^a   Brenner, Malcolm K ^a   Rooney, Cliona M ^a   Dotti, Gianpietro ^a   Savoldo, Barbara ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 15; RECOMBINANT INTERLEUKIN 2;

ADOPTIVE TRANSFER; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL SURVIVAL; CELL THERAPY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; EPSTEIN BARR VIRUS; HODGKIN DISEASE; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; LYMPHOMA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ANTINEOPLASTIC AGENTS; CELL DEATH; CELLS, CULTURED; HERPESVIRUS 4, HUMAN; HODGKIN DISEASE; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-15; LYMPHOCYTE ACTIVATION; LYMPHOMA; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY;

EID: 84871939748     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-2143     Document Type: Article

References (54)

1. Rooney CM, Smith CA, Ng CY, Loftin SK, Sixbey JW, Gan Y, et al. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 1998;92:1549-55.
2. Savoldo B, Goss JA, Hammer MM, Zhang L, Lopez T, Gee AP, et al. Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood 2006;108:2942-9.
3. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008;8:299-308.
4. Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A, et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J Exp Med 2004;200:1623-33.
5. Roskrow MA, Suzuki N, Gan Y, Sixbey JW, Ng CY, Kimbrough S, et al. Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for the treatment of patients with EBV-positive relapsed Hodgkin's disease. Blood 1998;91:2925-34.
6. Rosenberg SA, Packard BS, Aebersold PM, Solomon D, Topalian SL, Toy ST, et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 1988;319:1676-80.
7. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003;3:666-75.
8. Waldmann TA, Dubois S, Tagaya Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity 2001;14:105-10.
9. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, et al. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 2002;99:16168-73.
10. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002;298:850-4.
11. Lotze MT, Matory YL, Ettinghausen SE, Rayner AA, Sharrow SO, Seipp CA, et al. In vivo administration of purified human interleukin 2. II. Half life, immunologic effects, and expansion of peripheral lymphoid cells in vivo with recombinant IL 2. J Immunol 1985;135:2865-75.
12. Atkins MB. Interleukin-2: clinical applications. Semin Oncol 2002;29:12-7.
13. Siegel JP, Puri RK. Interleukin-2 toxicity. J Clin Oncol 1991;9:694-704.
14. + regulatory T cells following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2009;15:382-8.
15. + regulatory T cell populations in interleukin-2-treated HIV patients. Proc Natl Acad Sci U S A 2010;107:10632-7.
16. Sereti I, Imamichi H, Natarajan V, Imamichi T, Ramchandani MS, Badralmaa Y, et al. In vivo expansion of CD4CD45RO-CD25 T cells expressing foxP3 in IL-2-treated HIV-infected patients. J Clin Invest 2005;115:1839-47.
17. Malek TR. The main function of IL-2 is to promote the development of T regulatory cells. J Leukoc Biol 2003;74:961-5.
18. Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G. Ex vivo isolation and characterization of CD4(+)CD25(+) T cells with regulatory properties from human blood. J Exp Med 2001;193:1303-10.
19. Li J, Qian CN, Zeng YX. Regulatory T cells and EBV associated malignancies. Int Immunopharmacol 2009;9:590-2.
20. CurielTJ,CoukosG,ZouL, Alvarez X,Cheng P,MottramP, et al.Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9.
21. Wolf AM, Wolf D, Steurer M, Gastl G, Gunsilius E, Grubeck-Loebenstein B. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003;9:606-12.
22. Schreck S, Friebel D, Buettner M, Distel L, Grabenbauer G, Young LS, et al. Prognostic impact of tumour-infiltrating Th2 and regulatory T cells in classical Hodgkin lymphoma. Hematol Oncol 2009;27:31-9.
23. Marshall NA, Christie LE, Munro LR, Culligan DJ, Johnston PW, Barker RN, et al. Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma. Blood 2004;103:1755-62.
24. Baumforth KR, Birgersdotter A, Reynolds GM, Wei W, Kapatai G, Flavell JR, et al. Expression of the Epstein-Barr virus-encoded Epstein -Barr virus nuclear antigen 1 in Hodgkin's lymphoma cells mediates up-regulation of CCL20 and the migration of regulatory T cells. Am J Pathol 2008;173:195-204.
25. Waldmann TA. IL-15 in the life and death of lymphocytes: immunotherapeutic implications. Trends Mol Med 2003;9:517-21.
26. Klebanoff CA, Finkelstein SE, Surman DR, Lichtman MK, Gattinoni L, Theoret MR, et al. IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci U S A 2004;101:1969-74.
27. Quintarelli C, Vera JF, Savoldo B, Giordano Attianese GM, Pule M, Foster AE, et al. Co-expression of cytokine and suicide genes to enhance the activity and safety of tumor-specific cytotoxic T lymphocytes. Blood 2007;110:2793-802.
28. Hoyos V, Savoldo B, Quintarelli C, Mahendravada A, Zhang M, Vera J, et al. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 2010;24:1160-70.
29. Berger C, Berger M, Hackman RC, Gough M, Elliott C, Jensen MC, et al. Safety and immunologic effects of IL-15 administration in nonhuman primates. Blood 2009;114:2417-26.
30. WaldmannTA, Lugli E, Roederer M, Perera LP, Smedley JV, Macallister RP, et al. Safety (toxicity), pharmacokinetics, immunogenicity, and impact on elements of the normal immune system of recombinant human IL-15 in rhesus macaques. Blood 2011;117:4787-95.
31. Soper DM, Kasprowicz DJ, Ziegler SF. IL-2Rbeta links IL-2R signaling with Foxp3 expression. Eur J Immunol 2007;37:1817-26.
32. Wuest TY, Willette-Brown J, Durum SK, Hurwitz AA. The influence of IL-2 family cytokines on activation and function of naturally occurring regulatory T cells. J Leukoc Biol 2008;84:973-80.
33. Ruprecht CR, Gattorno M, Ferlito F, Gregorio A, Martini A, Lanzavecchia A, et al. Coexpression of CD25 and CD27 identi fies FoxP3+ regulatory T cells in inflamed synovia. J Exp Med 2005;201:1793-803.
34. Zanzi D, Stefanile R, Santagata S, Iaffaldano L, Iaquinto G, Giardullo N, et al. IL-15 interferes with suppressive activity of intestinal regulatory T cells expanded in celiac disease. Am J Gastroenterol 2011;106:1308-17.
35. Benito-Miguel M, Garcia-Carmona Y, Balsa A, Perez de AC, Cobo-Ibanez T, Martin-Mola E, et al. A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+CD25+ regulatory T cells and CD4+CD25- responder T cells. J Immunol 2009;183:8268-79.
36. Imamichi H, Sereti I, Lane HC. IL-15 acts as a potent inducer of CD4(+) CD25(hi) cells expressing FOXP3. Eur J Immunol 2008;38:1621-30.
37. Xu S, Sun Z, Sun Y, Zhu J, Li X, Zhang X, et al. IL-15 and dendritic cells induce proliferation of CD4(+)CD25(+) regulatory T cells from peripheral blood. Immunol Lett 2011;140:59-67.
38. Xia J, Liu W, Hu B, Tian Z, Yang Y. IL-15 promotes regulatory T cell function and protects against diabetes development in NK-depleted NOD mice. Clin Immunol 2010;134:130-9.
39. Ben AM, Belhadj HN, Moes N, Buyse S, Abdeladhim M, Louzir H, et al. IL-15 renders conventional lymphocytes resistant to suppressive functions of regulatory T cells through activation of the phosphatidylinositol 3-kinase pathway. J Immunol 2009;182:6763-70.
40. Burchill MA, Yang J, Vogtenhuber C, Blazar BR, Farrar MA. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J Immunol 2007;178:280-90.
41. Bensinger SJ, Walsh PT, Zhang J, Carroll M, Parsons R, Rathmell JC, et al. Distinct IL-2 receptor signaling pattern in CD4+CD25+ regulatory T cells. J Immunol 2004;172:5287-96.
42. Piscitelli SC, Forrest A, Vogel S, Chaitt D, Metcalf J, Stevens R, et al. Pharmacokinetic modeling of recombinant interleukin-2 in patients with human immunodeficiency virus infection. Clin Pharmacol Ther 1998;64:492-8.
43. Godfrey WR, Ge YG, Spoden DJ, Levine BL, June CH, Blazar BR, et al. In vitro-expanded human CD4(+)CD25(+) T-regulatory cells can markedly inhibit allogeneic dendritic cell-stimulated MLR cultures. Blood 2004;104:453-61.
44. MiyaraM,YoshiokaY, KitohA,ShimaT,WingK, NiwaA, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 2009;30:899-911.
45. Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol 2003;4:815.
46. Epardaud M, Elpek KG, Rubinstein MP, Yonekura AR, Bellemare- Pelletier A, Bronson R, et al. Interleukin-15/interleukin-15R alpha complexes promote destruction of established tumors by reviving tumor-resident CD8+ T cells. Cancer Res 2008;68:2972-83.
47. Bergamaschi C, Bear J, Rosati M, Beach RK, Alicea C, Sowder R, et al. Circulating IL-15 exists as heterodimeric complex with soluble IL-15Ralpha in human and mouse serum. Blood 2012;120:e1-e8.
48. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008;14:1264-70.
49. Dotti G, Savoldo B, Pule M, Straathof KC, Biagi E, Yvon E, et al. Human cytotoxic T lymphocytes with reduced sensitivity to Fas-induced apoptosis. Blood 2005;105:4677-84.
50. Dunne PJ, Faint JM, Gudgeon NH, Fletcher JM, Plunkett FJ, Soares MV, et al. Epstein-Barr virus-specific CD8(+) T cells that re-express CD45RA are apoptosis-resistant memory cells that retain replicative potential. Blood 2002;100:933-40.
51. Burchill MA, Yang J, Vang KB, Farrar MA. Interleukin-2 receptor signaling in regulatory T cell development and homeostasis. Immunol Lett 2007;114:1-8.
52. Yates J, Rovis F, Mitchell P, Afzali B, Tsang JY, Garin M, et al. The maintenance of human CD4+ CD25+ regulatory T cell function: IL-2, IL-4, IL-7 and IL-15 preserve optimal suppressive potency in vitro. Int Immunol 2007;19:785-99.
53. Dubois S, Mariner J, Waldmann TA, Tagaya Y. IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 2002;17:537-47.
54. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006;6:595-601.