Short-term cultured, interleukin-15 differentiated dendritic cells have potent immunostimulatory properties

Journal of Translational Medicine

Volumn 7, Issue , 2009, Pages

  Anguille, Sébastien ^a,b   Smits, Evelien L J M ^a   Cools, Nathalie ^a   Goossens, Herman ^a   Berneman, Zwi N ^a,b   Van Tendeloo, Vigor F I ^a,b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ANTWERP UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD83 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12P70; INTERLEUKIN 15; INTERLEUKIN 4; MESSENGER RNA; RESIQUIMOD; EPITOPE; IMMUNOGLOBULIN RECEPTOR; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 12; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; VIRUS ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; CULTURE TECHNIQUE; CYTOKINE RELEASE; DENDRITIC CELL; ELECTROPORATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; IMMUNOSTIMULATION; INTERMETHOD COMPARISON; MONOCYTE; T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; METABOLISM; PHAGOCYTOSIS; PHENOTYPE; TIME; VIROLOGY;

ADJUVANTS, IMMUNOLOGIC; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; ELECTROPORATION; EPITOPES; HUMANS; INTERLEUKIN-12; INTERLEUKIN-15; PHAGOCYTOSIS; PHENOTYPE; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; TIME FACTORS; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8; TRANSFECTION;

EID: 74549162674     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-7-109     Document Type: Article

References (58)

1. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J Exp Med 1974, 139:380-397. 10.1084/jem.139.2.380, 2139525, 4589990.
2. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 1973, 137:1142-1162. 10.1084/jem.137.5.1142, 2139237, 4573839.
3. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007, 449:419-426. 10.1038/nature06175, 17898760.
4. Palucka AK, Ueno H, Fay JW, Banchereau J. Taming cancer by inducing immunity via dendritic cells. Immunol Rev 2007, 220:129-150. 10.1111/j.1600-065X.2007.00575.x, 17979844.
5. Tuyaerts S, Aerts JL, Corthals J, Neyns B, Heirman C, Breckpot K, Thielemans K, Bonehill A. Current approaches in dendritic cell generation and future implications for cancer immunotherapy. Cancer Immunol Immunother 2007, 56:1513-1537. 10.1007/s00262-007-0334-z, 17503040.
6. Martin-Fontecha A, Lanzavecchia A, Sallusto F. Dendritic cell migration to peripheral lymph nodes. Handb Exp Pharmacol 2009, 31-49. full_text, 19031020.
7. Hsu FJ, Benike C, Fagnoni F, Liles TM, Czerwinski D, Taidi B, Engleman EG, Levy R. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med 1996, 2:52-58. 10.1038/nm0196-52, 8564842.
8. Figdor CG, de Vries IJ, Lesterhuis WJ, Melief CJ. Dendritic cell immunotherapy: mapping the way. Nat Med 2004, 10:475-480. 10.1038/nm1039, 15122249.
9. Ponsaerts P, Bosch G, Cools N, Van Driessche A, Nijs G, Lenjou M, Lardon F, Van Broeckhoven C, Van Bockstaele DR, Berneman ZN, Van Tendeloo VF. Messenger RNA electroporation of human monocytes, followed by rapid in vitro differentiation, leads to highly stimulatory antigen-loaded mature dendritic cells. J Immunol 2002, 169:1669-1675.
10. Dauer M, Schnurr M, Eigler A. Dendritic cell-based cancer vaccination: quo vadis?. Expert Rev Vaccines 2008, 7:1041-1053. 10.1586/14760584.7.7.1041, 18767953.
11. Czerniecki BJ, Carter C, Rivoltini L, Koski GK, Kim HI, Weng DE, Roros JG, Hijazi YM, Xu S, Rosenberg SA, Cohen PA. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells. J Immunol 1997, 159:3823-3837.
12. Dauer M, Obermaier B, Herten J, Haerle C, Pohl K, Rothenfusser S, Schnurr M, Endres S, Eigler A. Mature dendritic cells derived from human monocytes within 48 hours: a novel strategy for dendritic cell differentiation from blood precursors. J Immunol 2003, 170:4069-4076.
13. Dauer M, Schad K, Herten J, Junkmann J, Bauer C, Kiefl R, Endres S, Eigler A. FastDC derived from human monocytes within 48 h effectively prime tumor antigen-specific cytotoxic T cells. J Immunol Methods 2005, 302:145-155. 10.1016/j.jim.2005.05.010, 15992809.
14. Tawab A, Fan Y, Read EJ, Kurlander RJ. Effect of ex vivo culture duration on phenotype and cytokine production by mature dendritic cells derived from peripheral blood monocytes. Transfusion 2009, 49:536-547. 10.1111/j.1537-2995.2008.02020.x, 19243546.
15. Jarnjak-Jankovic S, Hammerstad H, Saeboe-Larssen S, Kvalheim G, Gaudernack G. A full scale comparative study of methods for generation of functional Dendritic cells for use as cancer vaccines. BMC Cancer 2007, 7:119. 10.1186/1471-2407-7-119, 1931601, 17608923.
16. Tanaka F, Yamaguchi H, Haraguchi N, Mashino K, Ohta M, Inoue H, Mori M. Efficient induction of specific cytotoxic T lymphocytes to tumor rejection peptide using functional matured 2 day-cultured dendritic cells derived from human monocytes. Int J Oncol 2006, 29:1263-1268.
17. Kanai T, Thomas EK, Yasutomi Y, Letvin NL. IL-15 stimulates the expansion of AIDS virus-specific CTL. J Immunol 1996, 157:3681-3687.
18. Kuniyoshi JS, Kuniyoshi CJ, Lim AM, Wang FY, Bade ER, Lau R, Thomas EK, Weber JS. Dendritic cell secretion of IL-15 is induced by recombinant huCD40LT and augments the stimulation of antigen-specific cytolytic T cells. Cell Immunol 1999, 193:48-58. 10.1006/cimm.1999.1469, 10202112.
19. Goddard RV, Prentice AG, Copplestone JA, Kaminski ER. In vitro dendritic cell-induced T cell responses to B cell chronic lymphocytic leukaemia enhanced by IL-15 and dendritic cell-B-CLL electrofusion hybrids. Clin Exp Immunol 2003, 131:82-89. 10.1046/j.1365-2249.2003.02047.x, 1808593, 12519390.
20. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006, 6:595-601. 10.1038/nri1901, 16868550.
21. Mortier E, Woo T, Advincula R, Gozalo S, Ma A. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med 2008, 205:1213-1225. 10.1084/jem.20071913, 2373851, 18458113.
22. Mohamadzadeh M, Berard F, Essert G, Chalouni C, Pulendran B, Davoust J, Bridges G, Palucka AK, Banchereau J. Interleukin 15 skews monocyte differentiation into dendritic cells with features of Langerhans cells. J Exp Med 2001, 194:1013-1020. 10.1084/jem.194.7.1013, 2193478, 11581322.
23. Feau S, Facchinetti V, Granucci F, Citterio S, Jarrossay D, Seresini S, Protti MP, Lanzavecchia A, Ricciardi-Castagnoli P. Dendritic cell-derived IL-2 production is regulated by IL-15 in humans and in mice. Blood 2005, 105:697-702. 10.1182/blood-2004-03-1059, 15353479.
24. Dubsky P, Saito H, Leogier M, Dantin C, Connolly JE, Banchereau J, Palucka AK. IL-15-induced human DC efficiently prime melanoma-specific naive CD8+ T cells to differentiate into CTL. Eur J Immunol 2007, 37:1678-1690. 10.1002/eji.200636329, 17492620.
25. Hardy MY, Kassianos AJ, Vulink A, Wilkinson R, Jongbloed SL, Hart DN, Radford KJ. NK cells enhance the induction of CTL responses by IL-15 monocyte-derived dendritic cells. Immunol Cell Biol 2009, 87:606-614. 10.1038/icb.2009.44, 19546878.
26. Jacobs B, Wuttke M, Papewalis C, Seissler J, Schott M. Dendritic cell subtypes and in vitro generation of dendritic cells. Horm Metab Res 2008, 40:99-107. 10.1055/s-2007-1022561, 18283627.
27. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005, 6:769-776. 10.1038/ni1223, 15995707.
28. Warger T, Osterloh P, Rechtsteiner G, Fassbender M, Heib V, Schmid B, Schmitt E, Schild H, Radsak MP. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood 2006, 108:544-550. 10.1182/blood-2005-10-4015, 16537810.
29. Pulendran B. Tolls and beyond-many roads to vaccine immunity. N Engl J Med 2007, 356:1776-1778. 10.1056/NEJMcibr070454, 17460233.
30. Smits EL, Ponsaerts P, Berneman ZN, Van Tendeloo VF. The use of TLR7 and TLR8 ligands for the enhancement of cancer immunotherapy. Oncologist 2008, 13:859-875. 10.1634/theoncologist.2008-0097, 18701762.
31. Zobywalski A, Javorovic M, Frankenberger B, Pohla H, Kremmer E, Bigalke I, Schendel DJ. Generation of clinical grade dendritic cells with capacity to produce biologically active IL-12p70. J Transl Med 2007, 5:18. 10.1186/1479-5876-5-18, 1858682, 17430585.
32. Boullart AC, Aarntzen EH, Verdijk P, Jacobs JF, Schuurhuis DH, Benitez-Ribas D, Schreibelt G, Rakt MW, Scharenborg NM, de Boer A, et al. Maturation of monocyte-derived dendritic cells with Toll-like receptor 3 and 7/8 ligands combined with prostaglandin E2 results in high interleukin-12 production and cell migration. Cancer Immunol Immunother 2008, 57:1589-1597. 10.1007/s00262-008-0489-2, 2522299, 18322684.
33. Dauer M, Lam V, Arnold H, Junkmann J, Kiefl R, Bauer C, Schnurr M, Endres S, Eigler A. Combined use of toll-like receptor agonists and prostaglandin E(2) in the FastDC model: rapid generation of human monocyte-derived dendritic cells capable of migration and IL-12p70 production. J Immunol Methods 2008, 337:97-105. 10.1016/j.jim.2008.07.003, 18657542.
34. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, Schmitt E, Knop J, Enk AH. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997, 27:3135-3142. 10.1002/eji.1830271209, 9464798.
35. Scandella E, Men Y, Gillessen S, Forster R, Groettrup M. Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 2002, 100:1354-1361. 10.1182/blood-2001-11-0017, 12149218.
36. Luft T, Jefford M, Luetjens P, Toy T, Hochrein H, Masterman KA, Maliszewski C, Shortman K, Cebon J, Maraskovsky E. Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. Blood 2002, 100:1362-1372. 10.1182/blood-2001-12-0360, 12149219.
37. Kalinski P, Schuitemaker JH, Hilkens CM, Kapsenberg ML. Prostaglandin E2 induces the final maturation of IL-12-deficient CD1a+CD83+ dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J Immunol 1998, 161:2804-2809.
38. Kalinski P, Vieira PL, Schuitemaker JH, de Jong EC, Kapsenberg ML. Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001, 97:3466-3469. 10.1182/blood.V97.11.3466, 11369638.
39. Lehner M, Morhart P, Stilper A, Petermann D, Weller P, Stachel D, Holter W. Efficient chemokine-dependent migration and primary and secondary IL-12 secretion by human dendritic cells stimulated through Toll-like receptors. J Immunother 2007, 30:312-322. 10.1097/01.cji.0000211345.11707.46, 17414322.
40. Saikh KU, Khan AS, Kissner T, Ulrich RG. IL-15-induced conversion of monocytes to mature dendritic cells. Clin Exp Immunol 2001, 126:447-455. 10.1046/j.1365-2249.2001.01672.x, 1906219, 11737061.
41. Pulendran B, Dillon S, Joseph C, Curiel T, Banchereau J, Mohamadzadeh M. Dendritic cells generated in the presence of GM-CSF plus IL-15 prime potent CD8+ Tc1 responses in vivo. Eur J Immunol 2004, 34:66-73. 10.1002/eji.200324567, 14971031.
42. Santegoets SJ, Bontkes HJ, Stam AG, Bhoelan F, Ruizendaal JJ, Eertwegh AJ, Hooijberg E, Scheper RJ, de Gruijl TD. Inducing antitumor T cell immunity: comparative functional analysis of interstitial versus Langerhans dendritic cells in a human cell line model. J Immunol 2008, 180:4540-4549.
43. Papewalis C, Jacobs B, Wuttke M, Ullrich E, Baehring T, Fenk R, Willenberg HS, Schinner S, Cohnen M, Seissler J, et al. IFN-alpha skews monocytes into CD56+-expressing dendritic cells with potent functional activities in vitro and in vivo. J Immunol 2008, 180:1462-1470.
44. Korthals M, Safaian N, Kronenwett R, Maihofer D, Schott M, Papewalis C, Diaz Blanco E, Winter M, Czibere A, Haas R, et al. Monocyte derived dendritic cells generated by IFN-alpha acquire mature dendritic and natural killer cell properties as shown by gene expression analysis. J Transl Med 2007, 5:46. 10.1186/1479-5876-5-46, 2064912, 17894866.
45. Santini SM, Lapenta C, Logozzi M, Parlato S, Spada M, Di Pucchio T, Belardelli F. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J Exp Med 2000, 191:1777-1788. 10.1084/jem.191.10.1777, 2193160, 10811870.
46. Iwamoto S, Ishida M, Takahashi K, Takeda K, Miyazaki A. Lipopolysaccharide stimulation converts vigorously washed dendritic cells (DCs) to nonexhausted DCs expressing CD70 and evoking long-lasting type 1 T cell responses. J Leukoc Biol 2005, 78:383-392. 10.1189/jlb.1104654, 15857939.
47. Verdijk P, Aarntzen EH, Punt CJ, de Vries IJ, Figdor CG. Maximizing dendritic cell migration in cancer immunotherapy. Expert Opin Biol Ther 2008, 8:865-874. 10.1517/14712598.8.7.865, 18549318.
48. Dieu MC, Vanbervliet B, Vicari A, Bridon JM, Oldham E, Ait-Yahia S, Briere F, Zlotnik A, Lebecque S, Caux C. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 1998, 188:373-386. 10.1084/jem.188.2.373, 2212459, 9670049.
49. Cyster JG. Chemokines and the homing of dendritic cells to the T cell areas of lymphoid organs. J Exp Med 1999, 189:447-450. 10.1084/jem.189.3.447, 2192905, 9927506.
50. Ten Brinke A, Karsten ML, Dieker MC, Zwaginga JJ, van Ham SM. The clinical grade maturation cocktail monophosphoryl lipid A plus IFNgamma generates monocyte-derived dendritic cells with the capacity to migrate and induce Th1 polarization. Vaccine 2007, 25:7145-7152. 10.1016/j.vaccine.2007.07.031, 17719152.
51. Bontkes HJ, Kramer D, Ruizendaal JJ, Kueter EW, van Tendeloo VF, Meijer CJ, Hooijberg E. Dendritic cells transfected with interleukin-12 and tumor-associated antigen messenger RNA induce high avidity cytotoxic T cells. Gene Ther 2007, 14:366-375. 10.1038/sj.gt.3302874, 17036057.
52. Park AY, Hondowicz BD, Scott P. IL-12 is required to maintain a Th1 response during Leishmania major infection. J Immunol 2000, 165:896-902.
53. Jongmans W, Tiemessen DM, van Vlodrop IJ, Mulders PF, Oosterwijk E. Th1-polarizing capacity of clinical-grade dendritic cells is triggered by Ribomunyl but is compromised by PGE2: the importance of maturation cocktails. J Immunother 2005, 28:480-487. 10.1097/01.cji.0000171290.78495.66, 16113604.
54. Van Tendeloo VF, Ponsaerts P, Berneman ZN. mRNA-based gene transfer as a tool for gene and cell therapy. Curr Opin Mol Ther 2007, 9:423-431.
55. Smits EL, Anguille S, Cools N, Berneman ZN, Van Tendeloo VF. Dendritic cell-based cancer gene therapy. Hum Gene Ther 2009, 20:1106-1118. 10.1089/hum.2009.145, 19656053.
56. Ponsaerts P, Van Tendeloo VF, Berneman ZN. Cancer immunotherapy using RNA-loaded dendritic cells. Clin Exp Immunol 2003, 134:378-384. 10.1046/j.1365-2249.2003.02286.x, 1808892, 14632740.
57. Van Driessche A, Ponsaerts P, Van Bockstaele DR, Van Tendeloo VF, Berneman ZN. Messenger RNA electroporation: an efficient tool in immunotherapy and stem cell research. Folia Histochem Cytobiol 2005, 43:213-216.
58. Schuurhuis DH, Lesterhuis WJ, Kramer M, Looman MG, van Hout-Kuijer M, Schreibelt G, Boullart AC, Aarntzen EH, Benitez-Ribas D, Figdor CG, et al. Polyinosinic polycytidylic acid prevents efficient antigen expression after mRNA electroporation of clinical grade dendritic cells. Cancer Immunol Immunother 2009, 58:1109-1115. 10.1007/s00262-008-0626-y, 19018531.