nature.com

D-mannose induces regulatory T cells and suppresses immunopathology - Nature Medicine

  • ️Chen, WanJun
  • ️Mon Jul 24 2017
  • Etchison, J.R. & Freeze, H.H. Enzymatic assay of D-mannose in serum. Clin. Chem. 43, 533–538 (1997).

    CAS  PubMed  Google Scholar 

  • Schneider, A. et al. Successful prenatal mannose treatment for congenital disorder of glycosylation-Ia in mice. Nat. Med. 18, 71–73 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Alton, G. et al. Direct utilization of mannose for mammalian glycoprotein biosynthesis. Glycobiology 8, 285–295 (1998).

    Article  CAS  PubMed  Google Scholar 

  • de Lonlay, P. & Seta, N. The clinical spectrum of phosphomannose isomerase deficiency, with an evaluation of mannose treatment for CDG-Ib. Biochim. Biophys. Acta 1792, 841–843 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Michaels, E.K., Chmiel, J.S., Plotkin, B.J. & Schaeffer, A.J. Effect of D-mannose and D-glucose on Escherichia coli bacteriuria in rats. Urol. Res. 11, 97–102 (1983).

    Article  CAS  PubMed  Google Scholar 

  • Kranjčec, B., Papeš, D. & Altarac, S. D-mannose powder for prophylaxis of recurrent urinary tract infections in women: a randomized clinical trial. World J. Urol. 32, 79–84 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Schaeffer, A.J., Chmiel, J.S., Duncan, J.L. & Falkowski, W.S. Mannose-sensitive adherence of Escherichia coli to epithelial cells from women with recurrent urinary tract infections. J. Urol. 131, 906–910 (1984).

    Article  CAS  PubMed  Google Scholar 

  • Wang, R. & Green, D.R. Metabolic checkpoints in activated T cells. Nat. Immunol. 13, 907–915 (2012).

    Article  CAS  PubMed  Google Scholar 

  • MacIver, N.J., Michalek, R.D. & Rathmell, J.C. Metabolic regulation of T lymphocytes. Annu. Rev. Immunol. 31, 259–283 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vander Heiden, M.G., Cantley, L.C. & Thompson, C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029–1033 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coombes, J.L. et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757–1764 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, C.M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775–1785 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thornton, A.M. & Shevach, E.M. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188, 287–296 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Read, S., Malmström, V. & Powrie, F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25+CD4+ regulatory cells that control intestinal inflammation. J. Exp. Med. 192, 295–302 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huehn, J., Polansky, J.K. & Hamann, A. Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat. Rev. Immunol. 9, 83–89 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Chen, W. et al. Conversion of peripheral CD4+CD25 naive T cells to CD4+CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875–1886 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, W. & Konkel, J.E. Development of thymic Foxp3+ regulatory T cells: TGF-β matters. Eur. J. Immunol. 45, 958–965 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konkel, J.E., Jin, W., Abbatiello, B., Grainger, J.R. & Chen, W. Thymocyte apoptosis drives the intrathymic generation of regulatory T cells. Proc. Natl. Acad. Sci. USA 111, E465–E473 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derynck, R. & Zhang, Y.E. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577–584 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Feng, X.H. & Derynck, R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature 394, 909–913 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y. et al. A critical function for TGF-β signaling in the development of natural CD4+CD25+Foxp3+ regulatory T cells. Nat. Immunol. 9, 632–640 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Nakatsukasa, H. et al. The DNA-binding inhibitor Id3 regulates IL-9 production in CD4+ T cells. Nat. Immunol. 16, 1077–1084 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, X. et al. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J. 18, 1280–1291 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tone, Y. et al. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9, 194–202 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Chen, W. & Konkel, J.E. TGF-β and 'adaptive' Foxp3+ regulatory T cells. J. Mol. Cell Biol. 2, 30–36 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Baecher-Allan, C., Brown, J.A., Freeman, G.J. & Hafler, D.A. CD4+CD25high regulatory cells in human peripheral blood. J. Immunol. 167, 1245–1253 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Chen, W. & Wahl, S.M. TGF-β: receptors, signaling pathways and autoimmunity. Curr. Dir. Autoimmun. 5, 62–91 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Massagué, J. & Chen, Y.G. Controlling TGF-β signaling. Genes Dev. 14, 627–644 (2000).

    PubMed  Google Scholar 

  • Shi, M. et al. Latent TGF-β structure and activation. Nature 474, 343–349 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worthington, J.J. et al. Integrin αvβ8-mediated TGF-β activation by effector regulatory T cells is essential for suppression of T-cell-mediated inflammation. Immunity 42, 903–915 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travis, M.A. et al. Loss of integrin αvβ8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449, 361–365 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards, J.P., Thornton, A.M. & Shevach, E.M. Release of active TGF-β1 from the latent TGF-β1/GARP complex on T regulatory cells is mediated by integrin β8. J. Immunol. 193, 2843–2849 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Chen, W., Frank, M.E., Jin, W. & Wahl, S.M. TGF-β released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 14, 715–725 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Amarnath, S., Dong, L., Li, J., Wu, Y. & Chen, W. Endogenous TGF-β activation by reactive oxygen species is key to Foxp3 induction in TCR-stimulated and HIV-1-infected human CD4+CD25 T cells. Retrovirology 4, 57 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hildeman, D.A., Mitchell, T., Kappler, J. & Marrack, P. T cell apoptosis and reactive oxygen species. J. Clin. Invest. 111, 575–581 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sena, L.A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulua, A.C. et al. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J. Exp. Med. 208, 519–533 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosca, M.G. et al. Oxidation of fatty acids is the source of increased mitochondrial reactive oxygen species production in kidney cortical tubules in early diabetes. Diabetes 61, 2074–2083 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seifert, E.L., Estey, C., Xuan, J.Y. & Harper, M.E. Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation. J. Biol. Chem. 285, 5748–5758 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Anderson, M.S. & Bluestone, J.A. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23, 447–485 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Akirav, E.M. et al. Detection of β cell death in diabetes using differentially methylated circulating DNA. Proc. Natl. Acad. Sci. USA 108, 19018–19023 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  • American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 37, S81–S90 (2014).

  • Walter, D.M. et al. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J. Immunol. 167, 4668–4675 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Takaoka, A. et al. A critical role for mouse CXC chemokine(s) in pulmonary neutrophilia during Th type 1-dependent airway inflammation. J. Immunol. 167, 2349–2353 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Staudt, V. et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33, 192–202 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Wu, L. & Derynck, R. Essential role of TGF-β signaling in glucose-induced cell hypertrophy. Dev. Cell 17, 35–48 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang, C.H. et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153, 1239–1251 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travis, M.A. & Sheppard, D. TGF-β activation and function in immunity. Annu. Rev. Immunol. 32, 51–82 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Davis, J.A. & Freeze, H.H. Studies of mannose metabolism and effects of long-term mannose ingestion in the mouse. Biochim. Biophys. Acta 1528, 116–126 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Derynck, R. & Akhurst, R.J. Differentiation plasticity regulated by TGF-β family proteins in development and disease. Nat. Cell Biol. 9, 1000–1004 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Mayatepek, E., Schröder, M., Kohlmüller, D., Bieger, W.P. & Nützenadel, W. Continuous mannose infusion in carbohydrate-deficient glycoprotein syndrome type I. Acta Paediatr. 86, 1138–1140 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Feuerer, M., Shen, Y., Littman, D.R., Benoist, C. & Mathis, D. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 31, 654–664 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasagi, S. et al. In vivo-generated antigen-specific regulatory T cells treat autoimmunity without compromising antibacterial immune response. Sci. Transl. Med. 6, 241ra78 (2014).

    Article  CAS  PubMed  Google Scholar 

  • Zanvit, P. et al. Antibiotics in neonatal life increase murine susceptibility to experimental psoriasis. Nat. Commun. 6, 8424 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Konkel, J.E. et al. Control of the development of CD8αα+ intestinal intraepithelial lymphocytes by TGF-β. Nat. Immunol. 12, 312–319 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar