482
Views
16
CrossRef citations to date
0
Altmetric
Articles

Selective pharmacological inhibition of phosphoinositide 3-kinase p110delta opposes the progression of autoimmune diabetes in non-obese diabetic (NOD) mice

, , , , , , , & show all
Pages 62-73 | Received 01 Feb 2012, Accepted 15 Sep 2012, Published online: 08 Oct 2012

References

  • Cantor J., Haskins K.. Recruitment and activation of macrophages by pathogenic CD4 T cells in type 1 diabetes: evidence for involvement of CCR8 and CCL1. J. Immunol.. 2007; 179 9: 5760–5767.
  • Thomas H. E., Darwiche R., Corbett J. A., Kay T. W.. Interleukin-1 plus gamma-interferon-induced pancreatic beta-cell dysfunction is mediated by beta-cell nitric oxide production. Diabetes. 2002; 51 2: 311–316.
  • Serreze D. V., Chapman H. D., Varnum D. S., . B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new “speed congenic” stock of NOD.Ig mu null mice. J. Exp. Med.. 1996; 184 5: 2049–2053.
  • Wong F. S., Wen L., Tang M., . Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes. 2004; 53 10: 2581–2587.
  • Tian J., Zekzer D., Lu Y., Dang H., Kaufman D. L.. B cells are crucial for determinant spreading of T cell autoimmunity among beta cell antigens in diabetes-prone nonobese diabetic mice. J. Immunol.. 2006; 176 4: 2654–2661.
  • 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 3: 1163–1168.
  • Marino E., Grey ST S. T.. A new role for an old player: do B cells unleash the self-reactive CD8+ T cell storm necessary for the development of type 1 diabetes?. J. Autoimmun.. 2008; 31 3: 301–305.
  • Noorchashm H., Lieu Y. K., Noorchashm N., . I-Ag7-mediated antigen presentation by B lymphocytes is critical in overcoming a checkpoint in T cell tolerance to islet beta cells of nonobese diabetic mice. J. Immunol.. 1999; 163 2: 743–750.
  • Katz J. D., Wang B., Haskins K., Benoist C., Mathis D.. Following a diabetogenic T cell from genesis through pathogenesis. Cell. 1993; 74 6: 1089–1100.
  • Brodie G. M., Wallberg M., Santamaria P., Wong F. S., Green E. A.. B-cells promote intra-islet CD8+ cytotoxic T-cell survival to enhance type 1 diabetes. Diabetes. 2008; 57 4: 909–917.
  • Duan B., Morel L.. Role of B-1a cells in autoimmunity. Autoimmun. Rev.. 2006; 5 6: 403–408.
  • Pao L. I., Lam K. P., Henderson J. M., . B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity. 2007; 27 1: 35–48.
  • Batten M., Groom J., Cachero T. G., . BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med.. 2000; 192 10: 1453–1466.
  • Marino E., Batten M., Groom J., . Marginal-zone B-cells of nonobese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes. 2008; 57 2: 395–404.
  • Martin F., Kearney J. F.. Marginal-zone B cells. Nat. Rev. Immunol.. 2002; 2 5: 323–335.
  • Martin F., Oliver A. M., Kearney J. F.. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity. 2001; 14 5: 617–629.
  • Lopes-Carvalho T., Kearney J. F.. Development and selection of marginal zone B cells. Immunol. Rev.. 2004; 197:192–205.
  • Ryan G. A., Wang C. J., Chamberlain J. L., . B1 cells promote pancreas infiltration by autoreactive T cells. J. Immunol.. 2010; 185 5: 2800–2807.
  • Noorchashm H., Noorchashm N., Kern J., . B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes. 1997; 46 6: 941–946.
  • Hu C. Y., Rodriguez-Pinto D., Du W., . Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest.. 2007; 117 12: 3857–3867.
  • Xiu Y., Wong C. P., Bouaziz J. D., . B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in Fc gamma R effector functions. J. Immunol.. 2008; 180 5: 2863–2875.
  • Fiorina P., Vergani A., Dada S., . Targeting CD22 reprograms B-cells and reverses autoimmune diabetes. Diabetes. 2008; 57 11: 3013–3024.
  • Zekavat G., Rostami S. Y., Badkerhanian A., . In vivo BLyS/BAFF neutralization ameliorates islet-directed autoimmunity in nonobese diabetic mice. J. Immunol.. 2008; 181 11: 8133–8144.
  • Pescovitz M. D., Greenbaum C. J., Krause-Steinrauf H., . Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med.. 2009; 361 22: 2143–2152.
  • Gong Q., Ou Q., Ye S., . Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J. Immunol.. 2005; 174 2: 817–826.
  • Yu S., Dunn R., Kehry M. R., Braley-Mullen H.. B cell depletion inhibits spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Immunol.. 2008; 180 11: 7706–7713.
  • Okkenhaug K., Vanhaesebroeck B.. PI3K in lymphocyte development, differentiation and activation. Nat. Rev. Immunol.. 2003; 3 4: 317–330.
  • Okkenhaug K., Vanhaesebroeck B.. PI3K-signalling in B- and T-cells: insights from gene-targeted mice. Biochem. Soc. Trans.. 2003; 31 Pt 1: 270–274.
  • Reif K., Okkenhaug K., Sasaki T., . Cutting edge: differential roles for phosphoinositide 3-kinases, p110γ and p110δ, in lymphocyte chemotaxis and homing. J. Immunol.. 2004; 173 4: 2236–2240.
  • Al-Alwan M. M., Okkenhaug K., Vanhaesebroeck B., Hayflick J. S., Marshall A. J.. Requirement for phosphoinositide 3-kinase p110δ signaling in B cell antigen receptor-mediated antigen presentation. J. Immunol.. 2007; 178 4: 2328–2335.
  • Vanhaesebroeck B., Ali K., Bilancio A., Geering B., Foukas L. C.. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem. Sci.. 2005; 30 4: 194–204.
  • Bilancio A., Okkenhaug K., Camps M., . Key role of the p110δ isoform of PI3K in B-cell antigen and IL-4 receptor signaling: comparative analysis of genetic and pharmacologic interference with p110δ function in B cells. Blood. 2006; 107 2: 642–650.
  • Jou S. T., Carpino N., Takahashi Y., . Essential, nonredundant role for the phosphoinositide 3-kinase p110δ in signaling by the B-cell receptor complex. Mol. Cell Biol.. 2002; 22 24: 8580–8591.
  • Clayton E., Bardi G., Bell S. E., . A crucial role for the p110δ subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med.. 2002; 196 6: 753–763.
  • Okkenhaug K., Bilancio A., Farjot G., . Impaired B and T cell antigen receptor signaling in p110δ PI 3-kinase mutant mice. Science. 2002; 297 5583: 1031–1034.
  • Sadhu C., Dick K., Tino W. T., Staunton D. E.. Selective role of PI3Kδ in neutrophil inflammatory responses. Biochem. Biophys. Res. Commun.. 2003; 308 4: 764–769.
  • Sadhu C., Masinovsky B., Dick K., Sowell C. G., Staunton D. E.. Essential role of phosphoinositide 3-kinase delta in neutrophil directional movement. J. Immunol.. 2003; 170 5: 2647–2654.
  • Lannutti B. J., Meadows S. A., Herman S. E., . CAL-101, a p110δ selective phosphatidylinositol-3-kinase inhibitor for the treatment of B-cell malignancies, inhibits PI3K signaling and cellular viability. Blood. 2011; 117 2: 591–594.
  • Herman S. E., Gordon A. L., Wagner A. J., . Phosphatidylinositol 3-kinase-delta inhibitor CAL-101 shows promising preclinical activity in chronic lymphocytic leukemia by antagonizing intrinsic and extrinsic cellular survival signals. Blood. 2010; 116 12: 2078–2088.
  • Ikeda H., Hideshima T., Fulciniti M., . PI3K/p110δ is a novel therapeutic target in multiple myeloma. Blood. 2010; 116 9: 1460–1468.
  • Lee K. S., Lee H. K., Hayflick J. S., Lee Y. C., Puri K. D.. Inhibition of phosphoinositide 3-kinaseδ attenuates allergic airway inflammation and hyperresponsiveness in murine asthma model. FASEB J.. 2006; 20 3: 455–465.
  • Puri K. D., Doggett T. A., Douangpanya J., . Mechanisms and implications of phosphoinositide 3-kinase δ in promoting neutrophil trafficking into inflamed tissue. Blood. 2004; 103 9: 3448–3456.
  • Park S. J., Lee K. S., Kim S. R., . Phosphoinositide 3-kinase δ inhibitor suppresses interleukin-17 expression in a murine asthma model. Eur. Respir. J.. 2010; 36 6: 1448–1459.
  • Haylock-Jacobs S., Comerford I., Bunting M., . PI3Kδ drives the pathogenesis of experimental autoimmune encephalomyelitis by inhibiting effector T cell apoptosis and promoting Th17 differentiation. J. Autoimmun.. 2011; 36 3-4: 278–287.
  • Soond D. R., Bjorgo E., Moltu K., . PI3K p110δ regulates T-cell cytokine production during primary and secondary immune responses in mice and humans. Blood. 2010; 115 11: 2203–2213.
  • Marone R., Cmiljanovic V., Giese B., Wymann M. P.. Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim. Biophys. Acta. 2008; 1784 1: 159–185.
  • Durand C. A., Hartvigsen K., Fogelstrand L., . Phosphoinositide 3-kinase p110δ regulates natural antibody production, marginal zone and B-1 B cell function, and autoantibody responses. J. Immunol.. 2009; 183 9: 5673–5684.
  • Fung-Leung W. P.. Phosphoinositide 3-kinase δ (PI3Kδ) in leukocyte signaling and function. Cell Signal.. 2011; 23 4: 603–608.
  • Ali K., Bilancio A., Thomas M., . Essential role for the p110δ phosphoinositide 3-kinase in the allergic response. Nature. 2004; 431 7011: 1007–1011.
  • Ali K., Camps M., Pearce W. P., . Isoform-specific functions of phosphoinositide 3-kinases: p110δ but not p110γ promotes optimal allergic responses in vivo. J. Immunol.. 2008; 180 4: 2538–2544.
  • Geoffrey R., Jia S., Kwitek A. E., . Evidence of a functional role for mast cells in the development of type 1 diabetes mellitus in the BioBreeding rat. J. Immunol.. 2006; 177 10: 7275–7286.
  • Okkenhaug K., Patton D. T., Bilancio A., . The p110delta isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J. Immunol.. 2006; 177 8: 5122–5128.
  • Sinclair L. V., Finlay D., Feijoo C., . Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat. Immunol.. 2008; 9 5: 513–521.
  • Randis T. M., Puri K. D., Zhou H., Diacovo T. G.. Role of PI3Kδ and PI3Kγ in inflammatory arthritis and tissue localization of neutrophils. Eur. J. Immunol.. 2008; 38 5: 1215–1224.
  • Judkowski V., Pinilla C., Schroder K., . Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol.. 2001; 166 2: 908–917.
  • Haskins K., McDuffie M.. Acceleration of diabetes in young NOD mice with a CD4+ islet-specific T cell clone. Science. 1990; 249 4975: 1433–1436.
  • Mueller R., Bradley L. M., Krahl T., Sarvetnick N.. Mechanism underlying counterregulation of autoimmune diabetes by IL-4. Immunity. 1997; 7 3: 411–418.
  • Michel C., Boitard C., Bach J. F.. Insulin autoantibodies in non-obese diabetic (NOD) mice. Clin. Exp. Immunol.. 1989; 75 3: 457–460.
  • von Herrath M., Nepom G. T.. Remodeling rodent models to mimic human type 1 diabetes. Eur. J. Immunol.. 2009; 39 8: 2049–2054.
  • von Herrath M., Nepom G. T.. Animal models of human type 1 diabetes. Nat. Immunol.. 2009; 10 2: 129–132.
  • Maxwell M. J., Tsantikos E., Kong A. M., . Attenuation of phosphoinositide 3-kinase delta signaling restrains autoimmune disease. J. Autoimmun.. 2012; 38 4: 381–391.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.