Interleukin-15/interleukin-15Rα complexes promote destruction of established tumors by reviving tumor-resident CD8+ T cells

Cancer Research

Volumn 68, Issue 8, 2008, Pages 2972-2983

  Epardaud, Mathieu ^a,d   Elpek, Kutlu G ^a   Rubinstein, Mark P ^e   Yonekura, Ai Ris ^a,b   Bellemare Pelletier, Angelique ^a   Bronson, Roderick ^c   Hamerman, Jessica A ^f   Goldrath, Ananda W ^e   Turley, Shannon J ^a,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d INRA Institut National de la Recherche Agronomique   (France)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 15 INTERLEUKIN 15 RECEPTOR ALPHA COMPLEX; INTERLEUKIN 15 RECEPTOR ALPHA; INTERLEUKIN 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; GENE REPRESSION; HALF LIFE TIME; HISTOPATHOLOGY; LYMPHOCYTE; LYMPHOCYTIC INFILTRATION; MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SOLID TUMOR; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR CELL; TUMOR ESCAPE; TUMOR VOLUME;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; HUMANS; INSULINOMA; MELANOMA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASMS; PANCREATIC NEOPLASMS; RECEPTORS, INTERLEUKIN-15;

EID: 42349091974     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0045     Document Type: Article

References (51)

1. Zitvogel L, Tesniere A, Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol 2006;6:715-27.
2. Pardoll D. Does the immune system see tumors as foreign or self? Annu Rev Immunol 2003;21:807-39.
3. Street SE, Hayakawa Y, Zhan Y, et al. Innate immune surveillance of spontaneous B cell lymphomas by natural killer cells and gy T cells. J Exp Med 2004;199:879-84.
4. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001;413:165-71.
5. Shankaran V, Ikeda H, Bruce AT, et al. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410:1107-11.
6. Ganss R, Hanahan D. Tumor microenvironment can restrict the effectiveness of activated antitumor lymphocytes. Cancer Res 1998;58:4673-81.
7. Kusmartsev S, Gabrilovich DI. Role of immature myeloid cells in mechanisms of immune evasion in cancer. Cancer Immunol Immunother 2006;55:237-45.
8. + regulatory T cell proliferation. J Exp Med 2005;202:919-29.
9. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15.
10. Hodi FS, Dranoff G. Combinatorial cancer immunotherapy. Adv Immunol 2006;90:341-68.
11. Gilboa E. DC-based cancer vaccines. J Clin Invest 2007;117:1195-203.
12. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003;3:666-75.
13. Gattinoni L, Powell DJ, Jr., Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 2006;6:383-93.
14. Dudley ME, Wunderlich JR, Robbins PF, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002;298:850-4.
15. June CH. Principles of adoptive T cell cancer therapy. J Clin Invest 2007;117:1204-12.
16. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
17. + T cells in the circulation but not in the tumor site. J Immunol 2006;177:1670-8.
18. + T cells in patients with melanoma. J Immunol 2005;175:6169-76.
19. Offringa R. Cancer. Cancer immunotherapy is more than a numbers game. Science 2006;314:68-9.
20. Smyth MJ, Cretney E, Kershaw MH, Hayakawa Y. Cytokines in cancer immunity and immunotherapy. Immunol Rev 2004;202:275-93.
21. Schwartz RN, Stover L, Dutcher J. Managing toxicities of high-dose interleukin-2. Oncology (Huntingt) 2002;16:11-20.
22. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006;6:595-601.
23. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 2005;6:1142-51.
24. Antony PA, Paulos CM, Ahmadzadeh M, et al. Interleukin-2-dependent mechanisms of tolerance and immunity in vivo. J Immunol 2006;176:5255-66.
25. 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.
26. Oh S, Berzofsky JA, Burke DS, Waldmann TA, Perera LP. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc Natl Acad Sci U S A 2003;100:3392-7.
27. Surh CD, Boyman O, Purton JF, Sprent J. Homeostasis of memory T cells. Immunol Rev 2006;211:154-63.
28. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006;24:657-79.
29. Klebanoff CA, Finkelstein SE, Surman DR, 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.
30. + T cells for use in adoptive immunotherapy of established tumors. Nat Med 2006;12:335-41.
31. Evans R, Fuller JA, Christianson G, Krupke DM, Troutt AB. IL-15 mediates anti-tumor effects after cyclophosphamide injection of tumor-bearing mice and enhances adoptive immunotherapy: the potential role of NK cell subpopulations. Cell Immunol 1997;179:66-73.
32. Chapoval AI, Fuller JA, Kremlev SG, Kamdar SJ, Evans R. Combination chemotherapy and IL-15 administration induce permanent tumor regression in a mouse lung tumor model: NK and T cell-mediated effects antagonized by B cells. J Immunol 1998;161:6977-84.
33. Kobayashi H, Carrasquillo JA, Paik CH, Waldmann TA, Tagaya Y. Differences of biodistribution, pharmacokinetics, and tumor targeting between interleukins 2 and 15. Cancer Res 2000;60:3577-83.
34. Zamai L, Ponti C, Mirandola P, et al. NK cells and cancer. J Immunol 2007;178:4011-6.
35. Rubinstein MP, Kovar M, Purton JF, et al. Converting IL-15 to a superagonist by binding to soluble IL-15R{α}. Proc Natl Acad Sci U S A 2006;103:9166-71.
36. Stoklasek TA, Schluns KS, Lefrancois L. Combined IL-15/IL-15Rα immunotherapy maximizes IL-15 activity in vivo. J Immunol 2006;177:6072-80.
37. Hanahan D. Heritable formation of pancreatic β-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985;315:115-22.
38. Miyazaki J, Araki K, Yamato E, et al. Establishment of a pancreatic β cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 1990;127:126-32.
39. Rubinstein MP, Kadima AN, Salem ML, et al. Transfer of TCR genes into mature T cells is accompanied by the maintenance of parental T cell avidity. J Immunol 2003;170:1209-17.
40. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. T cell receptor antagonist peptides induce positive selection. Cell 1994;76:17-27.
41. Speiser DE, Miranda R, Zakarian A, et al. Self antigens expressed by solid tumors do not efficiently stimulate naive or activated T cells: implications for immunotherapy. J Exp Med 1997;186:645-53.
42. Garbi N, Arnold B, Gordon S, Hammerling GJ, Ganss R. CpG motifs as proinflammatory factors render autochthonous tumors permissive for infiltration and destruction. J Immunol 2004;172:5861-9.
43. Ryschich E, Schmidt J, Hammerling GJ, Klar E, Ganss R. Transformation of the microvascular system during multistage tumorigenesis. Int J Cancer 2002;97:719-25.
44. Onrust SV, Hartl PM, Rosen SD, Hanahan D. Modulation of L-selectin ligand expression during an immune response accompanying tumorigenesis in transgenic mice. J Clin Invest 1996;97:54-64.
45. Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363-80.
46. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 2007;204:345-56.
47. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005;8:299-309.
48. Kamimura D, Sawa Y, Sato M, Agung E, Hirano T, Murakami M. IL-2 in vivo activities and antitumor efficacy enhanced by an anti-IL-2 mAb. J Immunol 2006;177:306-14.
49. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 1999;284:808-12.
50. Chen Q, Wang WC, Evans SS. Tumor microvasculature as a barrier to antitumor immunity. Cancer Immunol Immunother 2003;52:670-9.
51. +/CD44high T cells and its antitumor action. J Immunol 2008;180:2099-106.