Autoreactive cytotoxic T lymphocytes acquire higher expression of cytotoxic effector markers in the islets of NOD mice after priming in pancreatic lymph nodes

American Journal of Pathology

Volumn 178, Issue 6, 2011, Pages 2716-2725

  Graham, Kate L ^a   Krishnamurthy, Balasubramanian ^a   Fynch, Stacey ^a   Mollah, Zia U ^a   Slattery, Robyn ^b   Santamaria, Pere ^c   Kay, Thomas W ^a,d   Thomas, Helen E ^a,d  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; FINGOLIMOD; GAMMA INTERFERON; GRANZYME B; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DIABETES MELLITUS; DIABETOGENESIS; LYMPH NODE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; PANCREATIC LYMPH NODE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 79959452187     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.02.015     Document Type: Article

References (55)

1. + T-cells from diabetic versus prediabetic NODNONThy- 1a donors. Diabetes 1993, 42:44-55 (Pubitemid 23013794)
2. Hoglund P, Mintern J, Waltzinger C, Heath W, Benoist C, Mathis D: Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J Exp Med 1999, 189:331-339 (Pubitemid 29063254)
3. Gagnerault MC, Luan JJ, Lotton C, Lepault F: Pancreatic lymph nodes are required for priming of β cell reactive T cells in NOD mice. J Exp Med 2002, 196:369-377 (Pubitemid 34875666)
4. Coles RM, Mueller SN, Heath WR, Carbone FR, Brooks AG: Progression of armed CTL from draining lymph node to spleen shortly after localized infection with herpes simplex virus 1. J Immunol 2002, 168:834-838 (Pubitemid 34049585)
5. Jones CM, Cose SC, Coles RM, Winterhalter AC, Brooks AG, Heath WR, Carbone FR: Herpes simplex virus type 1-specific cytotoxic T-lymphocyte arming occurs within lymph nodes draining the site of cutaneous infection. J Virol 2000, 74:2414-2419 (Pubitemid 30091496)
6. + T cells during pulmonary influenza virus infection. J Immunol 2004, 173:1209-1218 (Pubitemid 38924298)
7. + T cells in influenza virus-infected mice. Proc Natl Acad Sci U S A 2003, 100:2657-2662 (Pubitemid 36297554)
8. + T cells recovered from an influenza pneumonia differentiate to a state of focused gene expression. Proc Natl Acad Sci U S A 2005, 102:6074-6079 (Pubitemid 40594257)
9. Kohlmeier JE, Cookenham T, Roberts AD, Miller SC, Woodland DL: Type I interferons regulate cytolytic activity of memory CD8(+) T cells in the lung airways during respiratory virus challenge. Immunity 2010, 33:96-105
10. McGill J, Van Rooijen N, Legge KL: Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med 2008, 205:1635-1646
11. Wakim LM, Gebhardt T, Heath WR, Carbone FR: Cutting edge: local recall responses by memory T cells newly recruited to peripheral nonlymphoid tissues. J Immunol 2008, 181:5837-5841
12. Bottazzo GF, Dean BM, McNally JM, MacKay EH, Swift PG, Gamble DR: In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis. N Engl J Med 1985, 313:353-360 (Pubitemid 15046367)
13. Itoh N, Hanafusa T, Miyazaki A, Miyagawa J, Yamagata K, Yamamoto K, Waguri M, Imagawa A, Tamura S, Inada M, et al: Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest 1993, 92:2313-2322 (Pubitemid 23333537)
14. Katz J, Benoist C, Mathis D: Major histocompatibility complex class I molecules are required for the development of insulitis in non-obese diabetic mice. Eur J Immunol 1993, 23:3358-3360 (Pubitemid 23353790)
15. Serreze DV, Leiter EH, Christianson GJ, Greiner D, Roopenian DC: Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 1994, 43:505-509
16. Sumida T, Furukawa M, Sakamoto A, Namekawa T, Maeda T, Zijlstra M, Iwamoto I, Koike T, Yoshida S, Tomioka H, et al: Prevention of insulitis and diabetes in β 2-microglobulin-deficient non-obese diabetic mice. Int Immunol 1994, 6:1445-1449 (Pubitemid 24296861)
17. Wicker LS, Leiter EH, Todd JA, Renjilian RJ, Peterson E, Fischer PA, Podolin PL, Zijlstra M, Jaenisch R, Peterson LB:β 2-microglobulindeficient NOD mice do not develop insulitis or diabetes. Diabetes 1994, 43:500-504 (Pubitemid 24064260)
18. Hamilton-Williams EE, Palmer SE, Charlton B, Slattery RM: β Cell MHC class I is a late requirement for diabetes. Proc Natl Acad Sci U S A 2003, 100:6688-6693 (Pubitemid 36666642)
19. Yamanouchi J, Verdaguer J, Han B, Amrani A, Serra P, Santamaria P: Cross-priming of diabetogenic T cells dissociated from CTL-induced shedding of β cell autoantigens. J Immunol 2003, 171:6900-6909 (Pubitemid 37532126)
20. + T cell-mediated autoimmune destruction. J Immunol 2004, 172:5714-5721 (Pubitemid 38542076)
21. Krishnamurthy B, Dudek NL, McKenzie MD, Purcell AW, Brooks AG, Gellert S, Colman PG, Harrison LC, Lew AM, Thomas HE, Kay TW: Responses against islet antigens in NOD mice are prevented by tolerance to proinsulin but not IGRP. J Clin Invest 2006, 116:3258-3265 (Pubitemid 44878640)
22. + T cells expressing identical endogenous TCR-α chains. J Immunol 1996, 157:4726-4735 (Pubitemid 126449398)
23. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ: Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994, 76:977-987 (Pubitemid 24106379)
24. Krishnamurthy B, Mariana L, Gellert SA, Colman PG, Harrison LC, Lew AM, Santamaria P, Thomas HE, Kay TW: Autoimmunity to both proinsulin and IGRP is required for diabetes in nonobese diabetic 8.3 TCR transgenic mice. J Immunol 2008, 180:4458-4464
25. Liu M, Shapiro ME: A new method for isolation of murine islets with markedly improved yields. Transplant Proc 1995, 27:3208-3210 (Pubitemid 26016142)
26. Smyth MJ, Kelly JM, Sutton VR, Davis JE, Browne KA, Sayers TJ, Trapani JA: Unlocking the secrets of cytotoxic granule proteins. J Leukoc Biol 2001, 70:18-29 (Pubitemid 32613658)
27. Schwab SR, Cyster JG: Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol 2007, 8:1295-1301 (Pubitemid 350131168)
28. Dudek NL, Thomas HE, Mariana L, Sutherland RM, Allison J, Estella E, Angstetra E, Trapani JA, Santamaria P, Lew AM, Kay TW: Cytotoxic T-cells from T-cell receptor transgenic NOD8.3 mice destroy betacells via the perforin and Fas pathways. Diabetes 2006, 55:2412-2418 (Pubitemid 44871141)
29. Casey KA, Mescher MF: IL-21 promotes differentiation of naive CD8 T cells to a unique effector phenotype. J Immunol 2007, 178:7640-7648 (Pubitemid 46898034)
30. + T cells. J Immunol 2008, 181:3818-3822
31. Feuerer M, Shen Y, Littman DR, Benoist C, Mathis D: How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 2009, 31:654-664
32. Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR: Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 2008, 319:198-202
33. Chen YG, Choisy-Rossi CM, Holl TM, Chapman HD, Besra GS, Porcelli SA, Shaffer DJ, Roopenian D, Wilson SB, Serreze DV: Activated NKT cells inhibit autoimmune diabetes through tolerogenic recruitment of dendritic cells to pancreatic lymph nodes. J Immunol 2005, 174:1196-1204
34. Thomas HE, Parker JL, Schreiber RD, Kay TW: IFN-α action on pancreatic β cells causes class I MHC upregulation but not diabetes. J Clin Invest 1998, 102:1249-1257 (Pubitemid 28436285)
35. Pang S, Zhang L, Wang H, Yi Z, Li L, Gao L, Zhao J, Tisch R, Katz JD, Wang B: CD8(+) T cells specific for β cells encounter their cognate antigens in the islets of NOD mice. Eur J Immunol 2009, 39:2716-2724
36. Lennon GP, Bettini M, Burton AR, Vincent E, Arnold PY, Santamaria P, Vignali DA: T cell islet accumulation in type 1 diabetes is a tightly regulated, cell-autonomous event. Immunity 2009, 31:643-653
37. + T cell inflammation. Proc Natl Acad Sci U S A 107:9317-9322
38. + T cells. J Exp Med 2003, 197:643-656 (Pubitemid 36314659)
39. Agarwal P, Raghavan A, Nandiwada SL, Curtsinger JM, Bohjanen PR, Mueller DL, Mescher MF: Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J Immunol 2009, 183:1695-1704
40. + T cells independently of its effects on survival and proliferation. J Immunol 2005, 175:8003-8010 (Pubitemid 41798362)
41. Li Q, Xu B, Michie SA, Rubins KH, Schreriber RD, McDevitt HO: Interferon-α initiates type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci U S A 2008, 105:12439-12444
42. Poligone B, Weaver DJ Jr., Sen P, Baldwin AS Jr., Tisch R: Elevated NF-kB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J Immunol 2002, 168:188-196 (Pubitemid 34014118)
43. Sen P, Bhattacharyya S, Wallet M, Wong CP, Poligone B, Sen M, Baldwin AS Jr., Tisch R: NF-k B hyperactivation has differential effects on the APC function of nonobese diabetic mouse macrophages. J Immunol 2003, 170:1770-1780 (Pubitemid 36197392)
44. Weaver DJ Jr., Poligone B, Bui T, Abdel-Motal UM, Baldwin AS Jr., Tisch R: Dendritic cells from nonobese diabetic mice exhibit a defect in NF-κ B regulation due to a hyperactive I κ B kinase. J Immunol 2001, 167:1461-1468 (Pubitemid 32703145)
45. King C, Ilic A, Koelsch K, Sarvetnick N: Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 2004, 117:265-277 (Pubitemid 38496245)
46. McGuire HM, Vogelzang A, Hill N, Flodstrom-Tullberg M, Sprent J, King C: Loss of parity between IL-2 and IL-21 in the NOD Idd3 locus. Proc Natl Acad Sci U S A 2009, 106:19438-19443
47. + cytotoxic T-cell survival to enhance type 1 diabetes. Diabetes 2008, 57:909-917
48. Hanninen A, Jalkanen S, Salmi M, Toikkanen S, Nikolakaros G, Simell O: Macrophages, T cell receptor usage, and endothelial cell activation in the pancreas at the onset of insulin-dependent diabetes mellitus. J Clin Invest 1992, 90:1901-1910
49. Wheat W, Kupfer R, Gutches DG, Rayat GR, Beilke J, Scheinman RI, Wegmann DR: Increased NF-κ B activity in B cells and bone marrowderived dendritic cells from NOD mice. Eur J Immunol 2004, 34: 1395-1404 (Pubitemid 39256019)
50. Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, Sgouroudis E, Piccirillo CA, Salomon BL, Bluestone JA: Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008, 28:687-697
51. Penaranda C, Tang Q, Ruddle NH, Bluestone JA: Prevention of diabetes by FTY720-mediated stabilization of peri-islet tertiary lymphoid organs. Diabetes 2010, 59:1461-1468
52. Astorri E, Bombardieri M, Gabba S, Peakman M, Pozzilli P, Pitzalis C: Evolution of ectopic lymphoid neogenesis and in situ autoantibody production in autoimmune nonobese diabetic mice: cellular and molecular characterization of tertiary lymphoid structures in pancreatic islets. J Immunol 2010, 185:3359-3368
53. Foulis AK, Farquharson MA, Meager A: Immunoreactive α-interferon in insulin-secreting β cells in type 1 diabetes mellitus. Lancet 1987, 2:1423-1427 (Pubitemid 18010318)
54. Gaglia JL, Guimaraes AR, Harisinghani M, Turvey SE, Jackson R, Benoist C, Mathis D, Weissleder R: Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest 2011, 121:442-445
55. Huang X, Yuang J, Goddard A, Foulis A, James RF, Lernmark A, Pujol-Borrell R, Rabinovitch A, Somoza N, Stewart TA: Interferon expression in the pancreases of patients with type I diabetes. Diabetes 1995, 44:658-664