Low-dose IL-2 induces cytokine cascade, eosinophilia, and a transient Th2 shift in melanoma patients

Cancer Immunology, Immunotherapy

Volumn 54, Issue 11, 2005, Pages 1095-1105

  Cragun, William Chad ^a   Yamshchikov, Galina V ^a   Bissonette, Eric A ^a   Smolkin, Mark E ^a   Eastham, Shannon ^a   Petroni, Gina R ^a   Schrecengost, Randy S ^a   Woodson, Elizabeth M H ^a   Slingluff Jr , Craig L ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Cancer; IL 5; Immunotherapy

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5;

ARTICLE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EOSINOPHILIA; HUMAN; IMMUNE RESPONSE; INFORMATION PROCESSING; MELANOMA; PRIORITY JOURNAL; TH2 CELL; VACCINATION;

ADULT; AGED; AMINO ACID SEQUENCE; CYTOKINES; EOSINOPHILIA; FEMALE; HUMANS; INTERLEUKIN-2; INTERLEUKIN-5; MALE; MELANOMA; MIDDLE AGED; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS; TH2 CELLS;

EID: 25844438797     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-005-0701-6     Document Type: Article

References (41)

1. Darrow TL, Slingluff CL, Seigler HF (1988) Autologous lymph node cell-derived tumor-specific cytotoxic T-cells for use in adoptive immunotherapy of human melanoma. Cancer 62:84-91
2. Slingluff CL Jr, Darrow TL, Seigler HF (1989) Melanoma-specific cytotoxic T cells generated from peripheral blood lymphocytes. Implications of a renewable source of precursors for adoptive cellular immunotherapy. Ann Surg 210:194-202
3. Yamshchikov G, Thompson L, Ross WG, Galavotti H, Aquila W, Deacon D, Caldwell J, Patterson JW, Hunt DF, Slingluff CL Jr (2001) Analysis of a natural immune response against tumor antigens in a melanoma survivor: lessons applicable to clinical trial evaluations. Clin Cancer Res 7:909s-916s
4. Rosenberg SA, Yang JC, Schwartzentruber DJ, Hwu P, Marincola FM, Topalian SL, Restifo NP, Sznol M, Schwarz SL, Spiess PJ, Wunderlich JR, Seipp CA, Einhorn JH, Rogers-Freezer L, White DE (1999) Impact of cytokine administration on the generation of antitumor reactivity in patients with metastatic melanoma receiving a peptide vaccine. J Immunol 163:1690-1695
5. Slingluff CL Jr, Yamshchikov GY, Barnd DL, Eastham S, Galavotti H, Patterson JW, Deacon DH, Hibbitts S, Teates D, Neese PY, Grosh WW, Petroni GR, Gibson J, Czarkowski AR, Ross M, Engelhard VH, Ross WG (2003) Clinical and immunologic results of a randomized phase II trial of vaccination utilizing four melanoma peptides either administered in GMCSF-in-adjuvant or pulsed on dendritic cells. J Clin Oncol 21:4016-4026
6. Thurner B, Haendle I, Roder C, Dieckmann D, Keikavoussi P, Jonuleit H, Bender A, Maczek C, Schreiner D, von den Driesch P, Brocker EB, Steinman RM, Enk A, Kampgen E, Schuler G (1999) Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J Exp Med 190:1669-1678
7. Tatsumi T, Kierstead LS, Ranieri E, Gesualdo L, Schena FP, Finke JH, Bukowski RM, Mueller-Berghaus J, Kirkwood JM, Kwok WW, Storkus WJ (2002) Disease-associated bias in T helper type 1 (Th1)/Th2 CD4(+) T cell responses against MAGE-6 in HLA-DRB10401(+) patients with renal cell carcinoma or melanoma. J Exp Med 196:619-628
8. Lowes MA, Bishop GA, Crotty K, Barnetson RS, Halliday GMT (1997) Helper 1 cytokine mRNA is increased in spontaneously regressing primary melanomas. J Invest Dermatol 108:914-919
9. Thompson RC, Pardoll DM, Jaffee EM, Ewend MG, Thomas MC, Tyler BM, Brem H (1996) Systemic and local paracrine cytokine therapies using transduced tumor cells are synergistic in treating intracranial tumors. J Immunother Emphasis Tumor Immunol 19:405-413
10. Nigam A, Yacavone RF, Zahurak ML, Johns CM, Pardoll DM, Piantadosi S, Levitsky HI, Nelson WG (1998) Immunomodulatory properties of antineoplastic drugs administered in conjunction with GM-CSF-secreting cancer cell vaccines. Int J Oncol 12:161-170
11. Ahlers JD, Dunlop N, Alling DW, Nara PL, Berzofsky JA (1997) Cytokine-in-adjuvant steering of the immune response phenotype to HIV-1 vaccine constructs: granulocyte-macrophage colony-stimulating factor and TNF-alpha synergize with IL-12 to enhance induction of cytotoxic T lymphocytes. J Immunol 158:3947-3958
12. Atkins MB, Kunkel L, Sznol M, Rosenberg SA (2000) High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J Sci Am 6(Suppl 1):11-14
13. Guirguis LM, Yang JC, White DE, Steinberg SM, Liewehr DJ, Rosenberg SA, Schwartzentruber DJ (2002) Safety and efficacy of high-dose interleukin-2 therapy in patients with brain metastases. J Immunother 25:82-87
14. Janssen RA, Mulder NH, The TH, de Leij L (1994) The immunobiological effects of interleukin-2 in vivo. Cancer Immunol Immunother 39:207-216
15. Palmieri G, Montella L, Milo M, Fiore R, Biondi E, Bianco AR, Martignetti A (2002) Ultra-low-dose interleukin-2 in unresectable hepatocellular carcinoma. Am J Clin Oncol 25:224-226
16. Rosenberg SA, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, Parkinson DR, Seipp CA, Einhorn JH, White DE (1994) Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. JAMA 271:907-913
17. Hefeneider SH, Conlon PJ, Henney CS, Gillis S (1983) In vivo interleukin 2 administration augments the generation of alloreactive cytolytic T lymphocytes and resident natural killer cells. J Immunol 130:222-227
18. Soiffer RJ, Murray C, Cochran K, Cameron C, Wang E, Schow PW, Daley JF, Ritz J (1992) Clinical and immunologic effects of prolonged infusion of low-dose recombinant interleukin-2 after autologous and T-cell-depleted allogeneic bone marrow transplantation. Blood 79:517-526
19. Soiffer RJ, Murray C, Shapiro C, Collins H, Chartier S, Lazo S, Ritz J (1996) Expansion and manipulation of natural killer cells in patients with metastatic cancer by low-dose continuous infusion and intermittent bolus administration of interleukin 2. Clin Cancer Res 2:493-499
20. Engelhardt M, Wirth K, Mertelsmann R, Lindemann A, Brennscheidt U (1997) Clinical and immunomodulatory effects of repetitive 2-day cycles of high-dose continuous infusion IL-2. Eur J Cancer 33:1050-1054
21. Schaafsma MR, Falkenburg JH, Landegent JE, Duinkerken N, Osanto S, Ralph P, Kaushansky K, Wagemaker G, Van Damme J, Willemze R et al (1991) In vivo production of interleukin-5, granulocyte-macrophage colony-stimulating factor, macrophages colony-stimulating factor, and interleukin-6 during intravenous administration of high-dose interleukin-2 in cancer patients. Blood 78:1981-1987
22. Phan GQ, Attia P, Steinberg SM, White DE, Rosenberg SA (2001) Factors associated with response to high-dose interleukin-2 in patients with metastatic melanoma. J Clin Oncol 19:3477-3482
23. Takeuchi E, Yanagawa H, Suzuki Y, Shinkawa K, Bando H, Sone S (2001) Interleukin (IL-)15 has less activity than IL-2 to promote type 2 cytokine predominance in tumour-associated mononuclear cells from lung cancer patients. Cytokine 13:119-123
24. Slingluff CL Jr, Petroni GR, Yamshchikov GV, Hibbitts S, Grosh WW, Chianese-Bullock KA, Bissonette EA, Barnd DL, Deacon DH, Patterson JW, Parekh J, Neese PY, Woodson EM, Wiernasz CJ, Merrill P (2004) Immunologic and clinical outcomes of vaccination with a multiepitope melanoma peptide vaccine plus low-dose interleukin-2 administered either concurrently or on a delayed schedule. J Clin Oncol 22:4474-4485
25. Woodson EM, Chianese-Bullock KA, Wiernasz K, Bissonette EA, Grosh WW, Neese P, Merrill P, Barnd DL, Petroni G, Slingluff CL Jr (2004) Assessment of the toxicities of systemic low-dose IL-2 administered in conjunction with a melanoma peptide vaccine. J Immunother 27:380-388
26. Sosman JA, Bartemes K, Offord KP, Kita H, Fisher SG, Kefer C, Ellis TA, Fisher RI, Higgins TJ, Gleich GJ (1995) Evidence for eosinophil activation in cancer patients receiving recombinant interleukin-4: effects of interleukin-4 alone and following interleukin-2 administration. Clin Cancer Res 1:805-812
27. van Haelst Pisani C, Kovach JS, Kita H, Leiferman KM, Gleich GJ, Silver JE, Dennin R, Abrams JS (1991) Administration of interleukin-2 (IL-2) results in increased plasma concentrations of IL-5 and eosinophilia in patients with cancer. Blood 78:1538-1544
28. Skipper JC, Hendrickson RC, Gulden PH, Brichard V, Van Pel A, Chen Y, Shabanowitz J, Wolfel T, Slingluff CL Jr, Boon T, Hunt DF, Engelhard VH (1996) An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J Exp Med 183:527-534
29. Chen Y, Sidney J, Southwood S, Cox AL, Sakaguchi K, Henderson RA, Appella E, Hunt DF, Sette A, Engelhard VH (1994) Naturally processed peptides longer than nine amino acid residues bind to the class I MHC molecule HLA-A2.1 with high affinity and in different conformations. J Immunol 152:2874-2881
30. Kittlesen DJ, Thompson LW, Gulden PH, Skipper JC, Colella TA, Shabanowitz J, Hunt DF, Engelhard VH, Slingluff CL Jr, Shabanowitz JA (1998) Human melanoma patients recognize an HLA-A1-restricted CTL epitope from tyrosinase containing two cysteine residues: implications for tumor vaccine development. J Immunol 160:2099-2106
31. Skipper JC, Kittlesen DJ, Hendrickson RC, Deacon DD, Harthun NL, Wagner SN, Hunt DF, Engelhard VH, Slingluff CL Jr (1996) Shared epitopes for HLA-A3-restricted melanoma-reactive human CTL include a naturally processed epitope from Pmel-17/gp100. J Immunol 157:5027-5033
32. Slingluff CL Jr, Yamshchikov G, Neese P, Galavotti H, Eastham S, Engelhard VH, Kittlesen D, Deacon D, Hibbitts S, Grosh WW, Petroni G, Cohen R, Wiernasz C, Patterson JW, Conway BP, Ross WG (2001) Phase I trial of a melanoma vaccine with gp100(280-288) peptide and tetanus helper peptide in adjuvant: immunologic and clinical outcomes. Clin Cancer Res 7:3012-3024
33. Slingluff CL Jr, Cox AL, Henderson RA, Hunt DF, Engelhard VH (1993) Recognition of human melanoma cells by HLA-A2.1-restricted cytotoxic T lymphocytes is mediated by at least six shared peptide epitopes. J Immunol 150:2955-2963
34. Kenyon NJ, Kelly EA, Jarjour NN (2000) Enhanced cytokine generation by peripheral blood mononuclear cells in allergic and asthma subjects. Ann Allergy Asthma Immunol 85:115-120
35. Shrikant P, Mescher MF (2002) Opposing effects of IL-2 in tumor immunotherapy: promoting CD8 T cell growth and inducing apoptosis. J Immunol 169:1753-1759
36. Macdonald D, Gordon AA, Kajitani H, Enokihara H, Barrett AJ (1990) Interleukin-2 treatment-associated eosinophilia is mediated by interleukin-5 production. Br J Haematol 76:168-173
37. Sun Q, Jones K, McClure B, Cambareri B, Zacharakis B, Iversen PO, Stomski F, Woodcock JM, Bagley CJ, D'Andrea R, Lopez AF (1999) Simultaneous antagonism of interleukin-5, granulocyte-macrophage colony-stimulating factor, and interleukin-3 stimulation of human eosinophils by targetting the common cytokine binding site of their receptors. Blood 94:1943-1951
38. Lopez AF, Sanderson CJ, Gamble JR, Campbell HD, Young IG, Vadas MA (1988) Recombinant human interleukin 5 is a selective activator of human eosinophil function. J Exp Med 167:219-224
39. Warren HS, Kinnear BF, Phillips JH, Lanier LL (1995) Production of IL-5 by human NK cells and regulation of IL-5 secretion by IL-4, IL-10, and IL-12. J Immunol 154:5144-5152
40. Yamaguchi Y, Suda T, Shiozaki H, Miura Y, Hitoshi Y, Tominaga A, Takatsu K, Kasahara T (1990) Role of IL-5 in IL-2-induced eosinophilia. In vivo and in vitro expression of IL-5 mRNA by IL-2. J Immunol 145:873-877
41. Sasaki G, Satoh T, Yokozeki H, Katayama I, Nishioka K (2000) Regulation of cyclophosphamide-induced eosinophilia in contact sensitivity: functional roles of interleukin-5-producing CD4(+) lymphocytes. Cell Immunol 203:124-133