Immunoregulatory natural killer cells suppress autoimmunity by down-regulating antigen-specific CD8 + T cells in mice

Endocrinology

Volumn 153, Issue 9, 2012, Pages 4367-4379

  Ehlers, Margret ^a   Papewalis, Claudia ^c   Stenzel, Wiebke ^a   Jacobs, Benedikt ^d   Meyer, Klaus L ^b   Deenen, René ^b   Willenberg, Holger S ^a   Schinner, Sven ^a   Thiel, Annette ^a   Scherbaum, Werner A ^a   Ullrich, Evelyn ^d   Zitvogel, Laurence ^e   Schott, Matthias ^a  

^a UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL BONN   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 18; PROGRAMMED DEATH 1 LIGAND 1; STEM CELL FACTOR RECEPTOR; STREPTOZOCIN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE SEVERITY; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNOREGULATION; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE FUNCTION; LYSIS; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOCIN DIABETES;

ANIMALS; ANTIGENS, CD8; APOPTOSIS; AUTOIMMUNITY; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; FLOW CYTOMETRY; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICROSCOPY, FLUORESCENCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84865409435     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1247     Document Type: Article

References (57)

1. Colucci F, Caligiuri MA, Di Santo JP 2003 What does it take to make a natural killer? Nat Rev Immunol 3:413-425 (Pubitemid 37323201)
2. Tak PP, Kummer JA, Hack CE, Daha MR, Smeets TJ, Erkelens GW, Meinders AE, Kluin PM, Breedveld FC 1994 Granzyme-positive cytotoxic cells are specifically increased in early rheumatoid synovial tissue. Arthritis Rheum 37:1735-1743 (Pubitemid 24371874)
3. Dalakas MC, Illa I 1995 Common variable immunodeficiency and inclusion body myositis: a distinct myopathy mediated by natural killer cells. Ann Neurol 37:806-810
4. Garcia-Suarez J, Prieto A, Reyes E, Arribalzaga K, Perez-Machado MA, Lopez-Rubio M, Manzano L, Alvarez-Mon M 1995. Persistent lymphocytosis of natural killer cells in autoimmune thrombocytopenic purpura (ATP) patients after splenectomy. Br J Haematol 89:653-655
5. Korsgren M, Persson CG, Sundler F, Bjerke T, Hansson T, Chambers BJ, Hong S, Van Kaer L, Ljunggren HG, Korsgren O 1999 Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J Exp Med 189:553-562 (Pubitemid 29187377)
6. Fort MM, Leach MW, Rennick DM 1998 A role for NK cells as regulators of CD4+ T cells in a transfer model of colitis. J Immunol 161:3256-3261
7. Matsumoto Y, Kohyama K, Aikawa Y, Shin T, Kawazoe Y, Suzuki Y, Tanuma N 1998 Role of natural killer cells and TCRγδ T cells in acute autoimmune encephalomyelitis. Eur J Immunol 28:1681-1688 (Pubitemid 28221173)
8. Shi FD, Wang HB, Li H, Hong S, Taniguchi M, Link H, Van Kaer L, Ljunggren HG 2000 Natural killer cells determine the outcome of B cell-mediated autoimmunity. Nat Immunol 1:245-251
9. Flodström M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N 2002 Target cell defense prevents the development of diabetes after viral infection. Nat Immunol 3:373-382 (Pubitemid 34308626)
10. Poirot L, Benoist C, Mathis D 2004 Natural killer cells distinguish innocuous and destructive forms of pancreatic islet autoimmunity. Proc Natl Acad Sci USA 101:8102-8107 (Pubitemid 38698061)
11. Lee IF, Qin H, Trudeau J, Dutz J, Tan R 2004 Regulation of autoimmune diabetes by complete Freund's adjuvant is mediated by NK cells. J Immunol 172:937-942 (Pubitemid 38113752)
12. Zhang C, Zhang J, Tian Z 2006 The regulatory effect of natural killer cells: do "NK-reg cells" exist? Cell Mol Immunol 3:241-254
13. Ebata K, Shimizu Y, Nakayama Y, Minemura M, Murakami J, Kato T, Yasumura S, Takahara T, Sugiyama T, Saito S 2006 Immature NK cells suppress dendritic cell functions during the development of leukemia in a mouse model. J Immunol 176:4113-4124 (Pubitemid 44264390)
14. Colucci F, Di Santo JP 2000 The receptor tyrosine kinase c-kit provides a critical signal for survival, expansion, and maturation of mouse natural killer cells. Blood 95:984-991 (Pubitemid 30062722)
15. Mazodier K, Marin V, Novick D, Farnarier C, Robitail S, Schleinitz N, Veit V, Paul P, Rubinstein M, Dinarello CA, Harlé JR, KaplanskiG 2005 Severe imbalance of IL-18/IL-18BP in patients with secondary hemophagocytic syndrome. Blood 106:3483-3489 (Pubitemid 41609184)
16. Ruth JH, Park CC, Amin MA, Lesch C, Marotte H, Shahrara S, Koch AE 2010 Interleukin-18 as an in vivo mediator of monocyte recruitment in rodent models of rheumatoid arthritis. Arthritis Res Ther 12:R118
17. Sánchez E, Palomino-Morales RJ, Ortego-Centeno N, Jiménez- Alonso J, González-Gay MA, López-Nevot MA, Sánchez- Román J, de Ramón E, González-Escribano MF, Pons-Estel BA, D'Alfonso S, Sebastiani GD, Alarcón-Riquelme ME, Martín J 2009 Identification of a new putative functional IL18 gene variant through an association study in systemic lupus erythematosus. Hum Mol Genet 18:3739-3748
18. Shibatomi K, Ida H, Yamasaki S, Nakashima T, Origuchi T, Kawakami A, Migita K, Kawabe Y, Tsujihata M, Anderson P, Eguchi K 2001 A novel role for interleukin-18 in human natural killer cell death: high serum levels and low natural killer cell numbers in patients with systemic autoimmune diseases. Arthritis Rheum 44:884-892 (Pubitemid 32319781)
19. Tucci M, Stucci S, Strippoli S, Silvestris F 2010 Cytokine overproduction, T-cell activation, and defective T-regulatory functions promote nephritis in systemic lupus erythematosus. J Biomed Biotechnol 2010:457146
20. Ullrich E, Terme M, Aymeric L, Apetoh L, Chaput N, Ryffel B, Mackensen A, Schultze JL, Zitvogel L 2008 IL-18 elicited suppressor NK cells with immunoregulatory functions. American Society of Hematology, 6-9 Dec, 2008, San Francisco, CA. (Abstract no. 106)
21. Bellmann K, Wenz A, Radons J, Burkart V, Kleemann R, Kolb H 1995 Heat shock induces resistance in rat pancreatic islet cells against nitric oxide, oxygen radicals and streptozotocin toxicity in vitro. J Clin Invest 95:2840-2845
22. Papewalis C, Wuttke M, Seissler J, Meyer Y, Kessler C, Jacobs B, Ullrich E, Willenberg HS, Schinner S, Baehring T, Scherbaum WA, Schott M 2008 Dendritic cell vaccination with xenogenic polypeptide hormone induces tumor rejection in neuroendocrine cancer. Clin Cancer Res 14:4298-4305
23. Ohly P, Dohle C, Abel J, Seissler J, Gleichmann H 2000 Zinc sulphate induces metallothionein in pancreatic islets of mice and protects against diabetes induced by multiple low doses of streptozotocin. Diabetologia 43:1020-1030 (Pubitemid 30655722)
24. Lu WT, Juang JH, Hsu BR, Huang HS 1998 Effects of high or low dose of streptozocin on pancreatic islets in C57BL/6 and C.B17-SCID mice. Transplant Proc 30:609-610
25. Schott-Ohly P, Lgssiar A, Partke HJ, Hassan M, Friesen N, Gleichmann H 2004 Prevention of spontaneous and experimentally induced diabetes in mice with zinc sulfate-enriched drinking water is associated with activation and reduction of NF-κB and AP-1 in islets, respectively. Exp Biol Med 229:1177
26. Saudemont A, Jouy N, Hetuin D, Quesnel B 2005 NK cells that are activated by CXCL10 can kill dormant tumor cells that resist CTL-mediated lysis and can express B7-H1 that stimulates T cells. Blood 105:2428-2435 (Pubitemid 40387042)
27. Schnickel GT, Hsieh GR, Kachikwu EL, Garcia C, Shefizadeh A, Fishbein MC, Ardehali A 2006 Cytoprotective gene HO-1 and chronic rejection in heart transplantation. Transplant Proc 38:3259-3262 (Pubitemid 44908532)
28. Ansari MJ, Salama AD, Chitnis T, Smith RN, Yagita H, Akiba H, Yamazaki T, Azuma M, Iwai H, Khoury SJ, Auchincloss Jr H, Sayegh MH 2003. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic(NOD)mice. JExp Med 198:63-69 (Pubitemid 36870186)
29. Koike J, Wakao H, Ishizuka Y, Sato TA, Hamaoki M, Seino K, Koseki H, Nakayama T, Taniguchi M 2004 Bone marrow allograft rejection mediated by a novel murine NK receptor, NKG2I. J Exp Med 199:137-144
30. Waggoner SN, Taniguchi RT, Mathew PA, Kumar V, Welsh RM 2010 Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J Clin Invest 120:1925-1938
31. Taniguchi RT, Guzior D, Kumar V 2007 2B4 inhibits NK-cell fratricide. Blood 110:2020-2023 (Pubitemid 47443917)
32. Liu D, Meckel T, Long EO 2010 Distinct role of rab27a in granule movement at the plasma membrane and in the cytosol of NK cells. PLoS One 5:e12870
33. Delovitch TL, Singh B 1997 The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7:727-738 (Pubitemid 28064887)
34. Ogasawara K, Hamerman JA, Ehrlich LR, Bour-Jordan H, Santamaria P, Bluestone JA, Lanier LL 2004 NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 20:757-767 (Pubitemid 38757445)
35. Like AA, Rossini AA 1976 Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 193:415-417
36. Lennon GP, Bettini M, Burton AR, Vincent E, Arnold PY, Santamaria P, Vignali DA 2009 T cell islet accumulation in type 1 diabetes is a tightly regulated, cell-autonomous event. Immunity 31:643-653
37. Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P 2007 Coxsackie B4 virus infection of β cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA 104:5115-5120 (Pubitemid 47186185)
38. Alba A, Planas R, Clemente X, Carrillo J, Ampudia R, Puertas MC, Pastor X, Tolosa E, Pujol-Borrell R, Verdaguer J, Vives-Pi M 2008 Natural killer cells are required for accelerated type 1 diabetes driven by interferon-β. Clin Exp Immunol 151:467-475 (Pubitemid 351160730)
39. Brauner H, Elemans M, Lemos S, Broberger C, Holmberg D, Flodström-Tullberg M, Kärre K, Höglund P 2010 Distinct phenotype and function of NK cells in the pancreas of nonobese diabetic mice. J Immunol 184:2272-2280
40. Gur C, Porgador A, Elboim M, Gazit R, Mizrahi S, Stern-Ginossar N, Achdout H, Ghadially H, Dor Y, Nir T, Doviner V, Hershkovitz O, Mendelson M, Naparstek Y, Mandelboim O 2010 The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat Immunol 11:121-128
41. Poulton LD, Smyth MJ, Hawke CG, Silveira P, Shepherd D, Naidenko OV, Godfrey DI, Baxter AG 2001 Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice. Int Immunol 13:887-896 (Pubitemid 32685201)
42. Kataoka S, Satoh J, Fujiya H, Toyota T, Suzuki R, Itoh K, Kumagai K 1983 Immunologic aspects of the nonobese diabetic (NOD) mouse. Abnormalities of cellular immunity. Diabetes 32:247-253 (Pubitemid 13138268)
43. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, Tennent B, McKenna S, Mobraaten L, Rajan TV, Greiner DL 1995. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 154:180-191
44. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, Torigoe K, Okura T, Nukada Y, Hattori K 1995 Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 378:88-91
45. Nakanishi K, Yoshimoto T, Tsutsui H, Okamura H 2001 Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol 19:423-474 (Pubitemid 32368042)
46. Johansson SE, Hall H, Björklund J, Höglund P 2004 Broadly impaired NK cell function in non-obese diabetic mice is partially restored by NK cell activation in vivo and by IL-12/IL-18 in vitro. Int Immunol 16:1-11 (Pubitemid 38054621)
47. Hayakawa Y, Smyth MJ 2006 CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 176:1517-1524 (Pubitemid 43134295)
48. Mebius RE 2003 Organogenesis of lymphoid tissues. Nat Rev Immunol 3:292-303 (Pubitemid 37328682)
49. Kim MY, Rossi S, Withers D, McConnell F, Toellner KM, Gaspal F, Jenkinson E, Anderson G, Lane PJ 2008 Heterogeneity of lymphoid tissue inducer cell populations present in embryonic and adult mouse lymphoid tissues. Immunology 124:166-174 (Pubitemid 351692897)
50. Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II, Littman DR, O'Shea JJ 2009. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206:35-41
51. Kanamori Y, Ishimaru K, Nanno M, Maki K, Ikuta K, Nariuchi H, Ishikawa H 1996 Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lymphohemopoietic progenitors develop. J Exp Med 184:1449-1459 (Pubitemid 26354700)
52. Luci C, Reynders A, Ivanov II, Cognet C, Chiche L, Chasson L, Hardwigsen J, Anguiano E, Banchereau J, Chaussabel D, Dalod M, Littman DR, Vivier E, Tomasello E 2009 Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat Immunol 10:75-82
53. Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, Diefenbach A 2009 RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+cells. Nat Immunol 10:83-91
54. Wang CJ, Chou FC, Chu CH, Wu JC, Lin SH, Chang DM, Sytwu HK 2008 Protective role of programmed death 1 ligand 1 (PD-L1)in nonobese diabetic mice: the paradox in transgenic models. Diabetes 57:1861-1869
55. Fife BT, Bluestone JA 2008 Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev 224:166-182
56. Hong TP, Andersen NA, Nielsen K, Karlsen AE, Fantuzzi G, Eizirik DL, Dinarello CA, Mandrup-Poulsen T 2000 Interleukin-18 mRNA, but not interleukin-18 receptor mRNA, is constitutively expressed in islet β-cells and up-regulated by interferon-γ. Eur Cytokine Netw 11:193-205
57. Terme M, Ullrich E, Aymeric L, Meinhardt K, Coudert J, Desbois M, Ghiringhelli F, Viaud S, Ryffel B, Yagita H, Chen L, Mecheri S, Kaplanski G, Prevost-Blondel A, Kato M, Schultze JL, Tartour E, Kroemer G, gli-Esposti M, Chaput N, Zitvogel L 16 March 2012 Cancer-induced immunosuppression: IL-18-elicited immunoablative NK cells. Cancer Res, 10.1158/0008-5472.CAN-11- 3379