The cross-regulatory relationship between human dendritic and regulatory T cells and its role in type 1 diabetes mellitus

Review of Diabetic Studies

Volumn 4, Issue 2, 2007, Pages 68-76

  Chang, Hsuen Wen ^a   Chow, Yen Hung ^a   Chong, Pele ^a   Sia, Charles ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

Anergy; Antigen; Dendritic cells; Treg cells; Type 1 diabetes

Indexed keywords

CELL ACTIVATION; DENDRITIC CELL; DOWN REGULATION; HUMAN; IMMUNOREGULATION; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION;

EID: 34548828531     PISSN: 16136071     EISSN: 16140575     Source Type: Journal    
DOI: 10.1900/RDS.2007.4.68     Document Type: Review

References (66)

1. Garcia CA, Prabakar KR, Diez J, Cao ZA, Allende G, Zeller M, Dogra R, Mendez A, Rosenkranz E, Dahl U, Ricordi C, Hanahan D, Pugliese A. Dendritic cells in human thymus and periphery display a proinsulin epitope in a transcription-dependent, capture-independent fashion. J Immunol 2005. 175:2111-2122.
2. Sospedra M, Ferrer-Francesch X, Dominguez O, Juan M, Foz-Sala M, Pujol-Borrell R. Transcription of broad range of self-antigens in human thymus suggests a role for central mechanisms in tolerance toward peripheral antigens. J Immunol 1998. 161:5918-5929.
3. Pugliese A, Zeller M, Fernandez A Jr, Zalcberg LJ, Bartlett RJ, Ricordi C, Pietropaolo M, Eisenbarth GS, Bennett ST, Patel DD. The insulin gene is transcribed in the human thymus and transcription levels correlated with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type 1 diabetes. Nat Genet 1997. 15:293-297.
4. Mannering SI, Morris JS, Stone NI, Jensen KP, van Endert PM and Harrison LC. CD4+ T cell proliferation in response to GAD and proinsulin in healthy, pre-diabetic, and diabetic donors. Ann NY Acad Sci 2004. 1037:16-21.
5. Oling V, Marttila J, Ilonen J, Kwok WW, Nepom G, Knip M, Simell O, Reijonen H. GAD65- and proinsulin-specific CD4+ T-cells detected by MHC class II tetramers in peripheral blood of type 1 diabetes patients and at-risk subjects. J Autoimmun 2005. 25(3):235-243.
6. Gronski MA, Weinem M. Death pathways in T cell homeostasis and their role in autoimmune diabetes. Rev Diabet Stud 2006. 3(2):88-95.
7. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003. 21:685-711.
8. Steinman RM, Pack M, Inaba K. Dendritic cell development and maturation. In: Ricciardi-Castagnoli P (ed.). Dendritic cells in fundamental and clinical immunology. Vol. 3, Plenum Press, New York, 1997, p. 1-6.
9. Ardavin C, Martinez del Hoyo G, Martin P, Anjuere F, Arias CF, Marin AR, Ruiz S, Parrillas V, Hernandez H. Origin and differentiation of dendritic cells. Trends Immunol 2001. 22(12):691-700.
10. Olweus J, BitMansour A, Warnke R, Thompson PA, Carballido J, Picker LJ, Lund-Johansen F. Dendritic cell ontogeny: a human dendritic cell lineage of myeloid origin. Proc Natl Acad Sci USA 1997. 94(23):12551-12556.
11. Coccia EM, Severa M, Giacomini E, Monneron D, Remoli ME, Julkunen I, Cella M, Lande R, Uze G. Viral infection and toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur J Immunol 2004. 34(3):796-805.
12. Thomas R, Lipsky PE. Human peripheral blood dendritic cell subsets. Isolation and characterization of precursor and mature antigen-presenting cells. J Immunol 1994. 153(9):4016-4028.
13. Rissoan MC, Soumelis V, Kadowaki N, Grouard G, Briere F, de Waal Malefyt R, Liu YJ. Reciprocal control of T helper cell and dendritic cell differentiation. Science 1999. 283(5405):1183-1186.
14. Kohrgruber N, Halanek N, Groger M, Winter D, Rappersberger K, Schmitt-Egenolf M, Stingl G, Maurer D. Survival, maturation, and function of CD11c- and CD11c+ peripheral blood dendritic cells are differentially regulated by cytokines. J Immunol 1999. 163:3250-3259.
15. 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(6):1101-1111.
16. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J. BDCA-2, BDCA-3 and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000. 165(11):6037-6046.
17. Ito T, Wang YH, Liu YJ. Plasmacytoid dendritic cell precursors/type I interferon-producing cells sense viral infection by Toll-like receptor (TLR) 7 and TLR9. Springer Semin Immunopathol 2005. 26(3):221-229.
18. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, Colonna M. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999. 5(8):919-923.
19. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, Antonenko S, Liu YJ. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999. 284(5421):1835-1837.
20. Kuwana M, Kaburaki J, Wright TM, Kawakami T, Ikeda Y. Induction of antigen-specific human CD4+ T cell anergy by peripheral blood DC2 precursors. Eur J Immunol 2001. 31(9):2547-2557.
21. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 1994. 179:1109-1118.
22. Quaratino S, Duddy LP, Londei M. Fully competent dendritic cells as inducers of T cell anergy in autoimmunity. Proc Natl Acad Sci USA 2000. 97(20):10911-10916.
23. 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. 25:2668-2672.
24. Corinti S, Albanesi C, la Sala A, Pastore S, Girolomoni G. Regulatory activity of autocrine IL-10 on dendritic cell functions. J Immunol 2001. 166:4312-4318.
25. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1997. 159(10):4772-4780.
26. 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.
27. Cella M, Facchetti F, Lanzavecchia A, Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent Th1 polarization. Nat Immunol 2000. 1:305-310.
28. Rissoan MC, Soumelis V, Kadowaki N, Grouard G, Briere F, Malefyt R de W and Liu YJ. Reciprocal Control of T Helper Cell and Dendritic Cell Differentiation. Science 1999, 283(5405): 1183-2001.
29. + regulatory T cells in human thymus. Nature 2005. 436:1181-1185.
30. 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(9):1213-1222.
31. Lundqvist A, Palmborg A, Pavlenko M, Levitskaya J, Pisa P. Mature dendritic cells induce tumor-specific type 1 regulatory T cells. J Immunother (1997) 2005. 28(3):229-235.
32. Gray CP, Arosio P, Hersey P. Heavy chain ferritin activates regulatory T cells by induction of changes in dendritic cells. Blood 2002. 99(9):3326-3334.
33. Penna G, Adorini L. 1alpha,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.
34. Gilliet M, Liu YJ. Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J Exp Med 2002. 195(6):695-704.
35. Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, Qin XF, Liu YJ, Gilliet M. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007. 204(1):105-115.
36. Kvale EO, Floisand Y, Lund-Johansen F, Rollag H, Farkas L, Ghanekar S, Brandtzaeg P, Jahnsen JL, Olweus J. Plasmacytoid DCs regulate recall reponses by rapid induction of IL-10 in memory T cells. Blood 2007. 109(8):3369-3376.
37. Moseman A, Liang X, Dawson AJ, Panoskaltsis-Mortari A, Krieg AM, Liu YJ, Blazar BR, Chen W. Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J Immunol 2004. 173:4433-4442.
38. Misra N, Bayry J, Lacroix-Desmazes S, Kazatchkine MD, Kavri SV. Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J Immunol 2004. 172:4676-4680.
39. Houot R, Perrot I, Garcia E, Durand I, Lebecque S. Human CD4+CD25high regulatory T cells modulate myeloid but not plasmacytoid dendritic cells activation. J Immunol 2006. 176:5293-5298.
40. Kryczek I, Wei S, Zou L, Zhu G, Mottram P, Xu H, Chen L, Zou W. Cutting edge: induction of B7-H4 on APCs through IL-10: novel suppressive mode for regulatory T cells. J Immunol 2006. 177:40-44.
41. Jansen A, van Hagen M, Drexhage HA. Defective maturation and function of antigen-presenting cells in type 1 diabetes. Lancet 1995. 345:491-492.
42. Takahashi K, Honeyman MC, Harrison LC. Impaired yield, phenotype, and function of monocyte-derived dendritic cells in humans at risk for insulin-dependent diabetes. J Immunol 1998. 161:2629-2635.
43. Zacher T, Knerr I, Rascher W, Kalden JR, Wassmuth R. Characterization of monocyte-derived dendritic cells in recent-onset diabetes mellitus type 1. Clin Immunol 2002. 105(1):17-24.
44. Skarsvik S, Tiittanen M, Lindstrom A, Casas R , Ludvigsson J, Vaarala O. Poor in vitro maturation and proinflammatory cytokine response of dendritic cells in children at genetic risk of type 1 diabetes. Scand J Immunol 2004. 60(6):647-652.
45. Peng R, Li Y, Brezner K, Litherland S, Clare-Salzler MJ. Abnormal peripheral blood dendritic cell populations in type 1 diabetes. Ann NY Acad Sci 2003. 1005(1): 222-225.
46. Summers KL, Behme MT, Mahon JL, Singh B. Characterization of dendritic cells in humans with type 1 diabetes. Ann NY Acad Sci 2003. 1005:222-229.
47. Summers KL, Marleau AM, Mahon JL, McManus R, Hramiak I, Singh B. Reduced IFN-alpha secretion by blood dendritic cells in human diabetes. Clin Immunol 2006. 121(1):81-89.
48. Vuckovic S, Withers G, Harris M, Khalil D, Gardiner D, Flesch I, Tepes S, Greer R, Cowley D, Cotterill A, Hart DN. Decreased blood dendritic cell counts in type 1 diabetic children. Clin Immunol 2007. 123:281-288.
49. Szabolcs P, Park KD, Reese M, Marti L, Broadwater G, Kurtzberg J. Absolute values of dendritic cell subsets in bone marrow, cord blood, and peripheral blood enumerated by a novel method. Stem Cells 2003. 21(3):296-303.
50. Angelini F, Del Duca E, Piccinini S, Pacciani V, Rossi P, Manca Bitti ML. Altered phenotype and function of dendritic cells in children with type 1 diabetes. Clin Exp Immunol 2005. 142(2):341-346.
51. Syme R, Bajwa R, Robertson L, Stewart D, Gluck S. Comparison of CD34 and monocyte-derived dendritic cells from mobilized peripheral blood from cancer patients. Stem Cells 2005. 23(1):74-81.
52. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005. 6(4):345-352.
53. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005. 6:338-344.
54. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis, Nature 1997. 389(6652):737-742.
55. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006. 212:28-50.
56. Fukaura H, Kent SC, Pietrusewicz MJ, Khoury SJ, Weiner HL, Hafler DA. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-beta1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J Clin Invest 1996. 98(1):70-77.
57. Ciubotariu R, Vasilescu R, Ho E, Cinti P, Cancedda C, Poli L, Late M, Liu Z, Berloco P, Cortesini R, Suciu-Foca Cortesini N. Detection of T suppressor cells in patients with organ allografts. Hum Immunol 2001. 62(1):15-20.
58. Kukreja A, Cost G, Marker J, Zhang C, Sun Z, Su KL, Ten S, Sanz M, Exley M, Wilson B, Porcelli S, Maclaren N. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 2002. 109(1):131-140.
59. Michalek J, Vrabelova Z, Hrotekova Z, Kyr M, Pejchlova M, Kolouskova S, Faresjo M, Stechova K. Immune regulatory T cells in siblings of children suffering from type 1 diabetes mellitus. Scand J Immunol 2006. 64:531-535.
60. Lindley S, Dayan CM, Bishop A, Roep BO, Peakman M, Tree TI. Defective suppressor function in CD4+CD25+ Tcells from patients with type 1 diabetes. Diabetes 2005. 54(1):92-99.
61. Putnam AL, Vendrame F, Dotta F, Gottlieb PA. CD4+CD25high regulatory T cells in human autoimmune diabetes. J Autoimmunity 2005. 24(1):55-62.
62. Yang Z, Zhou Z, Huang G, Ling H, Yan X, Peng J, Li X. The CD4+ regulatory T-cells is decreased in adults with latent autoimmune diabetes. Diab Res Clin Pract 2007. 76(1):126-131.
63. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25high regulatory cells in human peripheral blood. J Immunol 2001. 167(3):1245-1253.
64. Brusko T, Wasserfall C, McGrail K, Schatz R, Viener HL, Schatz D, Haller M, Rockell J, Gottlieb P, Clare-Salzler M, Atkinson M. No alterations in the frequency of FOXP3+ regulatory T-cells in type 1 diabetes. Diabetes 2007. 56(3):604-612.
65. Chen C, Lee WH, Yun P, Snow P, Liu CP. Induction of autoantigen-specific Th2 and Tr1 regulatory T cells and modulation of autoimmune diabetes. J Immunol 2003. 171:733-744.
66. Battaglia M, Stabilini A, Draghici E, Migliavacca B, Gregori S, Bonifacio E, Roncarolo MG. Induction of tolerance in type 1 diabetes via both CD4+CD25+ T regulatory cells and T regulatory type 1 cells. Diabetes 2006. 55(6):1571-1580.