IFN-γ and T-bet expression in human dendritic cells from normal donors and cancer patients is controlled through mechanisms involving ERK-1/2-dependent and IL-12-independent pathways

Journal of Immunology

Volumn 177, Issue 6, 2006, Pages 3554-3563

  Li, Huifen ^a   Wojciechowski, Wojciech ^a   Dell'Agnola, Chiara ^a   Lopez, Natalia E ^a   Espinoza Delgado, Igor ^a,b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN 1; CYCLOHEXIMIDE; DEXAMETHASONE; GAMMA INTERFERON; INTERLEUKIN 12; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR T BET;

ANTIGEN RECOGNITION; ARTICLE; CANCER PATIENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE EXPRESSION; HOST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INTERFERON PRODUCTION; LYMPHOCYTE ACTIVATION; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; TH1 CELL; TH2 CELL;

EID: 33748503611     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.6.3554     Document Type: Article

References (57)

1. Ramsdell, J. S., G. R. Pettit, and A. H. Tashjian, Jr. 1986. Three activators of protein kinase C, bryostatins, dioleins, and phorbol esters, show differing specificities of action on GH4 pituitary cells. J. Biol. Chem. 261: 17073-17080.
2. Homung, R. L., J. W. Pearson, M. Beckwith, and D. L. Longo. 1992. Preclinical evaluation of bryostatin as an anticancer agent against several murine tumor cell lines: in vitro versus in vivo activity. Cancer Res. 52: 101-107.
3. Kennedy, M. J., L. J. Prestigiacomo, G. Tyler, W. S. May, and N. E. Davidson. 1992. Differential effects of bryostatin 1 and phorbol ester on human breast cancer cell lines. Cancer Res. 52: 1278-1283.
4. Mohammad, R. M., A. al-Katib, G. R. Pettit, and L. L. Sensenbrenner. 1993. Differential effects of bryostatin 1 on human non-Hodgkin's B-lymphoma cell lines. Leuk. Res. 17: 1-8.
5. Philip, P. A., D. Rea, P. Thavasu, J. Carmichael, N. S. Stuart, H. Rockett, D. C. Talbot, T. Ganesan, G. R. Pettit, F. Balkwill, et al. 1993. Phase I study of bryostatin 1: assessment of interleukin 6 and tumor necrosis factor α induction in vivo. The Cancer Research Campaign Phase I Committee. J. Natl. Cancer Inst. 85: 1812-1818.
6. Armstrong, D. K., J. A. Blessing, J. Rader, and J. I. Sorosky. 2003. A randomized phase II evaluation of bryostatin-1 (NSC #339555) in persistent or recurrent squamous cell carcinoma of the cervix: a Gynecologic Oncology Group Study. Invest. New Drugs 21: 453-457.
7. Curiel, R. E., C. S. Garcia, L. Farooq, M. F. Aguero, and I. Espinoza-Delgado. 2001. Bryostatin-1 and IL-2 synergize to induce IFN-γ expression in human peripheral blood T cells: implications for cancer immunotherapy. J. Immunol. 167: 4828-4837.
8. Philip, P. A., and J. A. Zonder. 1999. Pharmacology and clinical experience with bryostatin 1: a novel anticancer drug. Expert Opin. Investig. Drugs 8: 2189-2199.
9. Bosco, M. C, S. Rottschafer, L. S. Taylor, J. R. Ortaldo, D. L. Longo, and I. Espinoza-Delgado. 1997. The antineoplastic agent bryostatin-1 induces proinflammatory cytokine production in human monocytes: synergy with interleukin-2 and modulation of interleukin-2Rγ chain expression. Blood 89: 3402-3411.
10. Tilden, A. B., and A. S. Kraft. 1991. The effect of bryostatin 1 on human lymphocyte-mediated cytotoxicity. J. Immunother. 10: 96-104.
11. Dunn, G. P., A. T. Bruce, H. Ikeda, L. J. Old, and R. D. Schreiber. 2002. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3: 991-998.
12. Uchijima, M., T. Nagata, T. Aoshi, and Y. Koide. 2005. IFN-γ overcomes low responsiveness of myeloid dendritic cells to CpG DNA. Immunol. Cell Biol. 83: 92-95.
13. Park, S. G., H. M. Ryu, S. O. Lim, Y. I. Kim, S. B. Hwang, and G. lung. 2005. Interferon-γ inhibits hepatitis B virus-induced NF-κB activation through nuclear localization of NF-κB-inducing kinase. Gastroenterology 128: 2042-2053.
14. Kelly, J. M., K. Takeda, P. K. Darcy, H. Yagita, and M. J. Smyth. 2002. A role for IFN-γ in primary and secondary immunity generated by NK cell-sensitive tumor-expressing CD80 in vivo. J. Immunol. 168: 4472-4479.
15. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259: 1739-1742.
16. Huang, S., W. Hendriks, A. Althage, S. Hemmi, H. Bluethmann, R. Kamijo, J. Vilcek, R. M. Zinkernagel, and M. Aguet. 1993. Immune response in mice that 'lack the interferon-γ receptor. Science 259: 1742-1745.
17. Durbin, J. E., R. Hackenmiller, M. C. Simon, and D. E. Levy. 1996. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84: 443-450.
18. + T cells through IL-12 produced by Listeria-induced macrophages. Science 260: 547-549.
19. O'Shea, J. J., and W. E. Paul. 2002. Regulation of T(H)1 differentiation-controlling the controllers. Nat. Immunol. 3: 506-508.
20. Hu, H. M., W. J. Urba, and B. A. Fox. 1998. Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J. Immunol. 161: 3033-3041.
21. Nakamori, M., M. Iwahashi, M. Nakamura, K. Ueda, X. Zhang, and H. Yamaue. 2003. Intensification of antitumor effect by T helper 1-dominant adoptive immunogene therapy for advanced orthotopic colon cancer. Clin. Cancer Res. 9: 2357-2365.
22. Tsung, K., J. B. Meko, G. R. Peplinski, Y. L. Tsung, and J. A. Norton. 1997. IL-12 induces T helper 1-directed antitumor response. J. Immunol. 158: 3359-3365.
23. Murata, Y., T. Ohteki, S. Koyasu, and J. Hamuro. 2002. IFN-γ and pro-inflammatory cytokine production by antigen-presenting cells is dictated by intracellular thiol redox status regulated by oxygen tension. Eur. J. Immunol. 32: 2866-2873.
24. Fukao, T., S. Matsuda, and S. Koyasu. 2000. Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN-γ production by dendritic cells. J. Immunol. 164: 64-71.
25. Stober, D., R. Schirmbeck, and J. Reimann. 2001. IL-12/IL-18-dependent IFN-γ release by murine dendritic cells. J. Immunol. 167: 957-965.
26. Lugo-Villarino, G., R. Maldonado-Lopez, R. Possemato, C. Penaranda, and L. H. Glimcher. 2003. T-bet is required for optimal production of IFN-γ and antigen-specific T cell activation by dendritic cells. Proc. Natl. Acad. Sci. USA 100: 7749-7754.
27. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
28. Lighvani, A. A., D. M. Frucht, D. Jankovic, H. Yamane, I. Aliberti, B. D. Hissong, B. V. Nguyen, M. Gadina, A. Sher, W. E. Paul, and J. J. O'Shea. 2001. T-bet is rapidly induced by interferon-γ in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98: 15137-15142.
29. Auphan, N., J. A. DiDonato, C. Rosette, A. Helmberg, and M. Karin. 1995. Immunosuppression by glucocorticoids: inhibition of NF-κB activity through induction of IκB synthesis. Science 270: 286-290.
30. Cippitelli, M., A. Sica, V. Viggiano, J. Ye, P. Ghosh, M. J. Birrer, and H. A. Young. 1995. Negative transcriptional regulation of the interferon-γ promoter by glucocorticoids and dominant negative mutants of c-Jun. J. Biol. Chem. 270: 12548-12556.
31. Wojciechowski, W., H. Li, S. Marshall, C. Dell'agnola, and I. Espinoza-Delgado. 2005. Enhanced expression of CD20 in human tumor B cells is controlled through ERK-dependent mechanisms. J. Immunol. 174: 7859-7868.
32. Vrana, J. A., and S. Grant. 2001. Synergistic induction of apoptosis in human leukemia cells (U937) exposed to bryostatin 1 and the proteasome inhibitor lactacystin involves dysregulation of the PKC/MAPK cascade. Blood 97: 2105-2114.
33. Tominaga, K., T. Yoshimoto, K. Torigoe, M. Kurimoto, K. Matsui, T. Hada, H. Okamura, and K. Nakanishi. 2000. IL-12 synergizes with IL-18 or IL-1β for IFN-γ production from human T cells. Int. Immunol. 12: 151-160.
34. Marcenaro, E., M. Della Chiesa, F. Bellora, S. Parolini, R. Millo, L. Moretta, and A. Moretta. 2005. IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J. Immunol. 174: 3992-3998.
35. Nefedova, Y., M. Huang, S. Kusmartsev, R. Bhattacharya, P. Cheng, R. Salup, R. Jove, and D. Gabrilovich. 2004. Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 172: 464-474.
36. Gabrilovich, D. I., J. Corak, I. F. Ciernik, D. Kavanaugh, and D. P. Carbone. 1997. Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin. Cancer Res. 3: 483-490.
37. Ghosh, P., K. L. Komschlies, M. Cippitelli, D. L. Longo, J. Subleski, J. Ye, A. Sica, H. A. Young, R. H. Wiltrout, and A. C. Ochoa. 1995. Gradual loss of T-helper 1 populations in spleen of mice during progressive tumor growth. J. Natl. Cancer Inst. 87: 1478-1483.
38. + T cells in peripheral blood of colorectal cancer patients and involvement in cancer estabv and progression. Cancer Immunol. Immunother. 42: 1-8.
39. Mohr, H., G. R. Pettit, and A. Plessing-Menze. 1987. Co-induction of lymphokine synthesis by the antineoplastic bryostatins. Immunobiology 175: 420-430.
40. Chan, S. H., B. Perussia, J. W. Gupta, M. Kobayashi, M. Pospisil, H. A. Young, S. F. Wolf, D. Young, S. C. Clark, and G. Trinchieri. 1991. Induction of interferon γ production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J. Exp. Med. 173: 869-879.
41. Berkow, R. L., L. Schlabach, R. Dodson, W. H. Benjamin, Jr., G. R. Pettit, P. Rustagi, and A. S. Kraft. 1993. In vivo administration of the anticancer agent bryostatin 1 activates platelets and neutrophils and modulates protein kinase C activity. Cancer Res. 53: 2810-2815.
42. Kraft, A. S., J. A. Reeves, and C. L. Ashendel. 1988. Differing modulation of protein kinase C by bryostatin 1 and phorbol esters in JB6 mouse epidermal cells. J. Biol. Chem. 263: 8437-8442.
43. Hennings, H., P. M. Blumberg, G. R. Pettit, C. L. Herald, R. Shores, and S. H. Yuspa. 1987. Bryostatin 1, an activator of protein kinase C, inhibits tumor promotion by phorbol esters in SENCAR mouse skin. Carcinogenesis 8: 1343-1346.
44. Szallasi, Z., L. Du, R. Levine, N. E. Lewin, P. N. Nguyen, M. D. Williams, G. R. Pettit, and P. M. Blumberg. 1996. The bryostatins inhibit growth of B16/F10 melanoma cells in vitro through a protein kinase C-independent mechanism: dissociation of activities using 26-epi-bryostatm 1. Cancer Res. 56: 2105-2111.
45. Dittmer, J. 2003. The biology of the Ets1 proto-oncogene. Mol. Cancer 2: 29.
46. Do, Y., V. L. Hegde, P. S. Nagarkatti, and M. Nagarkatti. 2004. Bryostatin-1 enhances the maturation and antigen-presenting ability of murine and human dendritic cells. Cancer Res. 64: 6756-6765.
47. Visconti, R., M. Gadina, M. Chiariello, E. H. Chen, L. F. Stancato, J. S. Gutkind, and J. J. O'Shea. 2000. Importance of the MKK6/p38 pathway for interleukin-12-induced STAT4 serine phosphorylation and transcriptional activity. Blood 96: 1844-1852.
48. Gollob, J. A., C. P. Schnipper, E. A. Murphy, J. Ritz, and D. A. Frank. 1999. The functional synergy between IL-12 and IL-2 involves p38 mitogen-activated protein kinase and is associated with the augmentation of STAT serine phosphorylation. J. Immunol. 162: 4472-4481.
49. Strengell, M., S. Matikainen, J. Siren, A. Lehtonen, D. Foster, I. Julkunen, and T. Sareneva. 2003. IL-21 in synergy with IL-15 or IL-18 enhances IFN-γ production in human NK and T cells. J. Immunol. 170: 5464-5469.
50. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
51. Yamaguchi, N., Y. Fujimori, Y. Fujibayashi, I. Kasumoto, H. Okamura, K. Nakanishi, and H. Hara. 2005. Interferon-γ production by human cord blood monocyte-derived dendritic cells. Ann. Hematol. 84: 423-428.
52. + T cells in the development of T helper type 1 responses. J. Exp. Med. 195: 473-483.
53. Schuler-Thurner, B., E. S. Schultz, T. G. Berger, G. Weinlich, S. Ebner, P. Woerl, A. Bender, B. Feuerstein, P. O. Fritsch, N. Romani, and G. Schuler. 2002. Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J. Exp. Med. 195: 1279-1288.
54. Sato, M., S. Goto, R. Kaneko, M. Ito, S. Sato, and S. Takeuchi. 1998. Impaired production of Th1 cytokines and increased frequency of Th2 subsets in PBMC from advanced cancer patients. Anticancer Res. 18: 3951-3955.
55. Elsasser-Beile, U., S. von Kleist, R. Fischer, M. Martin, U. Wetterauer, H. Gallati, and J. S. Monting. 1993. Impaired cytokine production in whole blood cell cultures of patients with urological carcinomas. J. Cancer Res. Clin. Oncol. 119: 430-433.
56. + CTL response. J. Cancer Res. Clin. Oncol. 131: 468-478.
57. Lametschwandtner, G., T. Biedermann, C. Schwarzler, C. Gunther, J. Kund, S. Fassl, S. Hinteregger, N. Carballido-Perrig, S. J. Szabo, L. H. Glimcher, and J. M. Carballido. 2004. Sustained T-bet expression confers polarized human TH2 cells with TH1-like cytokine production and migratory capacities. J. Allergy Clin. Immunol. 113: 987-994.