Protein kinase C inhibitor generates stable human tolerogenic dendritic cells

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2247-2257

  Matsumoto, Takuya ^a   Hasegawa, Hitoshi ^a   Onishi, Sachiko ^a   Ishizaki, Jun ^a   Suemori, Koichiro ^a   Yasukawa, Masaki ^a  

^a EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; 3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; BISINDOLYLMALEIMIDE I; CHEMOKINE RECEPTOR CCR7; CYCLIC AMP; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; LIPOPOLYSACCHARIDE; PROTEIN KINASE C INHIBITOR; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ACUTE GRAFT VERSUS HOST DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

ANIMALS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GRAFT VS HOST DISEASE; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS;

EID: 84883437581     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203053     Document Type: Article

References (72)

1. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Lutz, M. B., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23: 445-449.
3. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21: 685-711.
4. Thomson, A. W., and P. D. Robbins. 2008. Tolerogenic dendritic cells for autoimmune disease and transplantation. Ann. Rheum. Dis. 67(Suppl. 3): iii90-iii96.
5. Torres-Aguilar, H., M. Blank, L. J. Jara, and Y. Shoenfeld. 2010. Tolerogenic dendritic cells in autoimmune diseases: crucial players in induction and prevention of autoimmunity. Autoimmun. Rev. 10: 8-17.
6. Lutz, M. B. 2012. Therapeutic potential of semi-mature dendritic cells for tolerance induction. Front Immunol 3: 123.
7. Maldonado, R. A., and U. H. von Andrian. 2010. How tolerogenic dendritic cells induce regulatory T cells. Adv. Immunol. 108: 111-165.
8. Bonham, C. A., L. Peng, X. Liang, Z. Chen, L. Wang, L. Ma, H. Hackstein, P. D. Robbins, A. W. Thomson, J. J. Fung, et al. 2002. Marked prolongation of cardiac allograft survival by dendritic cells genetically engineered with NF-κB oligodeoxyribonucleotide decoys and adenoviral vectors encoding CTLA4-Ig. J. Immunol. 169: 3382-3391.
9. Horibe, E. K., J. Sacks, J. Unadkat, G. Raimondi, Z. Wang, R. Ikeguchi, D. Marsteller, L. M. Ferreira, A. W. Thomson, W. P. Lee, and M. Feili-Hariri. 2008. Rapamycin-conditioned, alloantigen-pulsed dendritic cells promote indefinite survival of vascularized skin allografts in association with T regulatory cell expansion. Transpl. Immunol. 18: 307-318.
10. Raimondi, G., T. L. Sumpter, B. M. Matta, M. Pillai, N. Corbitt, Y. Vodovotz, Z. Wang, and A. W. Thomson. 2010. Mammalian target of rapamycin inhibition and alloantigen-specific regulatory T cells synergize to promote long-term graft survival in immunocompetent recipients. J. Immunol. 184: 624-636.
11. Popov, I., M. Li, X. Zheng, H. San, X. Zhang, T. E. Ichim, M. Suzuki, B. Feng, C. Vladau, R. Zhong, et al. 2006. Preventing autoimmune arthritis using antigenspecific immature dendritic cells: a novel tolerogenic vaccine. Arthritis Res. Ther. 8: R141.
12. van Duivenvoorde, L. M., W. G. Han, A. M. Bakker, P. Louis-Plence, L. M. Charbonnier, F. Apparailly, E. I. van der Voort, C. Jorgensen, T.W. Huizinga, and R. E. Toes. 2007. Immunomodulatory dendritic cells inhibit Th1 responses and arthritis via different mechanisms. J. Immunol. 179: 1506-1515.
13. Adorini, L. 2003. Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting autoimmune diabetes. Ann. N. Y. Acad. Sci. 987: 258-261.
14. Ma, L., S. Qian, X. Liang, L. Wang, J. E. Woodward, N. Giannoukakis, P. D. Robbins, S. Bertera, M. Trucco, J. J. Fung, and L. Lu. 2003. Prevention of diabetes in NOD mice by administration of dendritic cells deficient in nuclear transcription factor-κB activity. Diabetes 52: 1976-1985.
15. Phillips, B. E., N. Giannoukakis, and M. Trucco. 2008. Dendritic cell mediated therapy for immunoregulation of type 1 diabetes mellitus. Pediatr. Endocrinol. Rev. 5: 873-879.
16. Tai, N., H. Yasuda, Y. Xiang, L. Zhang, D. Rodriguez-Pinto, K. Yokono, R. Sherwin, F. S. Wong, M. Nagata, and L. Wen. 2011. IL-10-conditioned dendritic cells prevent autoimmune diabetes in NOD and humanized HLADQ8/RIP-B7.1 mice. Clin. Immunol. 139: 336-349.
17. Chorny, A., E. Gonzalez-Rey, A. Fernandez-Martin, D. Pozo, D. Ganea, and M. Delgado. 2005. Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc. Natl. Acad. Sci. USA 102: 13562-13567.
18. Svajger, U., N. Obermajer, and M. Jeras. 2010. Novel findings in drug-induced dendritic cell tolerogenicity. Int. Rev. Immunol. 29: 574-607.
19. Steinbrink, K., M. Wölfl, H. Jonuleit, J. Knop, and A. H. Enk. 1997. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159: 4772-4780.
20. McBride, J. M., T. Jung, J. E. de Vries, and G. Aversa. 2002. IL-10 alters DC function via modulation of cell surface molecules resulting in impaired T-cell responses. Cell. Immunol. 215: 162-172.
21. Sato, K., N. Yamashita, M. Baba, and T. Matsuyama. 2003. Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells. Blood 101: 3581-3589.
22. Torres-Aguilar, H., S. R. Aguilar-Ruiz, G. González-Pérez, R. Munguía, S. Bajaña, M. A. Meraz-Ríos, and C. Sánchez-Torres. 2010. Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J. Immunol. 184: 1765-1775.
23. Li, G., S. Abediankenari, Y. J. Kim, T. B. Campbell, S. Ito, B. Graham-Evans, S. Cooper, and H. E. Broxmeyer. 2007. TGF-β combined with M-CSF and IL-4 induces generation of immune inhibitory cord blood dendritic cells capable of enhancing cytokine-induced ex vivo expansion of myeloid progenitors. Blood 110: 2872-2879.
24. Fogel-Petrovic, M., J. A. Long, N. L. Misso, P. S. Foster, K. D. Bhoola, and P. J. Thompson. 2007. Physiological concentrations of transforming growth factor b1 selectively inhibit human dendritic cell function. Int. Immunopharmacol. 7: 1924-1933.
25. Penna, G., and L. Adorini. 2000. 1a,25-Dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J. Immunol. 164: 2405-2411.
26. Piemonti, L., P. Monti, M. Sironi, P. Fraticelli, B. E. Leone, E. Dal Cin, P. Allavena, and V. Di Carlo. 2000. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J. Immunol. 164: 4443-4451.
27. Ureta, G., F. Osorio, J. Morales, M. Rosemblatt, M. R. Bono, and J. A. Fierro. 2007. Generation of dendritic cells with regulatory properties. Transplant. Proc. 39: 633-637.
28. Unger, W. W., S. Laban, F. S. Kleijwegt, A. R. van der Slik, and B. O. Roep. 2009. Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 39: 3147-3159.
29. Delgado, M., E. Gonzalez-Rey, and D. Ganea. 2005. The neuropeptide vasoactive intestinal peptide generates tolerogenic dendritic cells. J. Immunol. 175: 7311-7324.
30. Gonzalez-Rey, E., A. Chorny, A. Fernandez-Martin, D. Ganea, and M. Delgado. 2006. Vasoactive intestinal peptide generates human tolerogenic dendritic cells that induce CD4 and CD8 regulatory T cells. Blood 107: 3632-3638.
31. Auriemma, M., T. Brzoska, L. Klenner, V. Kupas, T. Goerge, M. Voskort, Z. Zhao, T. Sparwasser, T. A. Luger, and K. Loser. 2012. a-MSH-stimulated tolerogenic dendritic cells induce functional regulatory T cells and ameliorate ongoing skin inflammation. J. Invest. Dermatol. 132: 1814-1824.
32. Piemonti, L., P. Monti, P. Allavena, M. Sironi, L. Soldini, B. E. Leone, C. Socci, and V. Di Carlo. 1999. Glucocorticoids affect human dendritic cell differentiation and maturation. J. Immunol. 162: 6473-6481.
33. Xia, C. Q., R. Peng, F. Beato, and M. J. Clare-Salzler. 2005. Dexamethasone induces IL-10-producing monocyte-derived dendritic cells with durable immaturity. Scand. J. Immunol. 62: 45-54.
34. Monti, P., A. Mercalli, B. E. Leone, D. C. Valerio, P. Allavena, and L. Piemonti. 2003. Rapamycin impairs antigen uptake of human dendritic cells. Transplantation 75: 137-145.
35. Turnquist, H. R., G. Raimondi, A. F. Zahorchak, R. T. Fischer, Z. Wang, and A. W. Thomson. 2007. Rapamycin-conditioned dendritic cells are poor stimulators of allogeneic CD4+ T cells, but enrich for antigen-specific Foxp3+ T regulatory cells and promote organ transplant tolerance. J. Immunol. 178: 7018-7031.
36. Fedoric, B., and R. Krishnan. 2008. Rapamycin downregulates the inhibitory receptors ILT2, ILT3, ILT4 on human dendritic cells and yet induces T cell hyporesponsiveness independent of FoxP3 induction. Immunol. Lett. 120: 49-56.
37. Harry, R. A., A. E. Anderson, J. D. Isaacs, and C. M. U. Hilkens. 2010. Generation and characterisation of therapeutic tolerogenic dendritic cells for rheumatoid arthritis. Ann. Rheum. Dis. 69: 2042-2050.
38. Naranjo-Gómez, M., D. Raïch-Regué, C. Oñate, L. Grau-López, C. Ramo-Tello, R. Pujol-Borrell, E. Martínez- Cáceres, and F. E. Borràs. 2011. Comparative study of clinical grade human tolerogenic dendritic cells. J. Transl. Med. 9: 89.
39. Boks, M. A., J. R. Kager-Groenland, M. S. P. Haasjes, J. J. Zwaginga, S. M. van Ham, and A. ten Brinke. 2012. IL-10-generated tolerogenic dendritic cells are optimal for functional regulatory T cell induction: a comparative study of human clinical-applicable DC. Clin. Immunol. 142: 332-342.
40. Zeng, L., S. V. Webster, and P. M. Newton. 2012. The biology of protein kinase C. Adv. Exp. Med. Biol. 740: 639-661.
41. Davis, T. A., A. A. Saini, P. J. Blair, B. L. Levine, N. Craighead, D. M. Harlan, C. H. June, and K. P. Lee. 1998. Phorbol esters induce differentiation of human CD34+ hemopoietic progenitors to dendritic cells: evidence for protein kinase Cmediated signaling. J. Immunol. 160: 3689-3697.
42. Aksoy, E., Z. Amraoui, S. Goriely, M. Goldman, and F. Willems. 2002. Critical role of protein kinase C ε for lipopolysaccharide-induced IL-12 synthesis in monocyte-derived dendritic cells. Eur. J. Immunol. 32: 3040-3049.
43. Foey, A. D., and F. M. Brennan. 2004. Conventional protein kinase C and atypical protein kinase Cζ differentially regulate macrophage production of tumour necrosis factor-α and interleukin-10. Immunology 112: 44-53.
44. II plays an essential role in dendritic cell differentiation and autoregulates its own expression. J. Biol. Chem. 280: 28412-28423.
45. + monocyte differentiation towards macrophages and dendritic cells, respectively. J. Cell. Biochem. 102: 429-441.
46. Langlet, C., C. Springael, J. Johnson, S. Thomas, V. Flamand, M. Leitges, M. Goldman, E. Aksoy, and F. Willems. 2010. PKC-α controls MYD88-dependent TLR/IL-1R signaling and cytokine production in mouse and human dendritic cells. Eur. J. Immunol. 40: 505-515.
47. Hasegawa, H., T. Nomura, M. Kohno, N. Tateishi, Y. Suzuki, N. Maeda, R. Fujisawa, O. Yoshie, and S. Fujita. 2000. Increased chemokine receptor CCR7/EBI1 expression enhances the infiltration of lymphoid organs by adult Tcell leukemia cells. Blood 95: 30-38.
48. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, et al. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266: 15771-15781.
49. Gschwendt, M., S. Dieterich, J. Rennecke, W. Kittstein, H. J. Mueller, and F. J. Johannes. 1996. Inhibition of protein kinase C m by various inhibitors. Differentiation from protein kinase C isoenzymes. FEBS Lett. 392: 77-80.
50. Wilkinson, S. E., P. J. Parker, and J. S. Nixon. 1993. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem. J. 294: 335-337.
51. + regulatory T cells. J. Immunol. 185: 7186-7198.
52. Bhattacharya, N., A. Sarno, I. S. Idler, M. Führer, T. Zenz, H. Döhner, S. Stilgenbauer, and D. Mertens. 2010. High-throughput detection of nuclear factor-κB activity using a sensitive oligo-based chemiluminescent enzymelinked immunosorbent assay. Int. J. Cancer 127: 404-411.
53. Kohno, M., H. Hasegawa, A. Inoue, M. Muraoka, T. Miyazaki, K. Oka, and M. Yasukawa. 2006. Identification of N-arachidonylglycine as the endogenous ligand for orphan G-protein-coupled receptor GPR18. Biochem. Biophys. Res. Commun. 347: 827-832.
54. Hasegawa, H., A. Inoue, M. Kohno, J. Lei, T. Miyazaki, O. Yoshie, M. Nose, and M. Yasukawa. 2008. Therapeutic effect of CXCR3-expressing regulatory T cells on liver, lung and intestinal damages in a murine acute GVHD model. Gene Ther. 15: 171-182.
55. Chorny, A., E. Gonzalez-Rey, A. Fernandez-Martin, D. Ganea, and M. Delgado. 2006. Vasoactive intestinal peptide induces regulatory dendritic cells that prevent acute graft-versus-host disease while maintaining the graft-versus-tumor response. Blood 107: 3787-3794.
56. Förster, R., A. C. Davalos-Misslitz, and A. Rot. 2008. CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8: 362-371.
57. Pettit, A. R., C. Quinn, K. P. MacDonald, L. L. Cavanagh, G. Thomas, W. Townsend, M. Handel, and R. Thomas. 1997. Nuclear localization of RelB is associated with effective antigen-presenting cell function. J. Immunol. 159: 3681-3691.
58. Yoshimura, S., J. Bondeson, B. M. Foxwell, F. M. Brennan, and M. Feldmann. 2001. Effective antigen presentation by dendritic cells is NF-κB dependent: coordinate regulation of MHC, co-stimulatory molecules and cytokines. Int. Immunol. 13: 675-683.
59. Ouaaz, F., J. Arron, Y. Zheng, Y. Choi, and A. A. Beg. 2002. Dendritic cell development and survival require distinct NF-κB subunits. Immunity 16: 257-270.
60. Gerondakis, S., A. Banerjee, G. Grigoriadis, A. Vasanthakumar, R. Gugasyan, T. Sidwell, and R. J. Grumont. 2012. NF-κB subunit specificity in hemopoiesis. Immunol. Rev. 246: 272-285.
61. Platzer, C., E. Fritsch, T. Elsner, M. H. Lehmann, H. D. Volk, and S. Prösch. 1999. Cyclic adenosine monophosphate-responsive elements are involved in the transcriptional activation of the human IL-10 gene in monocytic cells. Eur. J. Immunol. 29: 3098-3104.
62. Alvarez, Y., C. Municio, S. Alonso, M. Sánchez Crespo, and N. Fernández. 2009. The induction of IL-10 by zymosan in dendritic cells depends on CREB activation by the coactivators CREB-binding protein and TORC2 and autocrine PGE2. J. Immunol. 183: 1471-1479.
63. Arruda, S., and J. L. Ho. 1992. IL-4 receptor signal transduction in human monocytes is associated with protein kinase C translocation. J. Immunol. 149: 1258-1264.
64. Schütze, S., T. Machleidt, and M. Krönke. 1994. The role of diacylglycerol and ceramide in tumor necrosis factor and interleukin-1 signal transduction. J. Leukoc. Biol. 56: 533-541.
65. Geijsen, N., M. Spaargaren, J. A. Raaijmakers, J. W. Lammers, L. Koenderman, and P. J. Coffer. 1999. Association of RACK1 and PKCb with the common b-chain of the IL-5/IL-3/GM-CSF receptor. Oncogene 18: 5126-5130.
66. Hernandez, A., M. Burger, B. B. Blomberg, W. A. Ross, J. J. Gaynor, I. Lindner, R. Cirocco, J. M. Mathew, M. Carreno, Y. Jin, et al. 2007. Inhibition of NF-κB during human dendritic cell differentiation generates anergy and regulatory Tcell activity for one but not two human leukocyte antigen DR mismatches. Hum. Immunol. 68: 715-729.
67. + dendritic cells. Immunity 9: 839-847.
68. Martin, E., B. O'Sullivan, P. Low, and R. Thomas. 2003. Antigen-specific suppression of a primed immune response by dendritic cells mediated by regulatory T cells secreting interleukin-10. Immunity 18: 155-167.
69. Vo, N., and R. H. Goodman. 2001. CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 276: 13505-13508.
70. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptormediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784.
71. Weichhart, T., G. Costantino, M. Poglitsch, M. Rosner, M. Zeyda, K. M. Stuhlmeier, T. Kolbe, T. M. Stulnig, W. H. Hörl, M. Hengstschläger, et al. 2008. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29: 565-577.
72. Sag, D., D. Carling, R. D. Stout, and J. Suttles. 2008. Adenosine 5′-monophosphateactivated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J. Immunol. 181: 8633-8641.