Skip to main content
Top
Published in: Transplantation Research 1/2012

Open Access 01-12-2012 | Review

Cell therapy using tolerogenic dendritic cells in transplantation

Authors: Aurélie Moreau, Emilie Varey, Laurence Bouchet-Delbos, Maria-Cristina Cuturi

Published in: Transplantation Research | Issue 1/2012

Login to get access

Abstract

Organ transplantation is the main alternative to the loss of vital organ function from various diseases. However, to avoid graft rejection, transplant patients are treated with immunosuppressive drugs that have adverse side effects. A new emerging approach to reduce the administration of immunosuppressive drugs is to co-treat patients with cell therapy using regulatory cells. In our laboratory, as part of a European project, we plan to test the safety of tolerogenic dendritic cell (TolDC) therapy in kidney transplant patients. In this mini-review, we provide a brief summary of the major protocols used to derive human TolDC, and then focus on the granulocyte macrophage-TolDC generated by our own team. Proof of safety of TolDC therapy in the clinic has already been demonstrated in patients with diabetes. However, in transplantation, DC therapy will be associated with the administration of immunosuppressive drugs, and interactions between drugs and DC are possible. Finally, we will discuss the issue of DC origin, as we believe that administration of autologous TolDC is more appropriate, as demonstrated by our experiments in animal models.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
2.
go back to reference Morelli AE, Thomson AW: Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol. 2007, 7 (8): 610-621. 10.1038/nri2132.CrossRefPubMed Morelli AE, Thomson AW: Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol. 2007, 7 (8): 610-621. 10.1038/nri2132.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
5.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
6.
go back to reference 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.CrossRef 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.CrossRef
7.
go back to reference 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. 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.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
9.
go back to reference 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.CrossRef 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.CrossRef
10.
go back to reference 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.CrossRef 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.CrossRef
11.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
12.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
13.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
14.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
15.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.PubMed 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.PubMed
18.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
21.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
22.
go back to reference 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 vivo homing ability. J Immunol. 2001, 166 (12): 7136-7143.CrossRefPubMed 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 vivo homing ability. J Immunol. 2001, 166 (12): 7136-7143.CrossRefPubMed
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
25.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
26.
go back to reference Roemeling-van Rhijn M, Weimar W, Hoogduijn MJ: Mesenchymal stem cells: application for solid-organ transplantation. CurrOpin Organ Transplant. 2012, 17 (1): 55-62. 10.1097/MOT.0b013e32834ee676.CrossRef Roemeling-van Rhijn M, Weimar W, Hoogduijn MJ: Mesenchymal stem cells: application for solid-organ transplantation. CurrOpin Organ Transplant. 2012, 17 (1): 55-62. 10.1097/MOT.0b013e32834ee676.CrossRef
27.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
28.
go back to reference Segovia M, Cuturi MC, Hill M: Preparation of mouse bone marrow-derived dendritic cells with immunoregulatory properties. Methods MolBiol. 2011, 677: 161-168. Segovia M, Cuturi MC, Hill M: Preparation of mouse bone marrow-derived dendritic cells with immunoregulatory properties. Methods MolBiol. 2011, 677: 161-168.
29.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
30.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
33.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
35.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
36.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
37.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
38.
go back to reference Dhodapkar MV, Steinman RM: Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cellsin vivo in humans. Blood. 2002, 100 (1): 174-177. 10.1182/blood.V100.1.174.CrossRefPubMed Dhodapkar MV, Steinman RM: Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cellsin vivo in humans. Blood. 2002, 100 (1): 174-177. 10.1182/blood.V100.1.174.CrossRefPubMed
39.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
40.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
41.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
42.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
44.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
45.
go back to reference 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 687PubMed 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 687PubMed
46.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
48.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
50.
go back to reference Tiefenthaler M, Hofer S, Ebner S, Ivarsson L, Neyer S, Herold M, Mayer G, Fritsch P, Heufler C: In vitro treatment 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.CrossRefPubMed Tiefenthaler M, Hofer S, Ebner S, Ivarsson L, Neyer S, Herold M, Mayer G, Fritsch P, Heufler C: In vitro treatment 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.CrossRefPubMed
51.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
53.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
56.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
58.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
59.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
60.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
61.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
62.
go back to reference 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.PubMed 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.PubMed
63.
go back to reference Mackensen A, Krause T, Blum U, Uhrmeister P, Mertelsmann R, Lindemann A: Homing of intravenously and intralymphatically injected human dendritic cells generatedin vitro from CD34+ hematopoietic progenitor cells. Cancer ImmunolImmunother. 1999, 48 (2–3): 118-122.CrossRef Mackensen A, Krause T, Blum U, Uhrmeister P, Mertelsmann R, Lindemann A: Homing of intravenously and intralymphatically injected human dendritic cells generatedin vitro from CD34+ hematopoietic progenitor cells. Cancer ImmunolImmunother. 1999, 48 (2–3): 118-122.CrossRef
Metadata
Title
Cell therapy using tolerogenic dendritic cells in transplantation
Authors
Aurélie Moreau
Emilie Varey
Laurence Bouchet-Delbos
Maria-Cristina Cuturi
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Transplantation Research / Issue 1/2012
Electronic ISSN: 2047-1440
DOI
https://doi.org/10.1186/2047-1440-1-13

Other articles of this Issue 1/2012

Transplantation Research 1/2012 Go to the issue