Plasmacytoid dendritic cells: No longer an enigma and now key to transplant tolerance?

American Journal of Transplantation

Volumn 13, Issue 5, 2013, Pages 1125-1133

  Rogers, N M ^a,b   Isenberg, J S ^a,b,c   Thomson, A W ^b,c  

^a Vascular Medicine Institute   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Immune regulation; plasmacytoid dendritic cells; tolerance; transplantation

Indexed keywords

CD123 ANTIGEN; CD36 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; FLT3 LIGAND; GLYCOPROTEIN P 15095; HLA DR ANTIGEN; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 7; L SELECTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; STAT5 PROTEIN; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MIGRATION; CELLULAR DISTRIBUTION; DOWN REGULATION; GRAFT SURVIVAL; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LIVER TRANSPLANTATION; LUNG TRANSPLANTATION; NONHUMAN; ORGAN TRANSPLANTATION; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SURGICAL MORTALITY; T LYMPHOCYTE ACTIVATION; TRANSPLANTATION TOLERANCE;

DENDRITIC CELLS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNE TOLERANCE; IMMUNITY, MUCOSAL; TRANSPLANTATION TOLERANCE;

EID: 84876934665     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12229     Document Type: Review

References (73)

1. Grouard G, Rissoan M, Filgueira L, Durand I, Banchereau J, Liu Y., The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185: 1101-1111.
2. Trinchieri G, Santoli D., Anti-viral activity induced by culturing lymphocytes with tumor-derived or virus-transformed cells. Enhancement of human natural killer cell activity by interferon and antagonistic inhibition of susceptibility of target cells to lysis. J Exp Med 1978; 147: 1314-1333.
3. Shortman K, Naik SH., Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007; 7: 19-30.
4. Belz GT, Nutt SL., Transcriptional programming of the dendritic cell network. Nat Rev Immunol 2007; 12: 101-113.
5. Wu L, Liu YJ., Development of dendritic-cell lineages. Immunity 2007; 26: 741-750.
6. Corcoran L, Ferrero I, Vremec D, et al. The lymphoid past of mouse plasmacytoid cells and thymic dendritic cells. J Immunol 2003; 170: 4926-4932.
7. Pelayo R, Hirose J, Huang J, et al. Derivation of 2 categories of plasmacytoid dendritic cells in murine bone marrow. Blood 2005; 105: 4407-4415.
8. Naik SH, Sathe P, Park HY, et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 2007; 8: 1217-1226.
9. Allman D, Dalod M, Asselin-Paturel C, et al. Ikaros is required for plasmacytoid dendritic cell differentiation. Blood 2006; 108: 4025-4034.
10. Rathinam C, Geffers R, Yucel R, et al. The transcriptional repressor Gfi1 controls STAT3-dependent dendritic cell development and function. Immunity 2005; 22: 717-728.
11. Cisse B, Caton ML, Lehner M, et al. Transcription factor E 2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 2008; 135: 37-48.
12. Schotte R, Nagasawa M, Weijer K, Spits H, Blom B., The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J Exp Med 2004; 200: 1503-1509.
13. Zuniga EI, McGavern DB, Pruneda-Paz JL, Teng C, Oldstone MB., Bone marrow plasmacytoid dendritic cells can differentiate into myeloid dendritic cells upon virus infection. Nat Immunol 2004; 5: 1227-1234.
14. Fancke B, Suter M, Hochrein H, O'Keeffe M, M-CSF: A novel plasmacytoid and conventional dendritic cell poietin. Blood 2008; 111: 150-159.
15. Coates PT, Barratt-Boyes SM, Zhang L, et al. Dendritic cell subsets in blood and lymphoid tissue of rhesus monkeys and their mobilization with Flt3 ligand. Blood 2003; 102: 2513-2521.
16. Rissoan MC, Duhen T, Bridon JM, et al. Subtractive hybridization reveals the expression of immunoglobulin-like transcript 7, Eph-B1, granzyme B, and 3 novel transcripts in human plasmacytoid dendritic cells. Blood 2002; 100: 3295-3303.
17. Bonaccorsi I, Cantoni C, Carrega P, et al. The immune inhibitory receptor LAIR-1 is highly expressed by plasmacytoid dendritic cells and acts complementary with NKp44 to control IFNalpha production. PLoS ONE 2010; 5: e15080.
18. Matsui T, Connolly JE, Michnevitz M, et al. CD2 distinguishes two subsets of human plasmacytoid dendritic cells with distinct phenotype and functions. J Immunol 2009; 182: 6815-6823.
19. Jesudason S, Collins MG, Rogers NM, Kireta S, Coates PT., Non-human primate dendritic cells. J Leukoc Biol 2012; 91: 217-228.
20. Evans DT, Serra-Moreno R, Singh RK, Guatelli JC., BST-2/tetherin: A new component of the innate immune response to enveloped viruses. Trends Microbiol 2010; 18: 388-396.
21. Zhang J, Raper A, Sugita N, et al. Characterization of Siglec-H as a novel endocytic receptor expressed on murine plasmacytoid dendritic cell precursors. Blood 2006; 107: 3600-3608.
22. Watarai H, Sekine E, Inoue S, Nakagawa R, Kaisho T, Taniguchi M., PDC-TREM, a plasmacytoid dendritic cell-specific receptor, is responsible for augmented production of type I interferon. Proc Natl Acad Sci USA 2008; 105: 2993-2998.
23. Castellaneta A, Sumpter TL, Chen L, Tokita D, Thomson AW., NOD2 ligation subverts IFN-alpha production by liver plasmacytoid dendritic cells and inhibits their T cell allostimulatory activity via B7-H1 up-regulation. J Immunol 2009; 183: 6922-6932.
24. Yoneyama H, Matsuno K, Zhang Y, et al. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int Immunol 2004; 16: 915-928.
25. Krug A, Uppaluri R, Facchetti F, et al. IFN-producing cells respond to CXCR3 ligands in the presence of CXCL12 and secrete inflammatory chemokines upon activation. J Immunol 2002; 169: 6079-6083.
26. Wendland M, Czeloth N, Mach N, et al. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc Natl Acad Sci USA 2007; 104: 6347-6352.
27. Siegal FP, Kadowaki N, Shodell M, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999; 284: 1835-1837.
28. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ., The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185: 1101-1111.
29. Fonteneau JF, Gilliet M, Larsson M, et al. Activation of influenza virus-specific CD4+ and CD8+ T cells: A new role for plasmacytoid dendritic cells in adaptive immunity. Blood 2003; 101: 3520-3526.
30. Bonasio R, Scimone ML, Schaerli P, Grabie N, Lichtman AH, von Andrian UH., Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat Immunol 2006; 7: 1092-1100.
31. Li J, Park J, Foss D, Goldschneider I., Thymus-homing peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. J Exp Med 2009; 206: 607-622.
32. Hadeiba H, Lahl K, Edalati A, et al. Plasmacytoid dendritic cells transport peripheral antigens to the thymus to promote central tolerance. Immunity 2012; 36: 438-450.
33. Hadeiba H, Sato T, Habtezion A, Oderup C, Pan J, Butcher EC., CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat Immunol 2008; 9: 1253-1260.
34. Martin-Gayo E, Sierra-Filardi E, Corbi AL, Toribio ML., Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood 2010; 115: 5366-5375.
35. Hanabuchi S, Ito T, Park WR, et al. Thymic stromal lymphopoietin- activated plasmacytoid dendritic cells induce the generation of FOXP3+ regulatory T cells in human thymus. J Immunol 2010; 184: 2999-3007.
36. Goubier A, Dubois B, Gheit H, et al. Plasmacytoid dendritic cells mediate oral tolerance. Immunity 2008; 29: 464-475.
37. Palomares O, Ruckert B, Jartti T, et al. Induction and maintenance of allergen-specific FOXP3+ Treg cells in human tonsils as potential first-line organs of oral tolerance. J Allergy Clin Immunol 2012; 129: 510-520 520 e 511-519.
38. de Heer HJ, Hammad H, Soullie T, et al. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 2004; 200: 89-98.
39. Contractor N, Louten J, Kim L, Biron CA, Kelsall BL., Cutting edge: Peyer's patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: Possible role for IL-10, TGFbeta, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J Immunol 2007; 179: 2690-2694.
40. Dubois B, Joubert G, Gomez de Aguero M, Gouanvic M, Goubier A, Kaiserlian D., Sequential role of plasmacytoid dendritic cells and regulatory T cells in oral tolerance. Gastroenterology 2009; 137: 1019-1028.
41. Morelli AE, Thomson AW., Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 2007; 7: 610-621.
42. Wood KJ, Bushell A, Hester J., Regulatory immune cells in transplantation. Nat Rev Immunol 2012; 12: 417-430.
43. Koyama M, Hashimoto D, Aoyama K, et al. Plasmacytoid dendritic cells prime alloreactive T cells to mediate graft-versus-host disease as antigen-presenting cells. Blood 2009; 113: 2088-2095.
44. Benson HL, Suzuki H, Lott J, et al. Donor lung derived myeloid and plasmacytoid dendritic cells differentially regulate T cell proliferation and cytokine production. Respir Res 2012; 13: 25.
45. Moseman EA, Liang X, Dawson AJ, et al. Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J Immunol 2004; 173: 4433-4442.
46. Gilliet M, Liu YJ., Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J Exp Med 2002; 195: 695-704.
47. Abe M, Wang Z, de Creus A, Thomson AW., Plasmacytoid dendritic cell precursors induce allogeneic T-cell hyporesponsiveness and prolong heart graft survival. Am J Transplant 2005; 5: 1808-1819.
48. Bjorck P, Coates PT, Wang Z, Duncan FJ, Thomson AW., Promotion of long-term heart allograft survival by combination of mobilized donor plasmacytoid dendritic cells and anti-CD154 monoclonal antibody. J Heart Lung Transplant 2005; 24: 1118-1120.
49. Ochando JC, Homma C, Yang Y, et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat Immunol 2006; 7: 652-662.
50. Liu X, Mishra P, Yu S, et al. Tolerance induction towards cardiac allografts under costimulation blockade is impaired in CCR7-deficient animals but can be restored by adoptive transfer of syngeneic plasmacytoid dendritic cells. Eur J Immunol 2011; 41: 611-623.
51. Li XL, Menoret S, Bezie S, et al. Mechanism and localization of CD8 regulatory T cells in a heart transplant model of tolerance. J Immunol 2010; 185: 823-833.
52. Fugier-Vivier IJ, Rezzoug F, Huang Y, et al. Plasmacytoid precursor dendritic cells facilitate allogeneic hematopoietic stem cell engraftment. J Exp Med 2005; 201: 373-383.
53. Banovic T, Markey KA, Kuns RD, et al. Graft-versus-host disease prevents the maturation of plasmacytoid dendritic cells. J Immunol 2009; 182: 912-920.
54. Gupta A, Kumar CA, Ningappa M, et al. Elevated myeloid: Plasmacytoid dendritic cell ratio associates with late, but not early, liver rejection in children induced with rabbit anti-human thymocyte globulin. Transplantation 2009; 88: 589-594.
55. Mazariegos GV, Zahorchak AF, Reyes J, et al. Dendritic cell subset ratio in peripheral blood correlates with successful withdrawal of immunosuppression in liver transplant patients. Am J Transplant 2003; 3: 689-696.
56. Tokita D, Sumpter TL, Raimondi G, et al. Poor allostimulatory function of liver plasmacytoid DC is associated with pro-apoptotic activity, dependent on regulatory T cells. J Hepatol 2008; 49: 1008-1018.
57. Paantjens AW, van de Graaf EA, Heerkens HD, et al. Chimerism of dendritic cell subsets in peripheral blood after lung transplantation. J Heart Lung Transplant 2011; 30: 691-697.
58. Mohty M, Blaise D, Faucher C, et al. Impact of plasmacytoid dendritic cells on outcome after reduced-intensity conditioning allogeneic stem cell transplantation. Leukemia 2005; 19: 1-6.
59. Rajasekar R, Lakshmi KM, George B, et al. Dendritic cell count in the graft predicts relapse in patients with hematologic malignancies undergoing an HLA-matched related allogeneic peripheral blood stem cell transplant. Biol Blood Marrow Transplant 2010; 16: 854-860.
60. Waller EK, Rosenthal H, Jones TW, et al. Larger numbers of CD4(bright) dendritic cells in donor bone marrow are associated with increased relapse after allogeneic bone marrow transplantation. Blood 2001; 97: 2948-2956.
61. Leventhal J, Abecassis M, Miller J, et al. Chimerism and tolerance without GVHD or engraftment syndrome in HLA-mismatched combined kidney and hematopoietic stem cell transplantation. Sci Transl Med 2012; 4: 124ra128.
62. Leventhal J, Abecassis M, Miller J, et al. Tolerance induction in HLA disparate living donor kidney transplantation by donor stem cell infusion: Durable chimerism predicts outcome. Transplantation 2013; 95: 169-176.
63. Young LJ, Wilson NS, Schnorrer P, et al. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat Immunol 2008; 9: 1244-1252.
64. Carotta S, Dakic A, D'Amico A, et al. The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 2010; 32: 628-641.
65. Matta BM, Raimondi G, Rosborough BR, Sumpter TL, Thomson AW., IL-27 production and STAT3-dependent upregulation of B7-H1 mediate immune regulatory functions of liver plasmacytoid dendritic cells. J Immunol 2012; 188: 5227-5237.
66. Tokita D, Mazariegos GV, Zahorchak AF, et al. High PD-L1/CD86 ratio on plasmacytoid dendritic cells correlates with elevated T-regulatory cells in liver transplant tolerance. Transplantation 2008; 85: 369-377.
67. Ito T, Yang M, Wang YH, et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007; 204: 105-115.
68. Mellor AL, Baban B, Chandler P, et al. Cutting edge: Induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol 2003; 171: 1652-1655.
69. Pallotta MT, Orabona C, Volpi C, et al. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol 2011; 12: 870-878.
70. Fallarino F, Asselin-Paturel C, Vacca C, et al. Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J Immunol 2004; 173: 3748-3754.
71. Grohmann U, Volpi C, Fallarino F, et al. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat Med 2007; 13: 579-586.
72. Huang Y, Bozulic LD, Miller T, Xu H, Hussain LR, Ildstad ST., CD8α+ plasmacytoid precursor DCs induce antigen-specific regulatory T cells that enhance HSC engraftment in vivo. Blood 2011; 117: 2494-2505.
73. Lu Y, Giver CR, Sharma A, et al. IFN-gamma and indoleamine 2,3-dioxygenase signaling between donor dendritic cells and T cells regulates graft versus host and graft versus leukemia activity. Blood 2012; 119: 1075-1085.