Synthetic imidazoquinolines potently and broadly activate the cellular immune response of patients with cutaneous T-cell lymphoma: Synergy with interferon-γ enhances production of interleukin-12

Clinical Lymphoma and Myeloma

Volumn 7, Issue 8, 2007, Pages 524-534

  Wysocka, Maria ^a   Newton, Sarah ^a   Benoit, Bernice M ^a   Introcaso, Camille ^a   Hancock, Aidan S ^b   Chehimi, Jihed ^b   Richardson, Stephen K ^a   Gelfand, Joel M ^a   Montaner, Luis J ^b   Rook, Alain H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WISTAR INSTITUTE   (United States)

Author keywords

Dendritic cells; Natural killer cells; S zary syndrome; Toll like receptors

Indexed keywords

3M 001; 3M 002; ALPHA INTERFERON; CD123 ANTIGEN; CD16 ANTIGEN; CD4 ANTIGEN; CD56 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; IMIDAZOQUINOLINE DERIVATIVE; IMMUNOMODULATING AGENT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 2 RECEPTOR ALPHA; MESSENGER RNA; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; UNCLASSIFIED DRUG;

ARTICLE; CANCER PATIENT; CELL COUNT; CELL FUNCTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; CYTOKINE PRODUCTION; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INTERFERON PRODUCTION; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; SEZARY SYNDROME; T LYMPHOCYTE; TREATMENT RESPONSE; UPREGULATION;

EID: 35748972931     PISSN: 15579190     EISSN: None     Source Type: Journal    
DOI: 10.3816/CLM.2007.n.037     Document Type: Article

References (79)

1. Haynes BF, Bunn P, Mann D, et al. Cell surface differentiation antigens of the malignant T cell in Sezary syndrome and mycosis fungoides. J Clin Invest 1981;67:523-530.
2. Diamandidou E, Cohen PR, Kurzrock R. Mycosis fungoides and Sezary syndrome. Blood 1996;88:2385-2409.
3. Vowels BR, Cassin M, Vonderheid EC, et al. Aberrant cytokine production by Sezary syndrome patients: cytokine secretion pattern resembles murineTh2 cells. J Invest Dermatol 1992;99:90-94.
4. Rook AH, Vowels BR, Jaworsky C, et al. The immunopathogenesis of cutaneous T-cell lymphoma. Abnormal cytokine production by Sezary T cells. Arch Dermatol 1993; 29:486-489.
5. Vowels BR, Lessin SR, Cassin M, et al. Th2 cytokine mRNA expression in skin in cutaneous T-cell lymphoma. J Invest Dermatol 1994; 103:669-773.
6. Saed G, Fivenson DP, Naidu Y, et al. Mycosis fungoides exhibits a Th1-type cell-mediated cytokine profile whereas Sezary syndrome expresses a Th2-type profile .J Invest Dermatol 1994;103:29-33.
7. Lessin SR, Vowels BR, Rook AH. Th2 cytokine profile in cutaneous T-cell lymphoma. J Invest Dermatol 1995;105:855-856.
8. Dummer R, Heald PW, Nestle FO, et al. Sezary syndrome T-cell clones display T-helper 2 cytokines and express the accessory factor-1 (interferon-gamma receptor beta-chain). Blood 1996;88:1383-1389.
9. Wysocka M, Zaki MH, French LE, et al. Sezary syndrome patients demonstrate a defect in dendritic cell populations: effects of CD40 ligand and treatment with GM-CSF on dendritic cell numbers and the production of cytokines. Blood 2002; 100:3287-3294.
10. Suchin KR, Cucchiara AJ, Gottleib SL, et al. Treatment of cutaneous T-cell lymphoma with combined immunomodulatory therapy: a 14-year experience at a single institution. Arch Dermatol 2002; 138:1054-1060.
11. Rook AH, Junkins-Hopkins JM, McGinnis KS, et al. Cytokines and other biologic agents as immunotherapeutics for cutaneous T-cell lymphoma. Adv Dermatol 2002; 18:29-43.
12. Vittorio CC, Junkins-Hopkins JM, McGinnis KS, et al. New biologic agents for the treatment of cutaneous T-cell lymphoma. Recent Results Cancer Res 2002; 160:321-328.
13. Kim EJ, Hess S, Richardson SK, et al. Immunopathogenesis and therapy of cutaneous T cell lymphoma. J Clin Invest 2005; 115:798-812.
14. Hino R, Shimauchi T, Tokura Y. Treatment with IFN-gamma increases serum levels of Th1 chemokines and decreases those of Th2 chemokines in patients with mycosis fungoides. J Dermatol Sci 2005; 38:189-195.
15. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20:197-216.
16. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005; 17:1-14.
17. Reis e Sousa C. Toll-like receptors and dendritic cells: for whom the bug tolls. Semin Immunol 2004; 16:27-34.
18. Diebold SS, Kaisho T, Hemmi H, et al. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004; 303:1529-1531.
19. Lund JM, Alexopoulou L, Sato A, et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA 2004; 101:5598-5603.
20. Heil F, Hemmi H, Hochrein H, et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004; 303:1526-1529.
21. Jurk M, Heil F, Vollmer J, et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol 2002; 3:499.
22. Suchin KR, Junkins-Hopkins JM, Rook AH. Treatment of stage IA cutaneous T-cell lymphoma with topical application of the immune response modifier imiquimod. Arch Dermatol 2002; 138:1137-1139.
23. Majewski S, Marczak M, Mlynarczyk B, et al. Imiquimod is a strong inhibitor of tumor cell-induced angiogenesis. Int J Dermatol 2005; 44:14-19.
24. Marks R, Gebauer K, Shumack S, et al. Imiquimod 5% cream in the treatment of superficial basal cell carcinoma: results of a multicenter 6-week dose-response trial. J Am Acad Dermatol 2001; 44:807-813.
25. Steinmann A, Funk JO, Schuler G, et al. Topical imiquimod treatment of a cutaneous melanoma metastasis. J Am Acad Dermatol 2000; 43:555-556.
26. Bong AB, Bonnekoh B, Franke I, et al. Imiquimod, a topical immune response modifier, in the treatment of cutaneous metastases of malignant melanoma. Dermatology 2002; 205:135-138.
27. Eedy DJ. Imiquimod: a potential role in dermatology? Br J Dermatol 2002; 147:1-6.
28. Rechtsteiner G, Warger T, Osterloh P, et al. Cutting edge: priming of CTL by transcutaneous peptide immunization with imiquimod. J Immunol 2005; 174:2476-2480.
29. Wille-Reece U, Wu CY, Flynn BJ, et al. Immunization with HIV-1 gag protein conjugated to a TLR7/8 agonist results in the generation of HIV-I gag-specific Th1 and CD8+ T cell responses. J Immunol 2005; 174:7676-7683.
30. Prins RM, Craft N, Bruhn KW, et al. The TLR-7 agonist, imiquimod, enhances dendritic cell survival and promotes tumor antigen-specific T cell priming: relation to central nervous system antitumor immunity. J Immunol 2006; 176:157-163.
31. Corden KB, Gorski KS, Gibson SJ, et al. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J Immunol 2005; 174:1259-1268.
32. Rogge L, D'Ambrosio D, Biffi M, et al. The role of Stat4 in species-specific regulation of Th cell development by type I IFNs. J Immunol 1998; 161:6567-6574.
33. Trinchieri G. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv Immunol 1998; 70:83-243.
34. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000; 406:782-787.
35. Pasare C, Medzhitov R. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 2004; 21:733-741.
36. Murphy GE Cutaneous T-cell lymphoma. Adv Pathol 1988; 1:131-156.
37. Introcaso CE, Hess SD, Kamoun M, et al. Association of change in clinical status and change in the percentage of the CD4+CD26-lymphocyte population in patients with Sezary syndrome. J Am Acad Dermatol 2005; 53:428-434.
38. Rook AH, Suchin KR, Kao DM, et al. Photopheresis: clinical applications and mechanism of action. J Investig Dermatol Symp Proc 1999; 4:85-90.
39. Rook AH, Kubin M, Cassin M, et al. IL-12 reverses cytokine and immune abnormalities in Sezary syndrome. J Immunol 1995; 154:1491-1498.
40. Kobayashi M, Fitz L, Ryan M, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989; 170:827-845.
41. Oppmann B, Lesley R, Blom B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000; 13:715-725.
42. Hart OM, Athie-Morales V, O'Connor GM, et al. TLR7/8-mediated activation of human NK cells results in accessory cell-dependent IFN-gamma production. J Immunol 2005; 175:1636-1642.
43. Gorski KS, Waller EL, Bjornton-Severson J, et al. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int Immunol 2006; 18:1115-1126.
44. Wynn TA, Jankovic D, Hieny S, et al. IL-12 exacerbates rather than suppresses T helper 2-dependent pathology in the absence of endogenous IFN-gamma. J Immunol 1995; 154:3999-4009.
45. Nakamura T, Lee RK, Nam SY, et al. Roles of IL-4 and IFN-gamma in stabilizing the T helper cell type 1 and 2 phenotype. J Immunol 1997; 158:2648-2653.
46. Napolitani G, Rinaldi A, Bertoni F, et al. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005; 6:769-776.
47. Hermann P, Rubio M, Nakajima T, et al. IFN-alpha priming of human monocytes differentially regulates gram-positive and gram-negative bacteria-induced IL-10 release and selectively enhances IL-12p70, CD80, and MHC class I expression. J Immunol 1998; 161:2011-2018.
48. D'Andrea A, Aste-Amezaga M, Valiante NM, et al. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 1993; 178:1041-1048.
49. Finkelman FD, Madden KB, Cheever AW, et al. Effects of interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites. J Exp Med 1994; 179:1563-1572.
50. Gerosa F, Paganin C, Peritt D, et al. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-gamma and interleukin-10. J Exp Med 1996; 183:2559-2569.
51. Library DH, Airan LE, Uyemura K, et al. Interferon-gamma differentially regulates interleukin-12 and interleukin-10 production in leprosy. J Clin Invest 1997; 99:336-341.
52. Gautier G, Humbert M, Deauvieau F, et al. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 2005; 201:1435-1446.
53. Peleman R, Wu J, Fargeas C, et al. Recombinant interleukin 4 suppresses the production of interferon gamma by human mononuclear cells. J Exp Med 1989; 170:1751-1756.
54. Vercelli D, Jabara HH, Lauener RP, et al. IL-4 inhibits the synthesis of IFN-gamma and induces the synthesis of IgE in human mixed lymphocyte cultures. J Immunol 1990; 144:570-573.
55. Walsh PT, Benoit BM, Wysocka M, et al. A role for regulatory T cells in cutaneous T-cell lymphoma; induction of a CD4 + CD25 + Foxp3+ T-cell phenotype associated with HTLV-1 infection. J Invest Dermatol 2006; 126:690-692.
56. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev 2001; 182:207-214.
57. Ortaldo JR, Mantovani A, Hobbs D, et al. Effects of several species of human leukocyte interferon on cytotoxic activity of NK cells and monocytes. Int J Cancer 1983; 31:285-289.
58. Herberman RB, Ortaldo JR, Mantovani A, et al. Effect of human recombinant interferon on cytotoxic activity of natural killer (NK) cells and monocytes. Cell Immunol 1982; 67:160-167.
59. Zhang X, Sun S, Hwang I, et al. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 1998; 8:591-599.
60. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 1999; 189:521-530.
61. Wysocka M, Benoit BM, Newton S, et al. Enhancement of the host immune responses in cutaneous T-cell lymphoma by CpG oligodeoxy-nucleotides and IL-15. SAW 2004; 104:4142-4149.
62. Mrozek E, Anderson P, Caligiuri MA. Role of interleukin-15 in the development of human CD56+ natural killer cells from CD34+ hematopoietic progenitor cells. Blood 1996; 87:2632-2640.
63. Williams NS, Klem J, Puzanov IJ, et al. Natural killer cell differentiation: insights from knockout and transgenic mouse models and in vitro systems. Immunol Rev 1998; 165:47-61.
64. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood 2001; 97:14-32.
65. Alves NL, Hooibrink B, Arosa FA, et al. IL-15 induces antigen-independent expansion and differentiation of human naive CD8+ T cells in vitro. Blood 2003; 102:2541-2546.
66. Berard M, Brandt K, Bulfone-Paus S, et al. IL-15 promotes the survival of naive and memory phenotype CD8+ T cells. J Immunol 2003; 170:5018-5026.
67. Judge AD, Zhang X, Fujii H, et al. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J Exp Med 2002; 196:935-946.
68. Caron G, Duluc D, Fremaux I, et al. Direct stimulation of human T cells via TLR5 and TLR7/8: flagellin and R-848 up-regulate proliferation and IFN-gamma production by memory CD4+ T cells. J Immunol 2005; 175:1551-1557.
69. Peng G, Guo Z, Kiniwa Y, et al. Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science 2005; 309:1380-1384.
70. Berger CL, Tigelaar R, Cohen J, et al. Cutaneous T-cell lymphoma: malignant proliferation of T-regulatory cells. Blood 2005; 105:1640-1647.
71. Hayes MP, Wang J, Norcross MA. Regulation of imerleukin-12 expression in human monocytes: selective priming by interferon-gamma of lipopolysaccharide- inducible p35 and p40 genes. Blood 1995; 86:646-650.
72. Ma X, Chow J, Gri G, et al. The interleukin 12 p40 gene promoter is primed by interferon gamma in monocytic cells. J Exp Med 1996; 183:147-157.
73. Liu J, Cao S, Herman LM, et al. Differential regulation of interleukin (IL)-12 p35 and p40 gene expression and interferon (IFN)-gamma-primed IL-12 production by IFN regulatory factor 1. J Exp Med 2005; 198:1265-1276.
74. Heystek HC, den Drijver B, Kapsenberg ML, et al. Type I IFNs differentially modulate IL-12p70 production by human dendritic cells depending on the maturation status of the cells and counteract IFN-gamma-mediated signaling. Clin Immunol 2003; 107:170-177.
75. Chomarat P, Rissoan MC, Banchereau J, et al. Interferon gamma inhibits interleukin 10 production by monocytes. J Exp Med 1993; 177:523-527.
76. Li C, Goodrich JM, Yang X. Interferon-gamma (IFN-gamma) regulates production of IL-10 and IL-12 in human herpesvirus-6 (HHV-6)-infected monocyte/macrophage lineage. Clin Exp Immunol 1997; 109:421-425.
77. Huang LY, Reis e Sousa C, Itoh Y, et al. IL-12 induction by a TH1-inducing adjuvant in vivo: dendritic cell subsets and regulation by IL-10. J Immunol 2001; 167:1423-1430.
78. He Q, Moore TT, Eko FO, et al. Molecular basis for the potency of IL-10-defident dendritic cells as a highly efficient APC system for activating Th1 response. J Immunol 2005; 174:4860-4869.
79. Brown R, Murray A, Pope B, et al. Eithet interleukin-12 or interferon-gamma can correct the dendritic cell defect induced by transforming growth factor beta in patients with myeloma. Br J Haematol 2004; 125:743-748.