Blockade of the programmed death-1 (PD1) pathway undermines potent genetic protection from type 1 diabetes

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Kochupurakkal, Nora M ^a   Kruger, Annie J ^b   Tripathi, Sudipta ^a   Zhu, Bing ^a   Adams, La Tonya ^a   Rainbow, Daniel B ^c   Rossini, Aldo ^b   Greiner, Dale L ^b   Sayegh, Mohamed H ^a   Wicker, Linda S ^c   Guleria, Indira ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME 1; CHROMOSOME 3; CHROMOSOME 4; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DISEASE RESISTANCE; DISEASE SEVERITY; FEMALE; GENE; GENE FREQUENCY; GENE LOCUS; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IDD GENE; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MOUSE; NONHUMAN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD274; DIABETES MELLITUS, TYPE 1; FEMALE; GENETIC PREDISPOSITION TO DISEASE; IMMUNOTHERAPY; MICE; MICE, INBRED NOD; PROGRAMMED CELL DEATH 1 RECEPTOR; SIGNAL TRANSDUCTION;

EID: 84896530741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089561     Document Type: Article

References (51)

1. Blank C, Mackensen A (2007) Contribution of the PD-L1/PD-1 pathway to Tcell exhaustion: an update on implications for chronic infections and tumor evasion. Cancer Immunol Immunother 56: 739-745. (Pubitemid 46348742)
2. Zhou Q, Munger ME, Highfill SL, Tolar J, Weigel BJ, et al. Program death-1 signaling and regulatory T cells collaborate to resist the function of adoptively transferred cytotoxic T lymphocytes in advanced acute myeloid leukemia. Blood 116: 2484-2493.
3. Trautmann L, Janbazian L, Chomont N, Said EA, Gimmig S, et al. (2006) Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 12: 1198-1202. (Pubitemid 44527357)
4. Guleria I, Gubbels Bupp M, Dada S, Fife B, Tang Q, et al. (2007) Mechanisms of PDL1-mediated regulation of autoimmune diabetes. Clin Immunol 125: 16-25. (Pubitemid 47376921)
5. Fife BT, Pauken KE, Eagar TN, Obu T, Wu J, et al. (2009) Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat Immunol 10: 1185-1192.
6. Wang J, Yoshida T, Nakaki F, Hiai H, Okazaki T, et al. (2005) Establishment of NOD-Pdcd1-/- mice as an efficient animal model of type I diabetes. Proc Natl Acad Sci U S A 102: 11823-11828. (Pubitemid 41170809)
7. Driver JP, Serreze DV, Chen YG (2011) Mouse models for the study of autoimmune type 1 diabetes: a NOD to similarities and differences to human disease. Semin Immunopathol 33: 67-87.
8. Wicker LS, Todd JA, Peterson LB (1995) Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 13: 179-200.
9. Hamilton-Williams EE, Cheung J, Rainbow DB, Hunter KM, Wicker LS, et al. (2012) Cellular mechanisms of restored beta-cell tolerance mediated by protective alleles of Idd3 and Idd5. Diabetes 61: 166-174.
10. Liu SM, Lee DH, Sullivan JM, Chung D, Jager A, et al. (2011) Differential IL-21 signaling in APCs leads to disparate Th17 differentiation in diabetes-susceptible NOD and diabetes-resistant NOD.Idd3 mice. J Clin Invest 121: 4303-4310.
11. Anderson AC, Chandwaskar R, Lee DH, Kuchroo VK (2008) Cutting edge: the Idd3 genetic interval determines regulatory T cell function through CD11b+ CD11c- APC. J Immunol 181: 7449-7452.
12. Yamanouchi J, Rainbow D, Serra P, Howlett S, Hunter K, et al. (2007) Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat Genet 39: 329-337. (Pubitemid 46328484)
13. D'Alise AM, Auyeung V, Feuerer M, Nishio J, Fontenot J, et al. (2008) The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc Natl Acad Sci U S A 105: 19857-19862.
14. Rainbow DB, Moule C, Fraser HI, Clark J, Howlett SK, et al. (2011) Evidence that Cd101 is an autoimmune diabetes gene in nonobese diabetic mice. J Immunol 187: 325-336.
15. Fraser HI, Dendrou CA, Healy B, Rainbow DB, Howlett S, et al. (2010) Nonobese diabetic congenic strain analysis of autoimmune diabetes reveals genetic complexity of the Idd18 locus and identifies Vav3 as a candidate gene. J Immunol 184: 5075-5084.
16. Hamilton-Williams EE, Martinez X, Clark J, Howlett S, Hunter KM, et al. (2009) Expression of diabetes-associated genes by dendritic cells and CD4 T cells drives the loss of tolerance in nonobese diabetic mice. J Immunol 183: 1533-1541.
17. Dai YD, Marrero IG, Gros P, Zaghouani H, Wicker LS, et al. (2009) Slc11a1 enhances the autoimmune diabetogenic T-cell response by altering processing and presentation of pancreatic islet antigens. Diabetes 58: 156-164.
18. Araki M, Chung D, Liu S, Rainbow DB, Chamberlain G, et al. (2009) Genetic evidence that the differential expression of the ligand-independent isoform of CTLA-4 is the molecular basis of the Idd5.1 type 1 diabetes region in nonobese diabetic mice. J Immunol 183: 5146-5157.
19. Kissler S, Stern P, Takahashi K, Hunter K, Peterson LB, et al. (2006) In vivo RNA interference demonstrates a role for Nramp1 in modifying susceptibility to type 1 diabetes. Nat Genet 38: 479-483.
20. Irie J, Reck B, Wu Y, Wicker LS, Howlett S, et al. (2008) Genome-wide microarray expression analysis of CD4+ T Cells from nonobese diabetic congenic mice identifies Cd55 (Daf1) and Acadl as candidate genes for type 1 diabetes. J Immunol 180: 1071-1079.
21. Hamilton-Williams EE, Rainbow DB, Cheung J, Christensen M, Lyons PA, et al. (2013) Fine mapping of type 1 diabetes regions Idd9.1 and Idd9.2 reveals genetic complexity. Mamm Genome 24: 358-375.
22. Lyons PA, Hancock WW, Denny P, Lord CJ, Hill NJ, et al. (2000) The NOD Idd9 genetic interval influences the pathogenicity of insulitis and contains molecular variants of Cd30, Tnfr2, and Cd137. Immunity 13: 107-115.
23. Yamanouchi J, Puertas MC, Verdaguer J, Lyons PA, Rainbow DB, et al. (2010) Idd9.1 locus controls the suppressive activity of FoxP3+CD4+CD25+ regulatory T-cells. Diabetes 59: 272-281.
24. Matsuki N, Stanic AK, Embers ME, Van Kaer L, Morel L, et al. (2003) Genetic dissection of V alpha 14J alpha 18 natural T cell number and function in autoimmune-prone mice. J Immunol 170: 5429-5437. (Pubitemid 36617829)
25. Hamilton-Williams EE, Wong SB, Martinez X, Rainbow DB, Hunter KM, et al. (2010) Idd9.2 and Idd9.3 protective alleles function in CD4+ T-cells and nonlymphoid cells to prevent expansion of pathogenic islet-specific CD8+ Tcells. Diabetes 59: 1478-1486.
26. Cannons JL, Chamberlain G, Howson J, Smink LJ, Todd JA, et al. (2005) Genetic and functional association of the immune signaling molecule 4-1BB (CD137/TNFRSF9) with type 1 diabetes. J Autoimmun 25: 13-20. (Pubitemid 41008662)
27. Waldner H, Sobel RA, Price N, Kuchroo VK (2006) The autoimmune diabetes locus Idd9 regulates development of type 1 diabetes by affecting the homing of islet-specific T cells. J Immunol 176: 5455-5462.
28. Robles DT, Eisenbarth GS, Dailey NJ, Peterson LB, Wicker LS (2003) Insulin autoantibodies are associated with islet inflammation but not always related to diabetes progression in NOD congenic mice. Diabetes 52: 882-886. (Pubitemid 36323599)
29. Podolin PL, Denny P, Armitage N, Lord CJ, Hill NJ, et al. (1998) Localization of two insulin-dependent diabetes (Idd) genes to the Idd10 region on mouse chromosome 3. Mamm Genome 9: 283-286. (Pubitemid 28181025)
30. Penha-Goncalves C, Moule C, Smink LJ, Howson J, Gregory S, et al. (2003) Identification of a structurally distinct CD101 molecule encoded in the 950-kb Idd10 region of NOD mice. Diabetes 52: 1551-1556. (Pubitemid 36666213)
31. Wicker LS, Chamberlain G, Hunter K, Rainbow D, Howlett S, et al. (2004) Fine mapping, gene content, comparative sequencing, and expression analyses support Ctla4 and Nramp1 as candidates for Idd5.1 and Idd5.2 in the nonobese diabetic mouse. J Immunol 173: 164-173. (Pubitemid 38797338)
32. Hunter K, Rainbow D, Plagnol V, Todd JA, Peterson LB, et al. (2007) Interactions between Idd5.1/Ctla4 and other type 1 diabetes genes. J Immunol 179: 8341-8349.
33. Lin X, Hamilton-Williams EE, Rainbow DB, Hunter KM, Dai YD, et al. (2013) Genetic interactions among Idd3, Idd5.1, Idd5.2, and Idd5.3 protective loci in the nonobese diabetic mouse model of type 1 diabetes. J Immunol 190: 3109-3120.
34. Luhder F, Katz J, Benoist C, Mathis D (1998) Major histocompatibility complex class II molecules can protect from diabetes by positively selecting T cells with additional specificities. J Exp Med 187: 379-387. (Pubitemid 28080067)
35. Yamazaki T, Akiba H, Iwai H, Matsuda H, Aoki M, et al. (2002) Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 169: 5538-5545. (Pubitemid 35291652)
36. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, et al. (2000) B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
37. Pearson T, Markees TG, Wicker LS, Serreze DV, Peterson LB, et al. (2003) NOD congenic mice genetically protected from autoimmune diabetes remain resistant to transplantation tolerance induction. Diabetes 52: 321-326. (Pubitemid 36173185)
38. Hill NJ, Lyons PA, Armitage N, Todd JA, Wicker LS, et al. (2000) NOD Idd5 locus controls insulitis and diabetes and overlaps the orthologous CTLA4/IDDM12 and NRAMP1 loci in humans. Diabetes 49: 1744-1747.
39. Cameron MJ, Arreaza GA, Grattan M, Meagher C, Sharif S, et al. (2000) Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J Immunol 165: 1102-1110. (Pubitemid 30484782)
40. Ridgway WM, Peterson LB, Todd JA, Rainbow DB, Healy B, et al. (2008) Gene-gene interactions in the NOD mouse model of type 1 diabetes. Adv Immunol 100: 151-175.
41. Bour-Jordan H, Thompson HL, Giampaolo JR, Davini D, Rosenthal W, et al. Distinct genetic control of autoimmune neuropathy and diabetes in the nonobese diabetic background. J Autoimmun 45: 58-67.
42. Chamberlain G, Wallberg M, Rainbow D, Hunter K, Wicker LS, et al. (2006) A 20-Mb region of chromosome 4 controls TNF-alpha-mediated CD8+ T cell aggression toward beta cells in type 1 diabetes. J Immunol 177: 5105-5114. (Pubitemid 44527581)
43. Paterson AM, Brown KE, Keir ME, Vanguri VK, Riella LV, et al. (2011) The programmed death-1 ligand 1:B7-1 pathway restrains diabetogenic effector T cells in vivo. J Immunol 187: 1097-1105.
44. Kadri N, Korpos E, Gupta S, Briet C, Lofbom L, et al. (2012) CD4(+) type II NKT cells mediate ICOS and programmed death-1-dependent regulation of type 1 diabetes. J Immunol 188: 3138-3149.
45. Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, et al. (2008) Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28: 687-697.
46. Grinberg-Bleyer Y, Baeyens A, You S, Elhage R, Fourcade G, et al. (2010) IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J Exp Med 207: 1871-1878.
47. Zhang L, Gajewski TF, Kline J (2009) PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 114: 1545-1552.
48. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366: 2443-2454.
49. Freeman GJ, Wherry EJ, Ahmed R, Sharpe AH (2006) Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J Exp Med 203: 2223-2227. (Pubitemid 44498355)
50. Quigley M, Pereyra F, Nilsson B, Porichis F, Fonseca C, et al. (2010) Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med 16: 1147-1151.
51. Ansari MJ, Salama AD, Chitnis T, Smith RN, Yagita H, et al. (2003) The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 198: 63-69. (Pubitemid 36870186)