IL-10/TGF-β-treated dendritic cells, pulsed with insulin, specifically reduce the response to insulin of CD4+ effector/memory T cells from type 1 diabetic individuals

Journal of Clinical Immunology

Volumn 30, Issue 5, 2010, Pages 659-668

  Torres Aguilar, Honorio ^a   Sánchez Torres, Carmen ^b   Jara, Luis J ^c,d   Blank, Miri ^a   Shoenfeld, Yehuda ^a,e  

^a SHEBA MEDICAL CENTER   (Israel)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c HOSPITAL DE ESPECIALIDADES   (Mexico)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

Dendritic cells; effector memory T cells; tolerance; type 1 diabetes

Indexed keywords

CANDIDIN; CD4 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INSULIN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG MECHANISM; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOTHERAPY; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESPONSE; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MONOCYTE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ADULT; ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY; INSULIN; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MALE; T-LYMPHOCYTE SUBSETS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77957568166     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-010-9430-5     Document Type: Article

References (48)

1. M Knip H Slijander 2008 Autoimmune mechanisms in type 1 diabetes Autoimmun Rev 7 550 557 10.1016/j.autrev.2008.04.008 18625444 1:CAS:528:DC%2BD1cXhtVCntrjN
2. P Concannon SS Rich GT Nepom 2009 Genetics of type 1A diabetes N Engl J Med 360 1646 1654 10.1056/NEJMra0808284 19369670 1:CAS:528:DC%2BD1MXkvVKltbs%3D
3. Y Shoenfeld G Zandman-Goddard L Stojanovich M Cutolo H Amital Y Levy M Abu-Shakra O Barzilai Y Berkun M Blank JF de Carvalho A Doria B Gilburd U Katz I Krause P Langevitz H Orbach V Pordeus M Ram E Toubi Y Sherer 2008 The mosaic of autoimmunity: hormonal and environmental factors involved in autoimmune diseases Isr Med Assoc J 10 8 12 18300563 (Pubitemid 351649455)
4. CH Wasserfall MA Atkinson 2006 Autoantibody markers for the diagnosis and prediction of type 1 diabetes Autoimmun Rev 5 424 428 10.1016/j.autrev.2005.12. 002 16890898 1:CAS:528:DC%2BD28XhtVGiu7vP (Pubitemid 44150627)
5. V Guzit D Tasher A Hanukuglu Z Landau Y Ben-Yehuda E Somekh I Dalal 2008 Atopy in children and adolescents with insulin-dependent diabetes mellitus Isr Med Assoc J 10 858 861
6. S Sharif GA Arreaza P Zucker TL Delovitch 2002 Regulatory natural killer T cells protect against spontaneous and recurrent type 1 diabetes Ann NY Acad Sci 958 77 88 10.1111/j.1749-6632.2002.tb02949.x 12021086 1:CAS:528: DC%2BD38XltFaks7w%3D
7. TP Di Lorenzo M Peakman BO Roep 2007 Systematic analysis of T cell epitopes in autoimmune diabetes Clin Exp Immunol 148 1 16 10.1111/j.1365-2249. 2006.03244.x 17349009 (Pubitemid 46364983)
8. BO Roep 2003 The role of T-cells in the pathogenesis of Type 1 diabetes: from cause to cure Diabetologia 46 305 321 12687328 1:CAS:528: DC%2BD3sXksVWjtL4%3D
9. BO Roep 1996 T-cell responses to autoantigens in IDDM. The search for the Holy Grail Diabetes 45 1147 1156 10.2337/diabetes.45.9.1147 8772714 1:CAS:528:DyaK28XlsFemsLY%3D
10. RA Smerdon M Peakman MJ Hussain L Alviggi PJ Watkins RD Leslie D Vergani 1993 Increase in simultaneous coexpression of naive and memory lymphocyte markers at diagnosis of IDDM Diabetes 42 127 133 10.2337/diabetes.42.1.127 8420810 1:STN:280:DyaK3s7jtFSltQ%3D%3D
11. HS MarttilaJ O Vaarala K Suzyki JF Elliott A Narvanen M Knip O Simell J Ilonen 2008 T-cell reactivity to insulin peptide A1-12 in children with recently diagnosed type t diabetes or multiple beta-cell autoantibodies J Autoimmun 31 142 148 10.1016/j.jaut.2008.04.024 1:CAS:528:DC%2BD1cXhtVymsb%2FF
12. LD Petersen G Duinkerken GJ Bruining RA van Lier RR de Vries BO Roep 1996 Increased numbers of in vivo activated T cells in patients with recent onset insulin-dependent diabetes mellitus J Autoimmun 9 731 737 10.1006/jaut.1996.0095 9115575 1:STN:280:DyaK2s7msFGmug%3D%3D (Pubitemid 27047022)
13. PJ Fairchild JM Austyn 1990 Thymic dendritic cells: phenotype and function Int Rev Immunol 6 187 196 10.3109/08830189009056629 2152502 1:STN:280:DyaK3s3htVeqtQ%3D%3D
14. C Scheinecker 2002 Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node J Exp Med 196 1079 1090 10.1084/jem.20020991 12391019 1:CAS:528:DC%2BD38XotFGltbo%3D (Pubitemid 35231766)
15. R Steinman 2003 Tolerogenic dendritic cells Annu Rev Immunol 21 685 711 10.1146/annurev.immunol.21.120601.141040 12615891 1:CAS:528:DC%2BD3sXjtF2is7g%3D (Pubitemid 37174545)
16. MV Dhodapkar RM Steinman J Krasovsky C Munz N Bhardwaj 2001 Antigen-specific7 inhibition of effector T cell function in humans after injection of immature dendritic cells J Exp Med 193 233 238 10.1084/jem.193.2. 233 11208863 1:CAS:528:DC%2BD3MXksl2ntQ%3D%3D (Pubitemid 32524454)
17. K Mahnke E Schmitt L Bonifaz AH Enk H Jonuleit 2002 Immature, but not inactive: the tolerogenic function of immature dendritic cells Immunol Cell Biol 80 477 483 10.1046/j.1440-1711.2002.01115.x 12225384
18. M Menges S Rossner C Voigtländer H Schindler NA Kukutsch C Bogdan K Erb G Schuler MB Lutz 2002 Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity J Exp Med 195 15 21 10.1084/jem.20011341 11781361 1:CAS:528:DC%2BD38XjslKqtQ%3D%3D (Pubitemid 34074492)
19. S Rutella S Danese G Leone 2006 Tolerogenic dendritic cells: cytokine modulation comes of age Blood 108 1435 1440 10.1182/blood-2006-03-006403 16684955 1:CAS:528:DC%2BD28Xpt1Sltrk%3D (Pubitemid 44316106)
20. H Torres-Aguilar 2010 Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells J Immunol 184 1765 1775 10.4049/jimmunol.0902133 20083662 1:CAS:528:DC%2BC3cXhsVGltb0%3D
21. K Sato N Yamashita M Baba T Matsuyama 2003 Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells Blood 101 3581 3589 10.1182/blood-2002-09-2712 12511411 1:CAS:528: DC%2BD3sXjs1aqtrw%3D (Pubitemid 36857945)
22. M Wållberg EA Green 2009 Are B cells a potential target for therapeutic intervention in the classical T cell-mediated autoimmune disease type 1 diabetes? Inflamm Allergy Drug Targets 8 130 138 10.2174/ 187152809788462572 19530995
23. L Ma S Qian X Liang L Wang JE Woodward N Giannoukakis PD Robbins S Bertera M Trucco JJ Fung L Lu 2003 Prevention of diabetes in NOD mice by administration of dendritic cells deficient in nuclear transcription factor-kappaB activity Diabetes 52 1976 1985 10.2337/diabetes.52.8.1976 12882913 1:CAS:528:DC%2BD3sXlvFCgt7o%3D (Pubitemid 36919789)
24. A Mukhopadhaya T Hanafusa I Jarchum YG Chen Y Iwai DV Serreze RM Steinman KV Tarbell TP DiLorenzo 2008 Selective delivery of beta cell antigen to dendritic cells in vivo leads to deletion and tolerance of autoreactive CD8+ T cells in NOD mice Proc Natl Acad Sci USA 105 6374 6379 10.1073/pnas.0802644105 18430797 (Pubitemid 351758353)
25. CQ Xia R Peng Y Qiu M Annamalai D Gordon MJ Clare-Salzler 2007 Transfusion of apoptotic beta-cells induces immune tolerance to beta-cell antigens and prevents type 1 diabetes in NOD mice Diabetes 56 2116 2123 10.2337/db06-0825 17496235 1:CAS:528:DC%2BD2sXos12qsLk%3D (Pubitemid 47195837)
26. B Krishnamurthy NL Dudek MD McKenzie AW Purcell AG Brooks S Gellert PG Colman LC Harrison AM Lew HE Thomas TW Kay 2006 Responses against islet antigens in NOD mice are prevented by tolerance to proinsulin but not IGRP J Clin Invest 116 3258 3265 10.1172/JCI29602 17143333 1:CAS:528:DC%2BD28XhtlWgsbnJ (Pubitemid 44878640)
27. C Aspord C Thivolet 2002 Nasal administration of CTB-insulin induces active tolerance against autoimmune diabetes in non-obese diabetic (NOD) mice Clin Exp Immunol 130 204 211 10.1046/j.1365-2249.2002.01988.x 12390307 1:CAS:528:DC%2BD38XovFWitro%3D (Pubitemid 35286206)
28. TG Markees DV Serreze NE Phillips CH Sorli EJ Gordon LD Shultz RJ Noelle BA Woda DL Greiner JP Mordes AA Rossini 1999 NOD mice have a generalized defect in their response to transplantation tolerance induction Diabetes 48 967 974 10.2337/diabetes.48.5.967 10331399 1:CAS:528:DyaK1MXjtFSgsbw%3D (Pubitemid 29226341)
29. TA Waldman S Dubois Y Tagaya 2001 Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy Immunity 14 105 110
30. FG Lakkis MH Sayegh 2003 Memory T cells: a hurdle to immunologic tolerance J Am Soc Nephrol 14 2402 2410 10.1097/01.ASN.0000085020.78117.70 12937320 (Pubitemid 37052389)
31. M Jenkins 1992 Memory and anergy: challenges to traditional T lymphocyte differentiation FASEB J 6 2428 2433 1563595 1:CAS:528:DyaK38Xitlegtr0%3D
32. AE Anderson BL Sayers MA Haniffa DJ Swan J Diboll XN Wang JD Isaacs CM Hilkens 2008 Differential regulation of naive and memory CD4+ T cells by alternatively activated dendritic cells J Leukoc Biol 84 124 133 10.1189/jlb.1107744 18430785 1:CAS:528:DC%2BD1cXot1Okt70%3D (Pubitemid 351960287)
33. ME Call KW Wucherpfennig 2005 The T cell receptor: critical role of the membrane environment in receptor assembly and function Annu Rev Immunol 23 101 125 10.1146/annurev.immunol.23.021704.115625 15771567 1:CAS:528: DC%2BD2MXktFOjtbs%3D (Pubitemid 40563166)
34. ML Ford BH Koehn ME Wagener W Jiang S Gangappa TC Pearson CP Larsen 2007 Antigen-specific precursor frequency impacts T cell proliferation, differentiation, and requirement for costimulation J Exp Med 204 299 309 10.1084/jem.20062319 17261633 1:CAS:528:DC%2BD2sXitVektL4%3D (Pubitemid 46294546)
35. SM Anderton DC Wraith 2002 Selection and fine-tuning of the autoimmune T-cell repertoire Nat Rev Immunol 2 487 498 10.1038/nri842 12094223 1:CAS:528:DC%2BD38XkvFKksrY%3D
36. LS Walker AK Abbas 2002 The enemy within: keeping self-reactive T cells at bay in the periphery Nat Rev Immunol 2 11 19 10.1038/nri701 11908514 1:CAS:528:DC%2BD38Xhslyit7k%3D
37. T Mustelin T Vang N Bottini 2005 Protein tyrosine phosphatases and the immune response Nat Rev Immunol 5 43 57 10.1038/nri1530 15630428 1:CAS:528:DC%2BD2MXlvVOk (Pubitemid 40070330)
38. LJ Appleman VA Boussiotis 2003 T cell anergy and costimulation Immunol Rev 192 161 180 10.1034/j.1600-065X.2003.00009.x 12670403 1:CAS:528: DC%2BD3sXjsVOntL4%3D (Pubitemid 36613331)
39. C Caux C Massacrier B Vanbervliet B Dubois C Van Kooten I Durand J Banchereau 1994 Activation of human dendritic cells through CD40 cross-linking J Exp Med 180 1263 1272 10.1084/jem.180.4.1263 7523569 1:CAS:528: DyaK2cXlslOiurw%3D
40. U Grohmann R Bianchi C Orabona F Fallarino C Vacca A Micheletti MC Fioretti P Puccetti 2003 Functional plasticity of dendritic cell subsets as mediated by CD40 versus B7 activation J Immunol 171 2581 2587 12928409 1:CAS:528:DC%2BD3sXmsVOrur8%3D
41. Y Cai YR Yang P Xia SL Zheng 2006 Blockade of CD154-CD40 pathway induces interleukin-10 dependent T regulatory type 1 like cells Chin Med J (Engl) 119 518 522 1:CAS:528:DC%2BD28XjslWjurk%3D
42. SA Nanji WW Hancock B Luo CD Schur RL Pawlick LF Zhu CC Anderson AM Shapiro 2006 Costimulation blockade of both inducible costimulator and CD40 ligand induces dominant tolerance to islet allografts and prevents spontaneous autoimmune diabetes in the NOD mouse Diabetes 55 27 33 10.2337/diabetes.55.01. 06.db04-1154 16380473 1:CAS:528:DC%2BD28XlvVSmsQ%3D%3D
43. PA Taylor TM Friedman R Korngold RJ Noelle BR Blazar 2002 Tolerance induction of alloreactive T cells via ex vivo blockade of the CD40:CD40L costimulatory pathway results in the generation of a potent immune regulatory cell Blood 99 4601 4609 10.1182/blood.V99.12.4601 12036894 1:CAS:528: DC%2BD38XksFGksb4%3D (Pubitemid 34627233)
44. M Casamayor-Palleja M Khan IC MacLennan 1995 A subset of CD4+ memory T cells contains preformed CD40 ligand that is rapidly but transiently expressed on their surface after activation through the T cell receptor complex J Exp Med 181 1293 1301 10.1084/jem.181.4.1293 7699321 1:STN:280:DyaK2M3htlKmtg%3D%3D
45. M Koschella D Voehringer H Pircher 2004 CD40 ligation in vivo induces bystander proliferation of memory phenotype CD8 T cells J Immunol 172 4804 4811 15067057 1:CAS:528:DC%2BD2cXivVShsr8%3D
46. M Feili-Hariri DH Falkner PA Morel 2002 Regulatory Th2 response induced following adoptive transfer of dendritic cells in prediabetic NOD mice Eur J Immunol 32 2021 2030 10.1002/1521-4141(200207)32:7<2021::AID-IMMU2021>3.0. CO;2-J 12115623 1:CAS:528:DC%2BD38XlsFaju70%3D (Pubitemid 34814559)
47. Y Li N Chu A Rostami GX Zhang 2006 Dendritic cells transduced with SOCS-3 exhibit a tolerogenic/DC2 phenotype that directs type 2 Th cell differentiation in vitro and in vivo J Immunol 177 1679 1688 16849477 1:CAS:528: DC%2BD28XmvFCmu74%3D
48. Y Yamaguchi H Tsumura M Miwa K Inaba 1997 Contrasting effects of TGF-beta 1 and TNF-alpha on the development of dendritic cells from progenitors in mouse bone marrow Stem Cells 15 144 153 10.1002/stem.150144 9090791 1:CAS:528:DyaK2sXis1Kjsbg%3D