Estrogen therapy delays autoimmune diabetes and promotes the protective efficiency of natural killer T-cell activation in female nonobese diabetic mice

Endocrinology

Volumn 157, Issue 1, 2016, Pages 258-267

  Gourdy, Pierre ^a,b,c   Bourgeois, Elvire A ^d,e   Levescot, Anaïs ^f,g,h   Pham, Linh ^d,e   Riant, Elodie ^a   Ahui, Marie Louise ^d,e   Damotte, Diane ^h   Gombert, Jean Marc ^i,j,k   Bayard, Francis ^a   Ohlsson, Claes ^l   Arnal, Jean François ^a,b   Herbelin, André ^e,f,j,k  

^a Université de Toulouse   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c TOULOUSE UNIVERSITY HOSPITAL   (France)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f INSERM   (France)

^g UNIVERSITÉ PARIS SACLAY   (France)

^h HÔTEL DIEU   (France)

ⁱ Laboratory of Immunology   (France)

^j UNIVERSITÉ DE POITIERS   (France)

^k POITIERS UNIVERSITY HOSPITAL   (France)

^l UNIVERSITY OF GOTHENBURG   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ESTROGEN; GAMMA INTERFERON; INTERLEUKIN 4; LUTEINIZING HORMONE; PLACEBO; ALPHA-GALACTOSYLCERAMIDE; CYTOKINE; DRUG IMPLANT; ESTRADIOL; GALACTOSYLCERAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD25+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESTROGEN BLOOD LEVEL; ESTROGEN THERAPY; FEMALE; FLOW CYTOMETRY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LUTEINIZING HORMONE BLOOD LEVEL; MOUSE; NATURAL KILLER T CELL; NONHUMAN; NONOBESE DIABETIC MOUSE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ADVERSE EFFECTS; AGONISTS; ANIMAL; AUTOIMMUNE DISEASES; BLOOD; C57BL MOUSE; DIABETES MELLITUS, TYPE 1; DRUG EFFECTS; DRUG IMPLANT; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; METABOLISM; MUTANT MOUSE STRAIN; NATURAL KILLER CELL; OVARIECTOMY; PREDIABETIC STATE; SECRETION (PROCESS);

ANIMALS; AUTOIMMUNE DISEASES; CYTOKINES; DIABETES MELLITUS, TYPE 1; DRUG IMPLANTS; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; GALACTOSYLCERAMIDES; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, MUTANT STRAINS; OVARIECTOMY; PREDIABETIC STATE; T-LYMPHOCYTES, REGULATORY;

EID: 84954548525     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1313     Document Type: Article

References (50)

1. Atkinson MA, Eisenbarth GS, Michels AW. Type 1 diabetes. Lancet. 2013;383:69-82.
2. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-2020: a multicentre prospective registration study. Lancet. 2009;373:2027-2033.
3. Lehuen A, Diana J, Zaccone P, Cooke A. Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol. 2010;10:501-513.
4. Herold KC, Vignali DA, Cooke A, Bluestone JA. Type 1 diabetes: translating mechanistic observations into effective clinical outcomes. Nat Rev Immunol. 2013;13:243-256.
5. Lernmark A, Larsson HE. Immune therapy in type 1 diabetes mellitus. Nat Rev Endocrinol. 2013;9:92-103.
6. Salomon B, Lenschow DJ, Rhee L, et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000;12:431-440.
7. Tang Q, Adams JY, Penaranda C, et al. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity. 2008;28:687-697.
8. Chatenoud L. Immune therapy for type 1 diabetes mellitus-what is unique about anti-CD3 antibodies? Nat Rev Endocrinol. 2010;6:149-157.
9. Simoni Y, Diana J, Ghazarian L, Beaudoin L, Lehuen A. Therapeutic manipulation of natural killer (NK) T cells in autoimmunity: are we close to reality? Clin Exp Immunol. 2013;171:8-19.
10. Berzins SP, Ritchie DS. Natural killer T cells: drivers or passengers in preventing human disease? Nat Rev Immunol. 2014;14:640-646.
11. Carnaud C, Gombert J, Donnars O, Garchon H, Herbelin A. Protection against diabetes and improved NK/NKT cell performance in NOD. NK1.1 mice congenic at the NK complex. J Immunol. 2001;166:2404-2411.
12. Jordan MA, Fletcher JM, Pellicci D, Baxter AG. Slamf1, the NKT cell control gene Nkt1. J Immunol. 2007;178:1618-1627.
13. Oikawa Y, Shimada A, Yamada S, et al. High frequency of valpha24 (β) vbeta11 (β) T-cells observed in type 1 diabetes. Diabetes Care. 2002;25:1818-1823.
14. Hammond KJ, Poulton LD, Palmisano LJ, Silveira PA, Godfrey DI, Baxter AG. β/α-T cell receptor (TCR) +CD4-CD8-(NKT) thymocytes prevent insulin-dependent diabetes mellitus in nonobese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J Exp Med. 1998;187:1047-1056.
15. Lehuen A, Lantz O, Beaudoin L, et al. Overexpression of natural killer T cells protects Vβ14-Jβ281 transgenic nonobese diabetic mice against diabetes. J Exp Med. 1998;188:1831-1839.
16. Sharif S, Arreaza GA, Zucker P, et al. Activation of natural killer T cells by β-galactosylceramide treatment prevents the onset and recurrence of autoimmune type 1 diabetes. Nat Med. 2001;7:1057-1062.
17. Hong S, Wilson MT, Serizawa I, et al. The natural killer T-cell ligand β-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat Med. 2001;7:1052-1056.
18. Luo X, Herold KC, Miller SD. Immunotherapy of type 1 diabetes: where are we and where should we be going? Immunity. 2010;32:488-499.
19. Nilsson S, Koehler KF, Gustafsson JA. Development of subtypeselective oestrogen receptor-based therapeutics. Nat Rev Drug Discov. 2011;10:778-792.
20. Sicotte NL, Liva SM, Klutch R, et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann Neurol. 2002;52:421-428.
21. Soldan SS, Alvarez Retuerto AI, Sicotte NL, Voskuhl RR. Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estriol. J Immunol. 2003;171:6267-6274.
22. Spence RD, Voskuhl RR. Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Front Neuroendocrinol. 2012;33:105-115.
23. Polanczyk MJ, Carson BD, Subramanian S, et al. Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J Immunol. 2004;173:2227-2230.
24. Polanczyk MJ, Hopke C, Huan J, Vandenbark AA, Offner H. Enhanced FoxP3 expression and Treg cell function in pregnant and estrogen-treated mice. J Neuroimmunol. 2005;170:85-92.
25. Arruvito L, Sanz M, Banham AH, Fainboim L. Expansion of CD4+CD25+ and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol. 2007;178:2572-2578.
26. Gourdy P, Araujo LM, Zhu R, et al. Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-γ production by invariant natural killer T cells. Blood. 2005;105:2415-2420.
27. Cui J, Shin T, Kawano T, et al. Requirement for V+14 NKT cells in IL-12-mediated rejection of tumors. Science. 1997;278:1623-1626.
28. Shahinian A, Pfeffer K, Lee KP, et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science. 1993;261:609-612.
29. Nilsson ME, Vandenput L, Tivesten A, et al. Measurement of a comprehensive sex steroid profile in rodent serum by high-sensitive gas chromatography-tandem mass spectrometry. Endocrinology. 2015;156:2492-2502.
30. Bach JF, Bendelac A, Brenner MB, et al. The role of innate immunity in autoimmunity. J Exp Med. 2004;200:1527-1531.
31. Lee TP, Chiang BL. Sex differences in spontaneous versus induced animal models of autoimmunity. Autoimmun Rev. 2012;11:A422-A429.
32. Tooley JE, Herold KC. Biomarkers in type 1 diabetes: application to the clinical trial setting. Curr Opin Endocrinol Diabetes Obes. 2014;21:287-292.
33. Straub RH. The complex role of estrogens in inflammation. Endocr Rev. 2007;28:521-574.
34. Le May C, Chu K, Hu M, et al. Estrogens protect pancreatic α-cells from apoptosis and prevent insulin-deficient diabetes mellitus in mice. Proc Natl Acad Sci USA. 2006;103:9232-9237.
35. Liu S, Kilic G, Meyers MS, et al. Oestrogens improve human pancreatic islet transplantation in a mouse model of insulin deficient diabetes. Diabetologia. 2013;56:370-381.
36. Arnal JF, Lenfant F, Flouriot G, et al. From in vivo gene targeting of oestrogen receptors to optimization of their modulation in menopause. Br J Pharmacol. 2012;165:57-66.
37. Paterni I, Granchi C, Katzenellenbogen JA, Minutolo F. Estrogen receptorsβ (ERβ) and α (ERα): subtype-selective ligands and clinical potential. Steroids. 2014;90 C: 13-29.
38. Mi QS, Ly D, Zucker P, McGarry M, Delovitch TL. Interleukin-4 but not interleukin-10 protects against spontaneous and recurrent type 1 diabetes by activated CD1d-restricted invariant natural killer T-cells. Diabetes. 2004;53:1303-1310.
39. Serreze DV, Chapman HD, Post CM, Johnson EA, Suarez-Pinzon WL, Rabinovitch A. Th1 to Th2 cytokine shifts in nonobese diabetic mice: sometimes an outcome, rather than the cause, of diabetes resistance elicited by immunostimulation. J Immunol. 2001;166:1352-1359.
40. Qin HY, Chaturvedi P, Singh B. In vivo apoptosis of diabetogenic T cells in NOD mice by IFN-γ/TNF-β. Int Immunol. 2004;16:1723-1732.
41. Lee IF, Qin H, Priatel JJ, Tan R. Critical role for IFN-γ in natural killer cell-mediated protection from diabetes. Eur J Immunol. 2008;38:82-89.
42. Naumov YN, Bahjat KS, Gausling R, et al. Activation of CD1drestricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc Natl Acad Sci USA. 2001;98:13838-13843.
43. Ly D, Mi QS, Hussain S, Delovitch TL. Protection from type 1 diabetes by invariant NK T cells requires the activity of CD4+CD25+ regulatory T cells. J Immunol. 2006;177:3695-3704.
44. Beaudoin L, Diana J, Ghazarian L, Simoni Y, Boitard C, Lehuen A. Plasmacytoid dendritic cells license regulatory T cells, upon iNKTcell stimulation, to prevent autoimmune diabetes. Eur J Immunol. 2014;44:1454-1466.
45. Seillet C, Laffont S, Tremollieres F, et al. The TLR-mediated response of plasmacytoid dendritic cells is positively regulated by estradiol in vivo through cell-intrinsic estrogen receptor β signaling. Blood. 2012;119:454-464.
46. Fitzpatrick F, Lepault F, Homo-Delarche F, Bach JF, Dardenne M. Influence of castration, alone or combined with thymectomy, on the development of diabetes in the nonobese diabetic mouse. Endocrinology. 1991;129:1382-1390.
47. Fox HS. Androgen treatment prevents diabetes in nonobese diabetic mice. J Exp Med. 1992;175:1409-1412.
48. Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013;339:1084-1088.
49. Kyvik KO, Nystrom L, Gorus F, et al. The epidemiology of type 1 diabetes mellitus is not the same in young adults as in children. Diabetologia. 2004;47:377-384.
50. Ostman J, Lonnberg G, Arnqvist HJ, et al. Gender differences and temporal variation in the incidence of type 1 diabetes: results of 8012 cases in the nationwide Diabetes Incidence Study in Sweden 1983-2002. J Intern Med. 2008;263:386-394.