Prolongation of heart allograft survival by immature dendritic cells generated from recipient type bone marrow progenitors

American Journal of Transplantation

Volumn 5, Issue 2, 2005, Pages 255-267

  Pêche, Hélène ^a   Trinité, Benjamin ^a   Martinet, Bernard ^a   Cuturi, Maria Cristina ^a  

^a Inst Transplant/Rech Transplant   (France)

Author keywords

Dendritic cells; Immunosuppression; Rat; Syngeneic; Transplantation

Indexed keywords

ALLOANTIBODY; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; KEYHOLE LIMPET HEMOCYANIN; MONOCLONAL ANTIBODY; NITRIC OXIDE; POLYCLONAL ANTIBODY; RECOMBINANT INTERLEUKIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC GRAFT REJECTION; CELL ADHESION; CELL MATURATION; CELLULAR IMMUNITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; GRAFT SURVIVAL; HEART TRANSPLANTATION; HEMATOPOIETIC STEM CELL; HUMORAL IMMUNITY; IMMUNOHISTOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; MALE; MIXED LYMPHOCYTE REACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; SPLEEN CELL; T LYMPHOCYTE;

ANIMALS; BONE MARROW CELLS; CELL ADHESION; CELL MOVEMENT; DENDRITIC CELLS; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; HEMOCYANIN; MICE; RATS; SPLEEN; STEM CELLS;

EID: 13144253118     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2004.00683.x     Document Type: Article

References (58)

1. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991; 9: 271-296,
2. Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol 1997; 9: 10-16.
3. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
4. Grohmann U, Fallarino F, Bianchi R et al. IL-6 inhibits the tolerogenic function of CD8 alpha+ dendritic cells expressing indoleamine 2,3-dioxygenase. J Immunol 2001; 167: 708-714.
5. Suss G, Shortman K. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. J Exp Med 1996; 183: 1789-1796.
6. Steinman RM, Turley S, Mellman I, Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med 2000; 191: 411-416.
7. 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: 233-238.
8. Roncarolo MG, Levings MK, Traversari C. Differentiation of T regulatory cells by immature dendritic cells. J Exp Med 2001; 193: F5-F9.
9. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000; 192: 1213-1222.
10. Hawiger D, Inaba K, Dorsett Y et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 2001; 194: 769-779.
11. Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med 1982; 155: 31-41.
12. Talmage DW, Dart G, Radovich J, Lafferty KJ. Activation of transplant immunity: effect of donor leukocytes on thyroid allograft rejection, Science 1976; 191: 385-388.
13. Josien R, Heslan M, Brouard S, Soulillou JP, Cuturi MC. Critical requirement for graft passenger leukocytes in allograft tolerance induced by donor blood transfusion. Blood 1998; 92: 4539-4544.
14. Chiffoleau E, Beriou G, Dutartre P, Usal C, Soulillou JP, Cuturi MC. Role for thymic and splenic regulatory CD4+ T cells induced by donor dendritic cells in allograft tolerance by LF15-0195 treatment. J Immunol 2002; 168: 5058-5069.
15. Morelli AE, Thomson AW. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev 2003; 196: 125-146.
16. Ichim TE, Zhong R, Min WP. Prevention of allograft rejection by in vitro generated tolerogenic dendritic cells. Transpl Immunol 2003; 11: 295-306.
17. Lu L, Thomson AW. Manipulation of dendritic cells for tolerance induction in transplantation and autoimmune disease. Transplantation 2002; 73(1 Suppl): S19-S22.
18. Fu F, Li Y, Qian S et al. Costimulatory molecule-deficient dendritic cell progenitors (MHC class II+, CD80dim, CD86-) prolong cardiac allograft survival in nonimmunosuppressed recipients. Transplantation 1996; 62: 659-665.
19. Lu L, Li W, Fu F et al. Blockade of the CD40-CD40 ligand pathway potentiates the capacity of donor-derived dendritic cell progenitors to induce long-term cardiac allograft survival. Transplantation 1997; 64: 1808-1815.
20. O'Connell PJ, Li W, Wang Z, Specht SM, Logar AJ, Thomson AW. Immature and mature CD8alpha+ dendritic cells prolong the survival of vascularized heart allografts. J Immunol 2002; 168: 143-154.
21. Garrovillo M, Ali A, Oluwole SF. Indirect allorecognition in acquired thymic tolerance: Induction of donor-specific tolerance to rat cardiac allografts by allopeptide-pulsed host dendritic cells. Transplantation 1999; 68: 1827-1834.
22. Ali A, Garrovillo M, Jin MX, Hardy MA, Oluwole SF. Major histocompatibility complex class I peptide-pulsed host dendritic cells induce antigen-specific acquired thymic tolerance to islet cells. Transplantation 2000; 69: 221-226.
23. Garrovillo M, Ali A, Depaz HA et al. Induction of transplant tolerance with immunodominant allopeptide-pulsed host lymphoid and myeloid dendritic cells. Am J Transplant 2001; 1: 129-137.
24. Spriewald BM, Billing JS, Ensminger SM, Morris PJ, Wood KJ. Linked unresponsiveness: Early cytokine gene expression profiles in cardiac allografts following pretreatment of recipients with bone marrow cells expressing donor MHC alloantigen. Cytokine 2002; 19: 6-13.
25. Inaba K, Inaba M, Romani N et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992; 176: 1693-1702.
26. Hagihara M, Li C, Gansuvd B et al. Extensive and long-term ex vivo production of dendritic cells from CD34 positive umbilical cord blood or bone marrow cells by novel culture system using mouse stroma. J Immunol Methods 2001; 253: 45-55.
27. Lutz MB, Kukutsch N, Ogilvie AL et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999; 223: 77-92.
28. Bowers WE, Yu S, Khandkar S. Differentiation of dendritic cells in cultures of rat and mouse bone marrow cells. Adv Exp Med Biol 1993; 329: 251-255.
29. Chen-Woan M, Delaney CP, Fournier V et al. A new protocol for the propagation of dendritic cells from rat bone marrow using recombinant GM-CSF, and their quantification using the mAb OX-62. J Immunol Methods 1995; 178: 157-171.
30. Powell TJ, Jenkins CD, Hattori R, MacPherson GG. Rat bone marrow-derived dendritic cells, but not ex vivo dendritic cells, secrete nitric oxide and can inhibit T-cell proliferation. Immunology 2003; 109: 197-208.
31. Mehlig M, Scheicher C, Dienes HP, Reske K. Development of rat DC by in vitro culture of bone marrow cells. Adv Exp Med Biol 1995; 378: 71-73.
32. Talmor M, Mirza A, Turley S, Mellman I, Hoffman LA, Steinman RM. Generation or large numbers of immature and mature dendritic cells from rat bone marrow cultures. Eur J Immunol 1998; 28: 811-817.
33. Grauer O, Wohlleben G, Seubert S, Weishaupt A, Kampgen E, Gold R. Analysis of maturation states of rat bone marrow-derived dendritic cells using an improved culture technique. Histochem Cell Biol 2002; 117: 351-362.
34. Peche H, Heslan M, Usal C, Amigorena S, Cuturi MC. Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection. Transplantation 2003; 76: 1503-1510.
35. 2+-dependent mechanism. J Exp Med 1997; 186: 467-472.
36. Ono K, Lindsey ES. Improved technique of heart transplantation in rats. J Thorac Cardiovasc Surg 1969; 57: 225-229.
37. van Denderen B, Peche H, Gagne K, Usal C, Cuturi MC, Soulillou JP. Identification of immunodominant donor MHC peptides following rejection and donor strain transfusion-induced tolerance of heart allografts in adult rats. Eur J Immunol 2001; 31: 1333-1339.
38. Peche H, van Denderen B, Roussel JC, Trinite B, Soulillou JP, Cuturi MC. Presentation of donor major histocompatibility complex class II antigens by dna vaccination prolongs heart allograft survival. Transplantation 2004; 77: 733-740.
39. Trinite B, Voisine C, Yagita H, Josien R. A subset of cytolytic dendritic cells in rat. J Immunol 2000; 165: 4202-4208.
40. McLellan AD, Kapp M, Eggert A et al. Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression. Blood 2002; 99: 2084-2093.
41. Brenan M, Rees DJ. Sequence analysis of rat integrin alpha E1 and alpha E2 subunits: Tissue expression reveals phenotypic similarities between intraepithelial lymphocytes and dendritic cells in lymph. Eur J Immunol 1997; 27: 3070-3079.
42. Brenan M, Puklavec M. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 1992; 175: 1457-1465.
43. Larsen CP, Morris PJ, Austyn JM. Migration of dendritic leukocytes from cardiac allografts into host spleens. A novel pathway for initiation of rejection. J Exp Med 1990; 171: 307-314.
44. DePaz HA, Oluwole OO, Adeyeri AO et al. Immature rat myeloid dendritic cells generated in low-dose granulocyte macrophage-colony stimulating factor prolong donor-specific rat cardiac allograft survival. Transplantation 2003; 75: 521-528.
45. Lutz MB, Suri RM, Niimi M et al. Immature dendritic cells generated with low doses of GM-CSF in the absence of IL-4 are maturation resistant and prolong allograft survival in vivo. Eur J Immunol 2000; 30: 1813-1822.
46. Gao JX, Madrenas J, Zeng W et al. CD40-deficient dendritic cells producing interleukin-10, but not interleukin-12, induce T-cell hyporesponsiveness in vitro and prevent acute allograft rejection. Immunology 1999; 98: 159-170.
47. Rastellini C, Lu L, Ricordi C, Starzl TE, Rao AS, Thomson AW. Granulocyte/macrophage colony-stimulating factor-stimulated hepatic dendritic cell progenitors prolong pancreatic islet allograft survival. Transplantation 1995; 60: 1366-1370.
48. Tiao MM, Lu L, Tao R et al. Application of recipient-derived dendritic cells to induce donor-specific T-cell hyporesponsiveness. Transplant Proc 2004; 36: 1592-1594.
49. Verhasselt V, Vosters O, Beuneu C, Nicaise C, Stordeur P, Goldman M. Induction of FOXP3-expressing regulatory CD4pos T cells by human mature autologous dendritic cells. Eur J Immunol 2004; 34: 762-772.
50. Feili-Hariri M, Falkner DH, Gambotto A et al. Dendritic cells transduced to express interleukin-4 prevent diabetes in nonobese diabetic mice with advanced insulitis. Hum Gene Ther 2003; 14: 13-23.
51. Feili-Hariri M, Dong X, Alber SM, Watkins SC, Salter RD, Morel PA. Immunotherapy of NOD mice with bone marrow-derived dendritic cells. Diabetes 1999; 48: 2300-2308.
52. Oluwole SF, Engelstad K, De Rosa C et al. Migration patterns of dendritic cells in the rat: Comparison of the effects of gamma and UV-B irradiation on the migration of dendritic cells and Lymphocytes. Cell Immunol 1991; 133: 390-407.
53. Lappin MB, Weiss JM, Delattre V et al. Analysis of mouse dendritic cell migration in vivo upon subcutaneous and intravenous injection. Immunology 1999; 98: 181-188.
54. Bonham CA, Lu L, Li Y, Hoffman RA, Simmons RL, Thomson AW. Nitric oxide production by mouse bone marrow-derived dendritic cells: Implications for the regulation of allogeneic T cell responses. Transplantation 1996; 62: 1871-1877.
55. Aiello S, Noris M, Piccinini G et al. Thymic dendritic cells express inducible nitric oxide synthase and generate nitric oxide in response to self- and alloantigens. J Immunol 2000; 164: 4649-4658.
56. Yang JS, Xu LY, Huang YM, Van Der Meide PH, Link H, Xiao BG. Adherent dendritic cells expressing high levels of interleukin-10 and low levels of interleukin-12 induce antigen-specific tolerance to experimental autoimmune encephalomyelitis. Immunology 2000; 101: 397-403.
57. Sayegh MH, Perico N, Imberti O, Hancock WW, Carpenter CB, Remuzzi G. Thymic recognition of class II major histocompatibility complex allopeptides induces donor-specific unresponsiveness to renal allografts. Transplantation 1993; 56: 461-465.
58. Saborio DV, Chowdhury NC, Jin MX, Chandraker A, Sayegh MH, Oluwole SF. Regulatory T cells maintain peripheral tolerance to islet allografts induced by intrathymic injection of MHC class I allopeptides. Cell Transplant 1999; 8: 375-381.