Cell therapy using tolerogenic dendritic cells in transplantation

Transplantation Research

Volumn 1, Issue 1, 2012, Pages

  Moreau, Aurélie ^a   Varey, Emilie ^a   Bouchet Delbos, Laurence ^a   Cuturi, Maria Cristina ^a  

^a INSERM   (France)

Author keywords

Clinical trial; Human; Tolerogenic dendritic cells; Transplantation

Indexed keywords

ABATACEPT; B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; COLECALCIFEROL; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISOLONE; TACROLIMUS; TUMOR NECROSIS FACTOR ALPHA;

AUTOTRANSPLANTATION; BONE MARROW CELL; CELL PROLIFERATION; CELL TRANSPLANTATION; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; DIABETES MELLITUS; HUMAN; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TOLEROGENIC DENDRITIC CELL TRANSPLANTATION;

EID: 84879670316     PISSN: None     EISSN: 20471440     Source Type: Journal    
DOI: 10.1186/2047-1440-1-13     Document Type: Review

References (63)

1. Correale P, Campoccia G, Tsang KY, Micheli L, Cusi MG, Sabatino M, Bruni G, Sestini S, Petrioli R, Pozzessere D, Marsili S, Fanetti G, Giorgi G, Francini G. Recruitment of dendritic cells and enhanced antigen-specific immune reactivity in cancer patients treated with hr-GM-CSF (Molgramostim) and hr-IL-2. results from a phase Ib clinical trial. Eur J Cancer 2001, 37(7):892-902. 10.1016/S0959-8049(01)00063-6, 11313178.
2. Morelli AE, Thomson AW. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 2007, 7(8):610-621. 10.1038/nri2132, 17627284.
3. Canning MO, Grotenhuis K, de Wit H, Ruwhof C, Drexhage HA. 1-alpha,25-Dihydroxyvitamin D3 (1,25(OH)(2)D(3)) hampers the maturation of fully active immature dendritic cells from monocytes. Eur J Endocrinol 2001, 145(3):351-357. 10.1530/eje.0.1450351, 11517017.
4. Penna G, Adorini L. 1 Alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol 2000, 164(5):2405-2411.
5. Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Dal Cin E, Allavena P, Di Carlo V. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol 2000, 164(9):4443-4451.
6. Raïch-Regué D, Grau-Lopez L, Naranjo-Gomez M, Ramo-Tello C, Pujol-Borrell R, Martinez-Caceres E, Borras FE. Stable antigen-specific T-cell hyporesponsiveness induced by tolerogenic dendritic cells from multiple sclerosis patients. Eur J Immunol 2012, 42(3):771-782. 10.1002/eji.201141835, 22488365.
7. Pedersen AE, Gad M, Walter MR, Claesson MH. Induction of regulatory dendritic cells by dexamethasone and 1alpha,25-Dihydroxyvitamin D(3). ImmunolLett 2004, 91(1):63-69.
8. Harry RA, Anderson AE, Isaacs JD, Hilkens CM. Generation and characterisation of therapeutic tolerogenic dendritic cells for rheumatoid arthritis. Ann Rheum Dis 2010, 69(11):2042-2050. 10.1136/ard.2009.126383, 3002758, 20551157.
9. Anderson AE, Sayers BL, Haniffa MA, Swan DJ, Diboll J, Wang XN, Isaacs JD, Hilkens CM. Differential regulation of naive and memory CD4+ T cells by alternatively activated dendritic cells. J LeukocBiol 2008, 84(1):124-133.
10. Anderson AE, Swan DJ, Sayers BL, Harry RA, Patterson AM, von Delwig A, Robinson JH, Isaacs JD, Hilkens CM. LPS activation is required for migratory activity and antigen presentation by tolerogenic dendritic cells. J LeukocBiol 2009, 85(2):243-250.
11. Raïch-Regué D, Naranjo-Gomez M, Grau-Lopez L, Ramo C, Pujol-Borrell R, Martinez-Caceres E, Borras FE. Differential effects of monophosphoryl lipid A and cytokine cocktail as maturation stimuli of immunogenic and tolerogenic dendritic cells for immunotherapy. Vaccine 2012, 30(2):378-387. 10.1016/j.vaccine.2011.10.081, 22085546.
12. Turnquist HR, Cardinal J, Macedo C, Rosborough BR, Sumpter TL, Geller DA, Metes D, Thomson AW. mTOR and GSK-3 shape the CD4+ T-cell stimulatory and differentiation capacity of myeloid DCs after exposure to LPS. Blood 2010, 115(23):4758-4769. 10.1182/blood-2009-10-251488, 2890188, 20335217.
13. Naranjo-Gomez M, Raïch-Regué D, Onate C, Grau-Lopez L, Ramo-Tello C, Pujol-Borrell R, Martinez-Caceres E, Borras FE. Comparative study of clinical grade human tolerogenic dendritic cells. J Transl Med 2011, 9:89. 10.1186/1479-5876-9-89, 3141500, 21658226.
14. Turnquist HR, Raimondi G, Zahorchak AF, Fischer RT, Wang Z, Thomson AW. 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 2007, 178(11):7018-7031.
15. Buelens C, Verhasselt V, De Groote D, Thielemans K, Goldman M, Willems F. Human dendritic cell responses to lipopolysaccharide and CD40 ligation are differentially regulated by interleukin-10. Eur J Immunol 1997, 27(8):1848-1852. 10.1002/eji.1830270805, 9295017.
16. Buelens C, Willems F, Delvaux A, Pierard G, Delville JP, Velu T, Goldman M. Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur J Immunol 1995, 25(9):2668-2672. 10.1002/eji.1830250940, 7589143.
17. Steinbrink K, Jonuleit H, Muller G, Schuler G, Knop J, Enk AH. Interleukin-10-treated human dendritic cells induce a melanoma-antigen-specific anergy in CD8(+) T cells resulting in a failure to lyse tumor cells. Blood 1999, 93(5):1634-1642.
18. Steinbrink K, Graulich E, Kubsch S, Knop J, Enk AH. CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 2002, 99(7):2468-2476. 10.1182/blood.V99.7.2468, 11895781.
19. Zahorchak AF, Kean LS, Tokita D, Turnquist HR, Abe M, Finke J, Hamby K, Rigby MR, Larsen CP, Thomson AW. Infusion of stably immature monocyte-derived dendritic cells plus CTLA4Ig modulates alloimmune reactivity in rhesus macaques. Transplantation 2007, 84(2):196-206. 10.1097/01.tp.0000268582.21168.f6, 17667811.
20. Gregori S, Tomasoni D, Pacciani V, Scirpoli M, Battaglia M, Magnani CF, Hauben E, Roncarolo MG. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 2010, 116(6):935-944. 10.1182/blood-2009-07-234872, 20448110.
21. Levings MK, Gregori S, Tresoldi E, Cazzaniga S, Bonini C, Roncarolo MG. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25 + CD4+ Tr cells. Blood 2005, 105(3):1162-1169.
22. Takayama T, Morelli AE, Onai N, Hirao M, Matsushima K, Tahara H, Thomson AW. Mammalian and viral IL-10 enhance C-C chemokine receptor 5 but down-regulate C-C chemokine receptor 7 expression by myeloid dendritic cells: impact on chemotactic responses andin vivohoming ability. J Immunol 2001, 166(12):7136-7143.
23. Garrod KR, Chang CK, Liu FC, Brennan TV, Foster RD, Kang SM. Targeted lymphoid homing of dendritic cells is required for prolongation of allograft survival. J Immunol 2006, 177(2):863-868.
24. Obermajer N, Muthuswamy R, Lesnock J, Edwards RP, Kalinski P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 2011, 118(20):5498-5505. 10.1182/blood-2011-07-365825, 21972293.
25. Hoogduijn MJ, Popp FC, Grohnert A, Crop MJ, van Rhijn M, Rowshani AT, Eggenhofer E, Renner P, Reinders ME, Rabelink TJ, van der Laan LJ, Dor FJ, Ijzermans JN, Genever PG, Lange C, Durrbach A, Houtgraaf JH, Christ B, Seifert M, Shagidulin M, Donckier V, Deans R, Ringden O, Perico N, Remuzzi G, Bartholomew A, Schlitt HJ, Weimar W, Baan CC, Dahlke MH. MISOT Study Group Advancement of mesenchymal stem cell therapy in solid organ transplantation (MISOT). Transplantation 2010, 90(2):124-126. 10.1097/TP.0b013e3181ea4240, 20606604, MISOT Study Group.
26. Roemeling-van Rhijn M, Weimar W, Hoogduijn MJ. Mesenchymal stem cells: application for solid-organ transplantation. CurrOpin Organ Transplant 2012, 17(1):55-62.
27. Hutchinson JA, Riquelme P, Sawitzki B, Tomiuk S, Miqueu P, Zuhayra M, Oberg HH, Pascher A, Lutzen U, Janssen U, Broichhausen C, Renders L, Thaiss F, Scheuermann E, Henze E, Volk HD, Chatenoud L, Lechler RI, Wood KJ, Kabelitz D, Schlitt HJ, Geissler EK, Fändrich F. Cutting edge: immunological consequences and trafficking of human regulatory macrophages administered to renal transplant recipients. J Immunol 2011, 187(5):2072-2078. 10.4049/jimmunol.1100762, 21804023.
28. Segovia M, Cuturi MC, Hill M. Preparation of mouse bone marrow-derived dendritic cells with immunoregulatory properties. Methods MolBiol 2011, 677:161-168.
29. Moreau A, Hill M, Thebault P, Deschamps JY, Chiffoleau E, Chauveau C, Moullier P, Anegon I, Alliot-Licht B, Cuturi MC. Tolerogenic dendritic cells actively inhibit T cells through heme oxygenase-1 in rodents and in nonhuman primates. FASEB J 2009, 23(9):3070-3077. 10.1096/fj.08-128173, 19420134.
30. Peche H, Trinite B, Martinet B, Cuturi MC. Prolongation of heart allograft survival by immature dendritic cells generated from recipient type bone marrow progenitors. Am J Transplant 2005, 5(2):255-267. 10.1111/j.1600-6143.2004.00683.x, 15643985.
31. Beriou G, Peche H, Guillonneau C, Merieau E, Cuturi MC. Donor-specific allograft tolerance by administration of recipient-derived immature dendritic cells and suboptimal immunosuppression. Transplantation 2005, 79(8):969-972. 10.1097/01.TP.0000158277.50073.35, 15849552.
32. Lutz MB, Suri RM, Niimi M, Ogilvie AL, Kukutsch NA, Rossner S, Schuler G, Austyn JM. Immature dendritic cells generated with low doses of GM-CSF in the absence of IL-4 are maturation resistant and prolong allograft survivalin vivo. Eur J Immunol 2000, 30(7):1813-1822. 10.1002/1521-4141(200007)30:7<1813::AID-IMMU1813>3.0.CO;2-8, 10940870.
33. Chitta S, Santambrogio L, Stern LJ. GMCSF in the absence of other cytokines sustains human dendritic cell precursors with T cell regulatory activity and capacity to differentiate into functional dendritic cells. ImmunolLett 2008, 116(1):41-54.
34. Berger TG, Strasser E, Smith R, Carste C, Schuler-Thurner B, Kaempgen E, Schuler G. Efficient elutriation of monocytes within a closed system (Elutra) for clinical-scale generation of dendritic cells. J Immunol Methods 2005, 298(1-2):61-72.
35. Hill M, Thebault P, Segovia M, Louvet C, Beriou G, Tilly G, Merieau E, Anegon I, Chiffoleau E, Cuturi MC. Cell therapy with autologous tolerogenic dendritic cells induces allograft tolerance through interferon-gamma and Epstein-Barr virus-induced gene 3. Am J Transplant 2011, 11(10):2036-2045. 10.1111/j.1600-6143.2011.03651.x, 21794083.
36. Redman BG, Chang AE, Whitfield J, Esper P, Jiang G, Braun T, Roessler B, Mule JJ. Phase Ib trial assessing autologous, tumor-pulsed dendritic cells as a vaccine administered with or without IL-2 in patients with metastatic melanoma. J Immunother 2008, 31(6):591-598. 10.1097/CJI.0b013e31817fd90b, 2642589, 18528294.
37. Dhodapkar MV, Steinman RM, Krasovsky J, Munz C, Bhardwaj N. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 2001, 193(2):233-238. 10.1084/jem.193.2.233, 2193335, 11208863.
38. Dhodapkar MV, Steinman RM. Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cellsin vivoin humans. Blood 2002, 100(1):174-177. 10.1182/blood.V100.1.174, 12070024.
39. Giannoukakis N, Phillips B, Finegold D, Harnaha J, Trucco M. Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care 2011, 34(9):2026-2032. 10.2337/dc11-0472, 3161299, 21680720.
40. Imai A, Sahara H, Tamura Y, Jimbow K, Saito T, Ezoe K, Yotsuyanagi T, Sato N. Inhibition of endogenous MHC class II-restricted antigen presentation by tacrolimus (FK506) via FKBP51. Eur J Immunol 2007, 37(7):1730-1738. 10.1002/eji.200636392, 17523132.
41. Lee YR, Yang IH, Lee YH, Im SA, Song S, Li H, Han K, Kim K, Eo SK, Lee CK. Cyclosporin A and tacrolimus, but not rapamycin, inhibit MHC-restricted antigen presentation pathways in dendritic cells. Blood 2005, 105(10):3951-3955. 10.1182/blood-2004-10-3927, 15657176.
42. Azhipa O, Kimizuka K, Nakao A, Toyokawa H, Okuda T, Neto JS, Alber SM, Kaizu T, Thomson AW, Demetris AJ, Murase N. Comparative analysis of the fate of donor dendritic cells and B cells and their influence on alloreactive T cell responses under tacrolimus immunosuppression. ClinImmunol 2005, 114(2):199-209.
43. Matsue H, Yang C, Matsue K, Edelbaum D, Mummert M, Takashima A. Contrasting impacts of immunosuppressive agents (rapamycin, FK506, cyclosporin A, and dexamethasone) on bidirectional dendritic cell-T cell interaction during antigen presentation. J Immunol 2002, 169(7):3555-3564.
44. Morelli AE, Antonysamy MA, Takayama T, Hackstein H, Chen Z, Qian S, Zurowski NB, Thomson AW. Microchimerism, donor dendritic cells, and alloimmune reactivity in recipients of Flt3 ligand-mobilized hemopoietic cells: modulation by tacrolimus. J Immunol 2000, 165(1):226-237.
45. Cos J, Villalba T, Parra R, Gallardo D, Bilbao I, Margarit C, Massuet L. FK506 in the maturation of dendritic cells. Haematologica 2002, 87(7):679-687. discussion 687.
46. Duperrier K, Velten FW, Bohlender J, Demory A, Metharom P, Goerdt S. Immunosuppressive agents mediate reduced allostimulatory properties of myeloid-derived dendritic cells despite induction of divergent molecular phenotypes. MolImmunol 2005, 42(12):1531-1540.
47. Monti P, Mercalli A, Leone BE, Valerio DC, Allavena P, Piemonti L. Rapamycin impairs antigen uptake of human dendritic cells. Transplantation 2003, 75(1):137-145. 10.1097/00007890-200301150-00025, 12544886.
48. Shimizu K, Fujii S, Fujimoto K, Kawa K, Yamada A, Kawano F. Tacrolimus (FK506) treatment of CD34+ hematopoietic progenitor cells promote the development of dendritic cells that drive CD4+ T cells toward Th2 responses. J LeukocBiol 2000, 68(5):633-640.
49. Szabo G, Gavala C, Mandrekar P. Tacrolimus and cyclosporine A inhibit allostimulatory capacity and cytokine production of human myeloid dendritic cells. J Investig Med 2001, 49(5):442-449. 10.2310/6650.2001.33789, 11523700.
50. Tiefenthaler M, Hofer S, Ebner S, Ivarsson L, Neyer S, Herold M, Mayer G, Fritsch P, Heufler C. In vitrotreatment of dendritic cells with tacrolimus: impaired T-cell activation and IP-10 expression. Nephrol Dial Transplant 2004, 19(3):553-560. 10.1093/ndt/gfg594, 14767008.
51. Han CH, Li HF, Wang YX, Zhang M, Wang Y, Yin M, Min ZL, Zheng KL. The influence of mycophenolate mofetil upon the maturation and allostimulatory activity of cultured dendritic cell progenitors and the effects of tolerance induction in allograft recipients. Zhonghua Yi XueZaZhi 2005, 85(19):1327-1332.
52. Mehling A, Grabbe S, Voskort M, Schwarz T, Luger TA, Beissert S. Mycophenolatemofetil impairs the maturation and function of murine dendritic cells. J Immunol 2000, 165(5):2374-2381.
53. Colic M, Stojic-Vukanic Z, Pavlovic B, Jandric D, Stefanoska I. Mycophenolate mofetil inhibits differentiation, maturation and allostimulatory function of human monocyte-derived dendritic cells. ClinExpImmunol 2003, 134(1):63-69.
54. Li X, Dou KF, Liu HL, Zhang FQ, Cai L. Immune tolerance induced by IL-10 and methylprednisolone modified dendritic cellsin vitro. Xi Bao Yu Fen ZiMian Yi XueZaZhi 2007, 23(5):436-438.
55. Luther C, Adamopoulou E, Stoeckle C, Brucklacher-Waldert V, Rosenkranz D, Stoltze L, Lauer S, Poeschel S, Melms A, Tolosa E. Prednisolone treatment induces tolerogenic dendritic cells and a regulatory milieu in myasthenia gravis patients. J Immunol 2009, 183(2):841-848. 10.4049/jimmunol.0802046, 19542375.
56. Rozkova D, Horvath R, Bartunkova J, Spisek R. Glucocorticoids severely impair differentiation and antigen presenting function of dendritic cells despite upregulation of Toll-like receptors. ClinImmunol 2006, 120(3):260-271.
57. Vanderheyde N, Verhasselt V, Goldman M, Willems F. Inhibition of human dendritic cell functions by methylprednisolone. Transplantation 1999, 67(10):1342-1347. 10.1097/00007890-199905270-00009, 10360588.
58. Emmer PM, van der Vlag J, Adema GJ, Hilbrands LB. Dendritic cells activated by lipopolysaccharide after dexamethasone treatment induce donor-specific allograft hyporesponsiveness. Transplantation 2006, 81(10):1451-1459. 10.1097/01.tp.0000208801.51222.bd, 16732184.
59. Yu G, Xu X, Vu MD, Kilpatrick ED, Li XC. NK cells promote transplant tolerance by killing donor antigen-presenting cells. J Exp Med 2006, 203(8):1851-1858. 10.1084/jem.20060603, 2118385, 16864660.
60. Divito SJ, Wang Z, Shufesky WJ, Liu Q, Tkacheva OA, Montecalvo A, Erdos G, Larregina AT, Morelli AE. Endogenous dendritic cells mediate the effects of intravenously injected therapeutic immunosuppressive dendritic cells in transplantation. Blood 2010, 116(15):2694-2705. 10.1182/blood-2009-10-251058, 2974582, 20576812.
61. Wang Z, Divito SJ, Shufesky WJ, Sumpter T, Wang H, Tkacheva OA, Wang W, Liu C, Larregina AT, Morelli AE. Dendritic cell therapies in transplantation revisited: deletion of recipient DCs deters the effect of therapeutic DCs. Am J Transplant 2012, 12(6):1398-1408. 10.1111/j.1600-6143.2012.04060.x, 22500950.
62. Eggert AA, Schreurs MW, Boerman OC, Oyen WJ, de Boer AJ, Punt CJ, Figdor CG, Adema GJ. Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res 1999, 59(14):3340-3345.
63. Mackensen A, Krause T, Blum U, Uhrmeister P, Mertelsmann R, Lindemann A. Homing of intravenously and intralymphatically injected human dendritic cells generatedin vitrofrom CD34+ hematopoietic progenitor cells. Cancer ImmunolImmunother 1999, 48(2-3):118-122.