CD8+ T cells induce complete regression of advanced ovarian cancers by an interleukin (IL)-2/IL-15-dependent mechanism

Clinical Cancer Research

Volumn 13, Issue 23, 2007, Pages 7172-7180

  Yang, Taimei ^a   Wall, Erika M ^a   Milne, Katy ^a   Theiss, Patty ^b   Watson, Peter ^a   Nelson, Brad H ^a,c  

^a UNIVERSITY OF VICTORIA   (Canada)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASCITES; BIOACCUMULATION; BLOOD; C57BL MOUSE; CANCER CELL; CANCER REGRESSION; CANCER TISSUE; CD8+ T LYMPHOCYTE; CELL DENSITY; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; GENE DELETION; GENETIC TRANSFECTION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; OVARY ADENOCARCINOMA; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WILD TYPE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; FEMALE; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-15; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NEOPLASM STAGING; OVARIAN NEOPLASMS; RATS;

EID: 37249046879     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-1724     Document Type: Article

References (62)

1. Darai E, Detchev R, Hugol D, Quang NT. Serum and cyst fluid levels of interleukin (IL)-6, IL-8 and tumour necrosis factor-α in women with endometriomas and benign and malignant cystic ovarian tumours. Hum Reprod 2003;18:1681-5.
2. Ripley D, Shoup B, Majewski A, Chegini N. Differential expression of interleukins IL-13 and IL-15 in normal ovarian tissue and ovarian carcinomas. Gynecol Oncol 2004;92:761-8.
3. Hakkarainen T, Hemminki A, Pereboev AV, et al. CD40 is expressed on ovarian cancer cells and can be utilized for targeting adenoviruses. Clin Cancer Res 2003;9:619-24.
4. - antitumor T cells. Cancer Res 2004;64:2175-82.
5. + T-cell responses against MHC class I epitopes of the HER-2/neu oncoprotein in patients with epithelial tumors. Cancer Immunol Immunother 2003;52:771-9.
6. Mustea A, Konsgen D, Braicu EI, et al. Expression of IL-10 in patients with ovarian carcinoma. Anticancer Res 2006;26:1715-8.
7. Abrahams VM, Straszewski SL, Kamsteeg M, et al. Epithelial ovarian cancer cells secrete functional Fas ligand. Cancer Res 2003;63:5573-81.
8. Santin AD, Bellone S, Ravaggi A, et al. Increased levels of interleukin-10 and transforming growth factor-β in the plasma and ascitic fluid of patients with advanced ovarian cancer. BJOG 2001;108:804-8.
9. Curiel TJ, Wei S, Dong H, et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med 2003;9:562-7.
10. Kryczek I, Zou L, Rodriguez P, et al. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 2006;203:871-81.
11. Zou W, Machelon V, Coulomb-L'Hermin A, et al. Stromal-derived factor-1 in human tumors recruits and alters the function of plasmacytoid precursor dendritic cells. Nat Med 2001;7:1339-46.
12. Sonoda K, Miyamoto S, Yotsumoto F, et al. Clinical significance of RCAS1 as a biomarker of ovarian cancer. Oncol Rep 2007;17:623-8.
13. Maccio A, Lai P, Santona MC, Pagliara L, Melis GB, Mantovani G. High serum levels of soluble IL-2 receptor, cytokines, and C reactive protein correlate with impairment of T cell response in patients with advanced epithelial ovarian cancer. Gynecol Oncol 1998;69:248-52.
14. + T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A 2007;104:3360-5.
15. + regulatory T cells in human ovarian carcinoma. Cancer Res 2005;65:5020-6.
16. Wolf D, Wolf AM, Rumpold H, et al. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 2005;11:8326-31.
17. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9.
18. +/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005;102:18538-43.
19. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13.
20. Matsushita N, Ghazizadeh M, Konishi H, Araki T. Association of ovarian tumor epithelium coexpressing HLA-DR and CA-125 antigens with tumor infiltrating cytotoxic T lymphocytes. J Nippon Med Sch 2003;70:40-4.
21. Kusuda T, Shigemasa K, Arihiro K, Fujii T, Nagai N, Ohama K. Relative expression levels of Th1 and Th2 cytokine mRNA are independent prognostic factors in patients with ovarian cancer. Oncol Rep 2005;13:1153-8.
22. Li Y, Bleakley M, Yee C. IL-21 influences the frequency, phenotype, and affinity of the antigen-specific CD8 T cell response. J Immunol 2005;175:2261-9.
23. + T cell expansion and function. J Exp Med 2005;201:139-48.
24. 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.
25. + T cells in the absence of IL-2/15 receptor β-chain expression or STAT5 activation. J Immunol 2004;173:3131-9.
26. Yu A, Zhou J, Marten N, et al. Efficient induction of primary and secondary T cell-dependent immune responses in vivo in the absence of functional IL-2 and IL-15 receptors. J Immunol 2003;170:236-42.
27. + T regulatory cells, immunotherapy of cancer, and interleukin-2. J Immunother 2005;28:120-8.
28. Antony PA, Paulos CM, Ahmadzadeh M, et al. Interleukin-2-dependent mechanisms of tolerance and immunity in vivo. J Immunol 2006;176:5255-66.
29. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostaticm aintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005;201:723-35.
30. Laurence A, Tato CM, Davidson TS, et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007;26:371-81.
31. D'Souza WN, Lefrancois L. IL-2 is not required for the initiation of CD8 Tcell cycling but sustains expansion. J Immunol 2003;171:5727-35.
32. D'Souza WN, Schluns KS, Masopust D, Lefrancois L. Essential role for IL-2 in the regulation of antiviral extralymphoid CD8 T cell responses. J Immunol 2002;168:5566-72.
33. + memory T cells. Nature 2006;441:890-3.
34. Schluns KS, Williams K, Ma A, Zheng XX, Lefrancois L. Cutting edge: requirement for IL-15 in thegeneration of primary and memory antigen-specific CD8 T cells. J Immunol 2002;168:4827-31.
35. Judge AD, Zhang X, Fujii H, Surh CD, Sprent J. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J Exp Med 2002;196:935-46.
36. Wall EM, Milne K, Martin ML, Watson PH, Theiss P, Nelson BH. Spontaneous mammary tumors differ widely in their inherent sensitivity to adoptively transferred T cells. Cancer Res 2007;67:6442-50.
37. Roby KF, Taylor CC, Sweetwood JP, et al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis 2000;21:585-91.
38. Suzuki H, Kundig TM, Furlonger C, et al. Deregulated T cell activation and autoimmunity inmice lacking interleukin-2 receptor β. Science 1995;268:1472-6.
39. Suzuki H, Duncan GS, Takimoto H, Mak TW. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor β chain. J Exp Med 1997;185:499-505.
40. Malek TR, Porter BO, Codias EK, Scibelli P, Yu A. Normal lymphoid homeostasis and lack of lethal autoimmunity in mice containing mature T cells with severely impaired IL-2 receptors. J Immunol 2000;164:2905-14.
41. Leung DT, Morefield S, Willerford DM. Regulation of lymphoid homeostasis by IL-2 receptor signals in vivo. J Immunol 2000;164:3527-34.
42. Abrahams VM, Kamsteeg M, Mor G. The Fas/Fas ligand system and cancer: immune privilege and apoptosis. Mol Biotechnol 2003;25:19-30.
43. 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.
44. Robbins PF, Dudley ME, Wunderlich J, et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 2004;173:7125-30.
45. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol 2005;175:7046-52.
46. + T cells: efficacy is limited by migration away from the site and induction of nonresponsiveness. J Immunol 1999;162:2858-66.
47. + Tcells requires g interferon and either perforin- or Fas-mediated cytolytic mechanisms. J Virol 2005;79:14546-54.
48. Yee C, Savage PA, Lee PP, Davis MM, Greenberg PD. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J Immunol 1999;162:2227-34.
49. Annenkov A, Chernajovsky Y. Engineering mouse T lymphocytes specific to type II collagen by transduction with a chimeric receptor consisting of a single chain Fv and TCRζ. Gene Ther 2000;7:714-22.
50. Strong RK, Penny DM, Feldman RM, et al. Engineering and expression of a secreted murine TCR with reduced N-linked glycosylation. J Immunol 1994;153:4111-21.
51. Prins RM, Graf MR, Merchant RE. Cytotoxic Tcells infiltrating a glioma express an aberrant phenotype that is associated with decreased function and apoptosis. Cancer Immunol Immunother 2001;50:285-92.
52. + T-cell memory in tumor immunology and immunotherapy. Immunol Rev 2006;211:214-24.
53. Roberts AD, Ely KH, Woodland DL. Differential contributions of central and effector memory T cells to recall responses. J Exp Med 2005;202:123-33.
54. Zhao Y, Parkhurst MR, Zheng Z, et al. Extrathymic generation of tumor-specific T cells from genetically engineered human hematopoietics tem cells via Notch signaling. Cancer Res 2007;67:2425-9.
55. Mercado R, Vijh S, Allen SE, Kerksiek K, Pilip IM, Pamer EG. Early programming of T cell populations responding to bacterial infection. J Immunol 2000;165:6833-9.
56. Ford ML, Koehn BH, Wagener ME, et al. Antigen-specific precursor frequency impacts T cell proliferation, differentiation, and requirement for costimulation. J Exp Med 2007;204:299-309.
57. Badovinac VP, Haring JS, Harty JT. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) Tcell response to infection. Immunity 2007;26:827-41.
58. da Silva RJ, da Silva MG, Vilela LC, Fecchio D. Cytokine profile of Ehrlich ascites tumor treated with Bothrops jararaca venom. Mediators Inflamm 2002;11:197-201.
59. Chen CK, Wu MY, Chao KH, Ho HN, Sheu BC, Huang SC. T lymphocytes and cytokine production in ascitic fluid of ovarian malignancies. J Formos Med Assoc 1999;98:24-30.
60. Radke J, Schmidt D, Bohme M, Schmidt U, Weise W, Morenz J. Cytokine level in malignant ascites and peripheral blood of patients with advanced ovarian carcinoma. Geburtshilfe Frauenheilkd 1996;56:83-7.
61. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 2005;11:335-9.
62. Butterfield LH, Ribas A, Dissette VB, et al. Determinant spreading associated with clinical response in dendritic cell-based immunotherapy for malignant melanoma. Clin Cancer Res 2003;9:998-1008.