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Review

Interactions between B-Lymphocytes and Type 1 NKT Cells in Autoimmune Diabetes

, &
Pages 249-257 | Received 25 Feb 2008, Accepted 28 Mar 2008, Published online: 09 Oct 2008

REFERENCES

  • Acevedo-Suárez C. A., Hulbert C., Woodward E. J., Thomas J. W. Uncoupling of anergy from developmental arrest in anti-insulin B-cells supports the development of autoimmune diabetes. J. Immunol. 2005; 174: 827–833
  • Akashi T., Nagafuchi S., Anzai K., Kondo S., Kitamura D., Wakana S., Ono J., Kikuchi M., Watanabee T. Direct evidence for the contribution of B-cells to progression of insulitis and development of diabetes in non-obese diabetic mice. Int. Immunol. 1997; 9: 1159–1164
  • Alard P., Manirarora J. N., Parnell S. A., Hudkins J. L., Clarck S. L., Kosiewicz M. M. Deficiency in NOD antigen-presenting cell function may be responsible for suboptimal CD4+CD25+ T-cell-mediated regulation and type 1 diabetes development in NOD mice. Diabetes 2006; 55: 2098–2105
  • Amano M., Baumgarth N., Dick M. D., Brossay L., Kronenberg M., Herzenberg L. A., Strober S. CD1 expression defines subsets of follicular and marginal zone B-cells in the spleen: β 2-microglobulin-dependent and independent forms. J. Immunol. 1998; 161: 1710–1717
  • Attavanavich K., Kearney J. F. Marginal zone, but not follicular B-cells, are potent activators of naïve CD4 T-cells. J. Immunol. 2004; 172: 803–811
  • Balazs M., Martin F., Zhou T., Kearney J. Blood dendritic cells interact with splenic marginal zone B-cells to initiate T-independent immune responses. Immunity 2002; 17: 341–352
  • Baxter A. G., Kinder S. J., Hammond K. J. L., Scollay R., Godfrey D. I. Association between αβTCR+CD4−CD8− T-cell deficiency and IDDM in NOD mice. Diabetes 1997; 46: 572–582
  • Baxter A. G., Mandel T. E. Haemolytic anemia in non-obese diabetic mice. Eur. J. Immunol. 1991; 21: 2051–2055
  • Bernard N. F., Ertug F., Margolese H. High incidence of thyroiditis and anti-thyroid antibobies in NOD mice. Diabetes 1992; 41: 40–46
  • Bezbradica J. S., Stanic A. K., Matsuki N., Bour-Jordan H., Bluestone J. A., Thomas J. W., Unutmaz D., Van Kaer L., Joyce S. Distinct roles of dendritic cells and B-cells in Vα14Jα 18 natural T-cell activation in vivo. J. Immunol. 2005; 174: 4696–4705
  • Bonifacio E., Atkinson M., Eisenbarth G., Serreze D., Lee-Chan E., Singh B. International workshop on lessons from animal models for human Type I diabetes: Identification of insulin but not glutamic acid decarboxylase or IA-2 as specific autoantigens of humoral autoimmunity in non obese diabetic mice. Diabetes 2001; 50: 2451–2458
  • Brigl M., Brenner M. B. CD1: Antigen presentation and T-cell function. Annu. Rev. Immunol. 2004; 22: 817–890
  • Brodie G. M., Wallberg M., Santamaria P., Wong F. S., Green E. A. Cells promote intra-islet CD8+ cytotoxic T-lymphocyte survival to enhance Type 1 diabetes. Diabetes 2008, DOI: 10.2337/db07-1256
  • Brodnicki T. C., O'Donnell K., Quirk F., Tarlinton D. M. Congenic non-obese diabetic mouse strains fail to confirm linkage of a marginal zone B-lymphocyte phenotype to the Idd11 locus on Chromosome 4. J. Immunol. 2006; 176: 701–702
  • Burdin N., Brossay L., Kronenberg K. Immunization with α -galactosylceramide polarizes CD1-reactive NK T-cells towards TH2 cytokine synthesis. Eur. J. Immunol. 1999; 29: 2014–2025
  • Cardell S. L. The natural killer T-lymphocyte: A player in the complex regulation of autoimmune diabetes in non-obese diabetic mice. Clin. Exp. Immunol. 2005; 143: 194–202
  • Cardell S, Tangri S, Chan S, Kronenberg M, Benoist C, Mathis D. CD1-restricted CD4+ T-cells in major histocompatibility complex Class II-deficient mice. J. Exp. Med. 1995; 182: 993–1004
  • Carnaud C., Gombert J.-M., Donnars O., Garchon H. J., 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
  • Carrillo J., Puertas M. C., Alba A., Ampudia R. M., Pastor X., Planas R., Riutort N., Alonso N., Pujol-Borrell R., Santamaria P., Vives-Pi M., Verdaguer J. Islet-infiltrating B-cells in non-obese diabetic mice predominantly target nervous system elements. Diabetes 2005; 54: 69–77
  • Chen Y. G., Choisy-Rossy C., Holl T. M., Chapman H. D., Besra G. S., Porcelli S. A., Shaffer D. J., Roopenian D., Wilson S. B., Serreze D. V. Activated NKT cells inhibit autoimmune diabetes through tolerogenic recruitment of dendritic cells to pancreatic lymph nodes. J. Immunol. 2005; 174: 1196–1204
  • Chen Y. G., Driver J. P., Silveira P. A., Serreze D. V. Congenic analysis confirms genes within the Idd13 locus contributes to impaired development of invariant NKT cells in NOD mice. Immunogenetics 2007; 59: 705–712
  • Chen Y. G., Silveira P. A., Osborne M. A., Chapman H. D., Serreze D. V. Cellular expression requirements for inhibition of Type 1 diabetes by a dominantly protective MHC haplotype. Diabetes 2007; 56: 424–430
  • Chiu P. P., Jevnikar A. M., Danska J. S. Genetic control of T- and B-lymphocyte activation in nonobese diabetic mice. J. Immunol. 2001; 167: 7169–7179
  • Chiu P. P., Serreze D. V., Danska J. S. Development and function of diabetogenic T-cells in B-cell-deficient nonobese diabetic mice. Diabetes 2001; 50: 763–770
  • Chung B., Aoukaty A., Dutz J., Terhorst C., Tan R. Signaling lymphocytic activation molecule-associated protein controls NKT cell functions. J. Immunol. 2005; 174: 3153–3157
  • Cinamon G., Zachariah M. A., Lam O. M., Foss F. W., Jr, Cyster J. G. Follicular shuttling of marginal zone B-cells facilitates antigen transport. Nat. Immunol. 2008; 9: 54–62
  • Constant S., Schweitzer N., West J., Ranney P., Bottomly K. B-Lymphocytes can be competent antigen-presenting cells for priming CD4+ T-cells to protein antigens in vivo. J. Immunol. 1995; 155: 3734–3741
  • Crowe N. Y., Uldrich A. P., Kyparissoudis K., Hammond K. J. L., Hayakawa Y., Sidobre S., Keating R., Kronenberg M., Smyth M. J., Godfrey D. I. Glycolipid antigen drives rapid expansion and sustained cytokine production by NK T-cells. J. Immunol. 2003; 171: 4020–4027
  • Dellabona P., Padovan E., Casorati M., Brockhaus M., Lanzavecchia A. An invariant Vα24-Jα Q/Vβ 11 T-cell receptor is expressed in all individuals by clonally expanded CD4−8− T-cells. J. Exp. Med. 1994; 180: 1171–1176
  • Dobersen M. J., Scharff J. E., Ginsberg-Fellner F., Notkins A. L. Cytotoxic autoantibodies to β cells in the serum of patients with insulin-dependent diabetes mellitus. New Engl. J. Med. 1980; 303: 1493–1498
  • Eisenbarth G. S., Morris M. A., Scearce R. M. Cytotoxic antibodies to cloned rat islet cells in serum of patients with diabetes mellitus. J. Clin. Invest. 1981; 67: 403–408
  • Esteban L. M., Tsoutsman T., Jordan M. A., Roach D., Poulton L. D., Brooks A., Naidenko O. V., Sidobre S., Godfrey D. I., Baxter A. G. Genetic control of NKT cell number maps to major diabetes and lupus loci. J. Immunol. 2003; 171: 2873–2878
  • Falcone M., Facciotti F., Ghidoli N., Monti P., Olivieri S., Zaccagnino L., Bonifacio E., Casorati G., Sanvito F., Sarvetnick N. Up-regulation of CD1d expression restores the immunoregulatory function of NKT cells and prevents autoimmune diabetes in non-obese diabetic mice. J. Immunol. 2004; 172: 5908–5916
  • Falcone M., Lee J., Patstone G., Yeung B., Sarvetnick N. B lymphocytes are crucial antigen-presenting cells in the pathogenic autoimmune response to GAD65 antigen in nonobese diabetic mice. J. Immunol. 1998; 161: 1163–1168
  • Feuerer M., Jiang W., Holler P. D., Satpathy A., Campbell C., Bogue M., Mathis D., Benoist C. Enhanced thymic selection of FoxP3+ regulatory T-cells in the NOD mouse model of autoimmune diabetes diabetes. Proc. Natl. Acad. Sci. USA 2007; 104: 18181–18186
  • Forsgren S., Andersson A., Hillorn V., Soderstrom A., Holmberg D. Immunoglobulin-mediated prevention of autoimmune diabetes in the non-obese diabetic (NOD) mouse. Scand. J. Immunol. 1991; 34: 445–451
  • Fowlkes B. J., Kruisbick A. M., Ton That H., Weston M. A., Coligan J. E., Schwartz R. H., Pardol D. M. A novel population of T-cell receptor α β bearing thymocytes which predominantly expresses a single Vα gene family. Nature 1987; 329: 251–254
  • Fox C. J., Danska J. S. Independent genetic regulation of T-cell and antigen-presenting cell participation in autoimmune islet inflammation. Diabetes 1998; 47: 331–338
  • Galli G., Nuti S., Tavarini S., Galli-Stampino L., De Lalla C., Casorati G., Dellabona P., Abrignani S. CD1d-restricted help to B-cells by human invariant natural killer T-lymphocytes. J. Exp. Med. 2003; 197: 1051–1057
  • Galli G., Pittoni P., Tonti E., Malzone C., Uematsu Y., Tortoli M., Maione D., Volpini G., Finco O., Nuti S., Tavarini S., Dellabona P., Rappuoli R., Casorati G., Abrignani S. Invariant NKT cells sustain specific B-cell responses and memory. Proc. Natl. Acad. Sci. USA 2007; 104: 3984–3989
  • Godfrey D. I., Berzins S. P. Control points in NKT cell development. Nat. Rev. Immunol. 2007; 7: 505–518
  • Godfrey D. I., Hammond K. J., Poulton L. D., Smyth M. J., Baxter A. G. NKT cells: Facts, functions and fallacies. Immunol. Today 2000; 21: 573–583
  • Godfrey D. I., Kinder S. J., Silveira P., Baxter A. G. Flow cytometric study of T-cell development in NOD mice reveals a deficiency in αβ TCR+CD4−CD8− thymocytes. J. Autoimmunity 1997; 10: 279–285
  • Godfrey D. I., Kronenberg M. Going both ways: Immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 2004; 114: 1379–1388
  • Godfrey D. I., MacDonald H. R., Kronenberg M., Smyth M. J., Van Kaer L. NKT cells: What's in a name?. Nat. Rev. Immunol. 2004; 4: 231–237
  • Gombert J. M., Herbelin A., Tancrede-Bohin E., Dy M., Carnaud C., Bach J. F. Early quantitative and functional deficiency of NK1+-like thymocytes in the NOD mouse. Eur. J. Immunol. 1996; 26: 2989–2998
  • Gray D., McConnell I., Kumararatne D. S., MacLennan I. C., Humphrey J. H., Bazin H. Marginal zone B-cells express CR1 and CR2 receptors. Eur. J. Immunol. 1984; 14: 47–52
  • Greeley S. A. W., Katsumata M., Yu L., Eisenbarth G. S., Moore D. J., Goodarzi H., Barker C. F., Naji A., Noorchasm H. Elimination of maternally-transmitted autoantibodies prevents diabetes in non-obese diabetic mice. Nat. Med. 2002; 8: 399–402
  • Griewank K., Borowski C., Rietdijk S., Wang N., Julien A., Wei D. G., Mamchak A. A., Terhorst C., Bendelac A. Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 2007; 27: 751–762
  • Hammond K. J., Pellicci D. G., Poulton L. D., Naidenklo O. V., Scalzo A. A., Baxter A. G., Godfrey D. I. CD1d-restricted NKT cells: An interstrain comparison. J. Immunol. 2001; 167: 1164–1173
  • Hammond K. J., Poulton L. D., Palmisano L. J., Silveira P. A., Godfrey D. I., Baxter A. G. α/β -T cell receptor (TCR)+CD4−CD8− (NKT) thymocytes prevent insulin-dependent diabetes mellitus in non-obese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J. Exp. Med. 1998; 187: 1047–1056
  • Hong S., Wilson M. T., Serizawa I., Wu L., Singh N., Naidenko O., Miura T., Haba T., Scherer D. C., Wei J., Kronenberg M., Koezuka Y., Van Kaer L. The natural killer T-cell ligand α -galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat. Med. 2001; 7: 1052–1056
  • Hu C. Y., Rodriguez-Pinto D., Du W., Ahuja A., Henegariu O., Wong F. S., Shlomchik M. J., Wen L. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 2007; 117: 3857–3867
  • Hussain S., Delovitch T. L. Dysregulated B7-1 and B7-2 expression on nonobese diabetic mouse B-cells is associated with increased T-cell co-stimulation and the development of insulitis. J. Immunol. 2005; 174: 680–687
  • Inoue Y., Kaifu T., Sugahara-Tobinai A., Nakamura A., Miyazaki J., Takai T. Activating Fcγ receptors participate in the development of autoimmune diabetes in NOD mice. J. Immunol. 2007; 179: 764–774
  • Jarpe A., Hickman M., Anderson J., Winter W., Peck A. Flow cytometric enumeration of mononuclear cell populations infiltrating the Islets of Langerhans in pre-diabetic NOD mice: development of a model of autoimmune insulitis for Type I diabetes. Regul. Immunol. 1991; 3: 305–317
  • Johnson E. A., Silveira P., Chapman H. D., Leiter E. H., Serreze D. V. Inhibition of autoimmune diabetes in non-obese diabetic mice by transgenic restoration of H2-E MHC Class II expression: Additive, but unequal, involvement of multiple APC subtypes. J. Immunol. 2001; 167: 2404–2410
  • Jordan M. A., Fletcher J. M., Pellicci D., Baxter A. G. Slamf1, the NKT cell control gene Nkt1. J. Immunol. 2007; 178: 1618–1627
  • Kanatsuna T., Lernmark A., Rubenstein A. H., Steiner D. F. Block in insulin release from column-perfused pancreatic β cells induced by islet cell surface antibodies and complement. Diabetes 1981; 30: 231–234
  • Kendall P. L., Yu G., Woodward E. J., Thomas J. W. Tertiary lymphoid structures in the pancreas promote selection of B-lymphocytes in autoimmune diabetes. J Immunol. 2007; 178: 5643–5645
  • Kitamura D., Rajewsky K. Targeted disruption of μ chain membrane exon causes loss of heavy-chain allelic exclusion. Nature 1992; 356: 154–156
  • Kronenberg M., Gapin L. The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2002; 2: 557–568
  • Kumar K. R., Li L., Yan M., Bhaskarabhatla M., Mobley A. B., Nguyen C., Mooney J. M., Schatzle J. D., Wakel E. K., Mohan C. Regulation of B-cell tolerance by the lupus susceptibility gene Ly108. Science 2006; 312: 1665–1669
  • Laloux V., Beaudoin L., Jeske D., Carnaud C., Lehuen A. NK T-cell-induced protection against diabetes in Vα 14-Jα 281 transgenic non-obese diabetic mice is associated with a TH2 shift circumscribed regionally to the islets and functionally to islets autoantigens. J. Immunol. 2001; 166: 3749–3756
  • Laloux V., Beaudoin L., Ronet C., Lehuen A. Phenotypic and functional differences between NKT cells colonizing splanchic and peripheral lymph nodes. J. Immunol. 2002; 168: 3251–3258
  • Lang G. A., Devera T. S., Lang M. L. Requirement for CD1d expression by B-cells to stimulate NKT cell enhanced antibody production. Blood 2008; 111: 2158–2162
  • Lang G. A., Illarionov P. A., Glatman-Freedman A., Besra G. S., Lang M. L. BCR targeting of biotin-galactosylceramide leads to enhanced presentation on CD1d and requires transport of BCR to CD1d-containing endocytic compartments. Int. Immunol. 2005; 17: 899–908
  • Lantz O., Bendelac A. An invariant T-cell receptor 〈 chain is used by a unique subset of major histocompatibility complex Class I-specific CD4+ and CD4−8− in mice and humans. J. Exp. Med. 1994; 180: 1097–1106
  • Lehuen A., Lantz O., Beaudoin L., Laloux V., Carnaud C., Bendelac A., Bach J. F., Monteiro R. C. Over-expression of natural killer T-cells protects Vα 14-Jα 281 transgenic non-obese diabetic mice against diabetes. J. Exp. Med. 1998; 188: 1831–1839
  • Linsen L., Somers V., Stinissen P. Immunoregulation of autoimmunity by natural killer T-cells. Hum. Immunol. 2005; 66: 1193–1202
  • Mariño E., Batten M., Groom J., Silveira P., Walters S., Liuwantara D., Mackay F., Grey S. Temporal depletion of B-cells, by selectively targeting BAFF, prevents diabetes in NOD mice. Tissue Antigens 2005; 66: 488
  • Mariño E., Batten M., Groom J., Walters S., Liuwantara D., Mackay F., Grey S. T. Marginal-zone B-cells of non-obese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes 2008; 57: 395–404
  • Matsuki N., Stanic A. K., Embers M. E., Van Kaer L., Morel L., Joyce S. Genetic dissection of Vα 14Jα 18 natural T-cell number and function in autoimmune-prone mice. J. Immunol. 2003; 170: 5429–5437
  • Mi Q. S., Ly D., Zucker P., McGarry M., Delovitch T. L. 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
  • Miao D., Yu L., Eisenbarth G. S. Role of autoantibodies in Type 1 diabetes. Front. Biosci. 2007; 12: 1889–1898
  • Naumov Y. N., Bahjat K. S., Gausling R., Abraham R., Exley M. A., Koezuka Y., Balk S. B., Strominger J. L., Clare-Salzer M., Wilson S. B. Activation of CD1d-restricted T-cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc. Natl. Acad. Sci. USA 2001; 98: 13838–13843
  • Nichols K. E., Hom J., Gong S. Y., Ganguly A., Ma C. S., Cannons J. L., Tangye S. G., Schwartzberg P. L., Koretzky G. A., Stein P. L. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 2005; 11: 340–345
  • Noorchashm H., Lieu Y. K., Noorchashm N., Rostami S. Y., Greeley S. A., Schlachterman A., Song H. K., Noto L. E., Jevnikar A. M., Barker C. F., Naji A. I-Ag7-mediated antigen presentation by B-lymphocytes is critical in overcoming a checkpoint in T-cell tolerance to islet beta cells of non-obese diabetic mice. J. Immunol. 1999; 163: 743–750
  • Noorchashm H., Moore D. J., Lieu Y. K., Noorchashm N., Schlachterman A., Song H. K., Barker C. F., Naji A. Contribution of the innate immune system to autoimmune diabetes: A role for the CR1/CR2 complement receptors. Cell. Immunol. 1999; 195: 75–79
  • Noorchashm H., Noorchashm N., Kern J., Rostami S. Y., Barker C. F., Naji A. B-Cells are required for the initiation of insulitis and sialitis in non-obese diabetic mice. Diabetes 1997; 46: 941–946
  • Pasquier B., Yin L., Fondaneche M. C., Relouzat F., Bloch-Queyrat C., Lambert N., Fischer A., de Saint-Basile G., Latour S. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J. Exp. Med. 2005; 201: 695–701
  • Pellicci D. G., Hammond K. J., Uldrich A. P., Baxter A. G., Smyth M. J., Godfrey D. I. A natural killer T (NKT) cell developmental pathway involving a thymus-dependent NK1.1-CD4+ CD1d- dependent precursor stage. J. Exp. Med. 2002; 195: 835–844
  • Porcelli S. A., Modlin R. L. The CD1 system: Antigen-presenting molecules for T-cell recognition of lipids and glycolipids. Annu. Rev. Immunol. 1999; 17: 297–329
  • Poulton L. D., Smyth M. J., Hawke C. G., Silveira P., Shepherd D., Naidenko O. V., Godfrey D. I., Baxter A. G. Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice. Int. Immunol. 2001; 13: 887–896
  • Roark J. H., Park S. H., Jayawardena J., Kavita U., Shannon M., Bendelac A. CD1.1 expression by mouse antigen-presenting cells and marginal zone B-cells. J Immunol. 1998; 160: 3121–3127
  • Rocha-Campos A. C., Melki R., Zhu R., Deruytter N., Damotte D., Dy M., Herbelin A., Garchon H. J. Genetic and functional analysis of the Nkt1 locus using congenic NOD mice: Improved Vα 14-NKT cell performance but failure to protect against diabetes. Diabetes 2006; 55: 1163–1170
  • Rolf J., Motta V., Duarte N., Lundholm M., Berntman E., Bergman M. L., Sorokin L., Cardell S. L., Holmberg D. The enlarged population of marginal zone/CD1dhigh B-lymphocytes in non-obese diabetic mice maps to diabetes susceptibility region Idd11. J. Immunol. 2005; 174: 4821–4827
  • Salomon B., Lenschow D. J., Rhee L., Ashourian N., Singh B., Sharpe A., Bluestone J. A. B7/CD28 co-stimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T-cells that control autoimmune diabetes. Immunity 2000; 12: 431–440
  • Savino W., Boitard C., Bach J. F., Dardenne M. Studies on the thymus in non-obese diabetic mouse: Changes in the microenvironmental compartments. Lab. Invest. 1991; 64: 405–417
  • Serreze D. V., Chapman H. D., Varnum D. S., Hanson M. S., Reifnyder P. C., Richard S. D., Fleming S. A., Leiter E. H., Shultz L. D. B-Lymphocytes are essential for the initiation of T-cell-mediated autoimmune diabetes: Analysis of a new speed congenic stock of NOD.Igμnull mice. J. Exp. Med. 1996; 184: 2049–2053
  • Serreze D. V., Fleming S. A., Chapman H. D., Richard S. D., Leiter E. H., Tisch R. M. B lymphocytes are critical antigen-presenting cells for the initiation of T-cell-mediated autoimmune diabetes in non-obese diabetic mice. J. Immunol. 1998; 161: 3912–3918
  • Sharif S., Arreaza G. A., Zucker P., Mi Q. S., Sondhi J., Naidenko O. V., Kronenberg M., Koezuka Y., Delovitch T. L., Gombert J. M., Leite-De-Moraes M., Gouarin C., Zhu R., Hameg A., Nakayama T., Taniguchi M., Lepault F., Lehuen A, Bach J. F., Herbelin A. Activation of natural killer T-cells by α -galactosylceramide treatment prevents the onset and recurrence of autoimmune Type 1 diabetes. Nat. Med. 2001; 7: 1057–1062
  • Shi F. D., Flodstrom M., Balasa B., Kim S. H., Van Gunst K., Strominger J. L., Wilson S. B., Sarvetnick N. Germ line deletion of the CD1d locus exacerbates diabetes in the NOD mouse. Proc. Natl. Acad. Sci. USA 2001; 98: 6777–6782
  • Shimosaka A. Role of NKT cells and alpha-galactosyl ceramide. Int. J. Hematol. 2002; 76: 277–279
  • Shortman K., Liu Y. J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2002; 2: 151–161
  • Silveira P. A., Baxter A. G. The NOD mouse as a model of SLE. Autoimmunity 2001; 34: 53–64
  • Silveira P. A., Chapman H. D., Stolp J., Johnson E., Cox S. L., Hunter K., Wicker L. S., Serreze D. V. Genes within the Idd5 and Idd9/11 diabetes susceptibility loci affect the pathogenic activity of B-cells in NOD mice. J. Immunol. 2006; 177: 7033–7041
  • Silveira P. A., Dombrowsky J., Johnson E., Chapman H. D., Nemazee D., Serreze D. V. B-Cell selection defects underlie the development of diabetogenic APC in non-obese diabetic mice. J. Immunol. 2004; 172: 5086–5094
  • Silveira P. A., Grey S. T. B-Cells in the spotlight: Innocent bystanders or major players in the pathogenesis of Type 1 diabetes. Trends Endocrinol. Metab. 2006; 17: 128–135
  • Silveira P. A., Johnson E., Chapman H. D., Bui T., Tisch R. M., Serreze D. V. The preferential ability of B-lymphocytes to act as diabetogenic APC in NOD mice depends on expression of self antigen-specific immunoglobulin receptors. Eur. J. Immunol. 2002; 32: 3657–3666
  • Singh N., Hong S., Scherer D. C., Serizawa I., Burdin N., Kronenberg M., Koezuka Y., Van Kaer L. Cutting edge: Activation of NK T-cells by CD1d and α-galactosylceramide directs conventional T-cells to the acquisition of a TH2 phenotype. J. Immunol. 1999; 163: 2373–2377
  • Sköld M., Behar S. M. Role of CD1d-restricted NKT cells in microbial immunity. Infect. Immun. 2003; 71: 5447–5455
  • Sköld M., Stenstrom M., Sidobre S., Hoglund P., Kronenberg M., Cardell S. MWC-dependent and -independent modulation of endogenous Ly49 receptors on NK1.1+ T-lymphocytes directed by T-cell receptor type. Immunology 2003; 110: 313–321
  • Smyth M. J., Crowe N. Y., Hayakawa Y., Takeda K., Yagita H., Godfrey D. I. NKT cells - conductors of tumor immunity?. Curr. Opin. Immunol. 2002; 14: 165–171
  • Sonoda K. H., Stein-Streinlein J. CD1d on antigen-transporting APC and splenic marginal zone B-cells promotes NKT cell-dependent tolerance. Eur. J. Immunol. 2002; 32: 848–857
  • Takahashi T., Strober S. Natural killer T-cells and innate immune B-cells from lupus-prone NZB/W mice interact to generate IgM and IgG autoantibodies. Eur. J. Immunol. 2008; 38: 156–165
  • Tian J., Zekzer D., Lu Y., Dang H., Kaufman D. L. B-Cells are crucial for determinant spreading of T-cell autoimmunity among β cell antigens in diabetes-prone non-obese diabetic mice. J. Immunol. 2006; 176: 2654–2661
  • Unternaehrer J. J., Chow A., Pypaert M., Inaba K., Mellman I. The tetraspanin CD9 mediates lateral association of MHC Class II molecules on the dendritic cell surface. Proc. Natl. Acad. Sci USA 2007; 104: 234–239
  • Vasquez A. C., Feili-Hariri M, Tan R. J., Morel P. A. Qualitative and quantitative abnormalities in splenic dendritic cell populations in NOD mice. Clin. Exp. Immunol. 2004; 135: 209–218
  • Waldschmidt T. J., Kroese F. G., Tygrett L. T., Conrad D. H., Lynch R. G. The expression of B-cell surface receptors. III. The murine low-affinity IgE Fc receptor is not expressed on Ly 1 or ‘Ly 1-like’ B-cells. Int. Immunol. 1991; 3: 305–315
  • Wheat W., Kupfer R., Gutches D. G., Rayat G. R., Beilke J., Scheinman R. I., Wegmann D. R. Increased NF-κ B activity in B-cells and bone marrow-derived dendritic cells from NOD mice. Eur J Immunol 2004; 34: 1395–1404
  • Won W. J., Kearney J. F. CD9 is a unique marker for marginal zone B-cells, B1 cells, and plasma cells in mice. J. Immunol. 2002; 168: 5605–5611
  • Wong F. S., Visintin I., Wen L., Granata J., Flavell R., Janeway C. A. The role of lymphocyte subsets in accelerated diabetes in non-obese diabetic-rat insulin promoter-B7-1 (NOD-RIP-B7-1) mice. J. Exp. Med. 1998; 187: 1985–1993
  • Wong F. S., Wen L. B-Cells in autoimmune diabetes. Rev. Diabetic Stud. 2005; 2: 121–135
  • Wong S., Guerder S., Visintin I., Reich E. P., Swenson K. E., Flavell R. A., Janeway C. A. Expression of the co-stimulator molecule B7-1 in pancreatic β cells accelerates diabetes in the NOD mouse. Diabetes 1995; 44: 326–329
  • Wu A. J., Hua H., Munson S. H., McDevitt H. O. Tumor necrosis factor-α regulation of CD4+CD25+ T-cell levels in NOD mice. Proc. Natl. Acad. Sci. USA 2002; 99: 12287–12292
  • Yang M., Charlton B., Gautam A. M. Development of insulitis and diabetes in B-cell-deficient NOD mice. J. Autoimmun. 1997; 10: 257–260
  • Yoshimoto T., Bendelac A., Watson C., Hu-Li J., Paul W. E. Role of NK1.1+ T-cells in a TH2 response and in immunoglobin E production. Sciences 1995; 270: 1845–1847
  • Yu L., Eisenbarth G. S. Humoral autoimmunity. Immunology of Type I Diabetes, 2nd Edition, G. S. Eisenbarth. Landes Bioscience, Austin, TX 2004; 247–260
  • Zeng D., Liu Y., Sidobre S., Kronenberg M., Strober S. Activation of natural killer T-cells in NZB/W mice induces TH1-type immune responses exacerbating lupus. J. Clin. Invest. 2005; 112: 1211–1222

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