IL-10-dependent Tr1 cells attenuate astrocyte activation and ameliorate chronic central nervous system inflammation

Brain

Volumn 139, Issue 7, 2016, Pages 1939-1957

  Mayo, Lior ^a,b   Cunha, Andre Pires Da ^a   Madi, Asaf ^a   Beynon, Vanessa ^a   Yang, Zhiping ^c   Alvarez, Jorge I ^d,e   Prat, Alexandre ^d   Sobel, Raymond A ^f   Kobzik, Lester ^c   Lassmann, Hans ^g   Quintana, Francisco J ^a   Weiner, Howard L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g Medical University of Vienna   (Austria)

Author keywords

astrocyte; interleukin 10; multiple sclerosis; neuroinflammation; T lymphocytes

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR ALPHA; LATENCY ASSOCIATED PEPTIDE; LENTIVIRUS VECTOR; MONOCLONAL ANTIBODY CD3; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTOME; CD3 ANTIGEN; IMMUNOLOGIC FACTOR; OKT 3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL LINEAGE; CHRONIC CENTRAL NERVOUS SYSTEM INFLAMMATION; CHRONIC INFLAMMATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; LENTIVIRINAE; LIGAND BINDING; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NONVIRAL GENE THERAPY; OLIGODENDROGLIA; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY T LYMPHOCYTE; STREPTOCOCCUS PNEUMONIA; TH0 CELL; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; NONOBESE DIABETIC MOUSE;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, CD3; ASTROCYTES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOLOGIC FACTORS; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MUROMONAB-CD3; PNEUMONIA, PNEUMOCOCCAL; T-LYMPHOCYTES, REGULATORY;

EID: 84977514700     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aww113     Document Type: Article

References (63)

1. Allan SE, Broady R, Gregori S, Himmel ME, Locke N, Roncarolo MG, et al. CD4 + T-regulatory cells: toward therapy for human diseases. Immunol Rev 2008; 223: 391-421.
2. Alvarez JI, Dodelet-Devillers A, Kebir H, Ifergan I, Fabre PJ, Terouz S, et al. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 2011; 334: 1727-31.
3. Anderson AC, Anderson DE, Bregoli L, Hastings WD, Kassam N, Lei C, et al. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007; 318: 1141-3.
4. Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, et al. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 2010; 11: 854-61.
5. Argaw AT, Asp L, Zhang J, Navrazhina K, Pham T, Mariani JN, et al. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J Clin Invest 2012; 122: 2454-68.
6. Arredouani M, Yang Z, Ning Y, Qin G, Soininen R, Tryggvason K, et al. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med 2004; 200: 267-72.
7. Astier AL, Astier AL, Hafler DA, Hafler DA. Abnormal Tr1 differentiation in multiple sclerosis. J Neuroimmunol 2007; 191: 70-8.
8. Baeten DL, Kuchroo VK. How Cytokine networks fuel inflammation: Interleukin-17 and a tale of two autoimmune diseases. Nat Med 2013; 19: 824-5.
9. Barrat FJ, Cua DJ, Boonstra A, Richards DF, Crain C, Savelkoul HF, et al. In vitro generation of interleukin 10-producing regulatory CD4( + ) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)-and Th2-inducing cytokines. J Exp Med 2002; 195: 603-16.
10. Basso AS, Frenkel D, Quintana FJ, Costa-Pinto FA, Petrovic-Stojkovic S, Puckett L, et al. Reversal of axonal loss and disability in a mouse model of progressive multiple sclerosis. J Clin Invest 2008; 118: 1532-43.
11. Clarke LE, Barres BA. Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 2013; 14: 311-21.
12. Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372: 1502-17.
13. Daifotis AG, Koenig S, Chatenoud L, Herold KC. Anti-CD3 clinical trials in type 1 diabetes mellitus. Clin Immunol 2013; 149: 268-78.
14. Dal-Secco D, Wang J, Zeng Z, Kolaczkowska E, Wong CH, Petri B, et al. A dynamic spectrum of monocytes arising from the in situ reprogramming of CCR2 + monocytes at a site of sterile injury. J Exp Med 2015; 212: 447-56.
15. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 2011; 12: 388-99.
16. Ding X, Yan Y, Li X, Li K, Ciric B, Yang J, et al. Silencing IFNgamma binding/signaling in astrocytes versus microglia leads to opposite effects on central nervous system autoimmunity. J Immunol 2015; 194: 4251-64.
17. Farez MF, Quintana FJ, Gandhi R, Izquierdo G, Lucas M, Weiner HL. Toll-like receptor 2 and poly(ADP-ribose) polymerase 1 promote central nervous system neuroinflammation in progressive EAE. Nat Immunol 2009; 10: 958-64.
18. Fitzgerald DC, Zhang G-X, El-Behi M, Fonseca-Kelly Z, Li H, Yu S, et al. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat Immunol 2007; 8: 1372-9.
19. Frenkel D, Huang Z, Maron R, Koldzic DN, Hancock WW, Moskowitz MA, et al. Nasal vaccination with myelin oligodendrocyte glycoprotein reduces stroke size by inducing IL10-producing CD4+ T cells. J Immunol 2003; 171: 6549-55.
20. Han MH, Hwang SI, Roy DB, Lundgren DH, Price JV, Ousman SS, et al. Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 2008; 451: 1076-81.
21. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hovelmeyer N, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005; 11: 146-52.
22. Huber AK, Wang L, Han P, Zhang X, Ekholm S, Srinivasan A, et al. Dysregulation of the IL-23/IL-17 axis and myeloid factors in secondary progressive multiple sclerosis. Neurology 2014; 83: 1500-7.
23. Huber S, Gagliani N, Esplugues E, O'Connor W Jr, Huber FJ, Chaudhry A, et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3(-) and Foxp3 + regulatory CD4 + T cells in an interleukin-10-dependent manner. Immunity 2011; 34: 554-65.
24. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 2000; 192: 1075-80.
25. Kickler K, Ni Choileain S, Williams A, Richards A, Astier AL. Calcitriol modulates the CD46 pathway in T cells. PLoS One 2012; 7: e48486.
26. Kim RY, Hoffman AS, Itoh N, Ao Y, Spence R, Sofroniew MV, et al. Astrocyte CCL2 sustains immune cell infiltration in chronic experimental autoimmune encephalomyelitis. J Neuroimmunol 2014; 274: 53-61.
27. Kleinewietfeld M, Hafler DA. Regulatory T cells in autoimmune neuroinflammation. Immunol Rev 2014; 259: 231-44.
28. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 2011; 12: 231-8.
29. Lassmann H, van Horssen J, Mahad D. Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol 2012; 8: 647-56.
30. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002; 8: 500-8.
31. Mayo L, Quintana FJ, Weiner HL. The innate immune system in demyelinating disease. Immunol Rev 2012; 248: 170-87.
32. Mayo L, Trauger SA, Blain M, Nadeau M, Patel B, Alvarez JI, et al. Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation. Nat Med 2014; 20: 1147-56.
33. Mildner A, Mack M, Schmidt H, Bruck W, Djukic M, Zabel MD, et al. CCR2+ Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 2009; 132 (Pt 9): 2487-500.
34. Miranda-Hernandez S, Baxter AG. Role of toll-like receptors in multiple sclerosis. Am J Clin Exp Immunol 2013; 2: 75-93.
35. Miron VE, Boyd A, Zhao JW, Yuen TJ, Ruckh JM, Shadrach JL, et al. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 2013; 16: 1211-18.
36. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Ann Rev Immunol 2001; 19: 683-765.
37. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011; 11: 723-37.
38. Myer DJ, Gurkoff GG, Lee SM, Hovda DA, Sofroniew MV. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 2006; 129 (Pt 10): 2761-72.
39. Nagelhus EA, Ottersen OP. Physiological roles of aquaporin-4 in brain. Physiol Rev 2013; 93: 1543-62.
40. Nylander A, Hafler DA. Multiple sclerosis. J Clin Invest 2012; 122: 1180-8.
41. Ochi H, Abraham M, Ishikawa H, Frenkel D, Yang K, Basso AS, et al. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+ CD25-LAP + T cells. Nat Med 2006; 12: 627-35.
42. Petereit HF, Pukrop R, Fazekas F, Bamborschke SU, Ropele S, Kolmel HW, et al. Low interleukin-10 production is associated with higher disability and MRI lesion load in secondary progressive multiple sclerosis. J Neurol Sci 2003; 206: 209-14.
43. Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat Med 2011; 17: 64-70.
44. Prinz M, Priller J, Sisodia SS, Ransohoff RM. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 2011; 14: 1227-35.
45. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006; 212: 28-50.
46. Saura J, Tusell JM, Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia 2003; 44: 183-9.
47. Seifert G, Schilling K, Steinhauser C. Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat Rev Neurosci 2006; 7: 194-206.
48. Soldan SS, Alvarez Retuerto AI, Sicotte NL, Voskuhl RR. Dysregulation of IL-10 and IL-12p40 in secondary progressive multiple sclerosis. J Neuroimmunol 2004; 146: 209-15.
49. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledgebased approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-50.
50. Tsai HH, Li H, Fuentealba LC, Molofsky AV, Taveira-Marques R, Zhuang H, et al. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 2012; 337: 358-62.
51. Ulitsky I, Maron-Katz A, Shavit S, Sagir D, Linhart C, Elkon R, et al. Expander: from expression microarrays to networks and functions. Nat Protoc 2010; 5: 303-22.
52. van Boxel-Dezaire AH, Hoff SC, van Oosten BW, Verweij CL, Drager AM, Ader HJ, et al. Decreased interleukin-10 and increased interleukin-12p40 mRNA are associated with disease activity and characterize different disease stages in multiple sclerosis. Ann Neurol 1999; 45: 695-703.
53. Watkins TA, Emery B, Mulinyawe S, Barres BA. Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 2008; 60: 555-69.
54. Weiner HL. A shift from adaptive to innate immunity: a potential mechanism of disease progression in multiple sclerosis. J Neurol 2008; 255 (Suppl 1): 3-11.
55. Weiner HL, da Cunha AP, Quintana F, Wu H. Oral tolerance. Immunol Rev 2011; 241: 241-59.
56. Wingerchuk DM, Carter JL. Multiple sclerosis: current and emerging disease-modifying therapies and treatment strategies. Mayo Clin Proc 2014; 89: 225-40.
57. Wu HY, Center EM, Tsokos GC, Weiner HL. Suppression of murine SLE by oral anti-CD3: inducible CD4+ CD25-LAP + regulatory T cells control the expansion of IL-17 + follicular helper T cells. Lupus 2009; 18: 586-96.
58. Wu HY, Maron R, Tukpah A-M, Weiner HL. Mucosal anti-CD3 monoclonal antibody attenuates collagen-induced arthritis that is associated with induction of LAP + regulatory T cells and is enhanced by administration of an emulsome-based Th2-skewing adjuvant. J Immunol 2010; 185: 3401-7.
59. Wu HY, Quintana FJ, da Cunha AP, Dake BT, Koeglsperger T, Starossom SC, et al. In vivo induction of Tr1 cells via mucosal dendritic cells and AHR signaling. PLoS One 2011; 6: e23618.
60. Wu HY, Quintana FJ, Weiner HL. Nasal anti-CD3 antibody ameliorates lupus by inducing an IL-10-secreting CD4+ CD25-LAP + regulatory T cell and is associated with down-regulation of IL-17 + CD4+ ICOS + CXCR5+ follicular helper T cells. J Immunol 2008; 181: 6038-50.
61. Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med 2014; 211: 1533-49.
62. Yan Y, Ding X, Li K, Ciric B, Wu S, Xu H, et al. CNS-specific therapy for ongoing EAE by silencing IL-17 pathway in astrocytes. Mol Ther 2012; 20: 1338-48.
63. Yang Z, Chiou TT, Stossel TP, Kobzik L. Plasma gelsolin improves lung host defense against pneumonia by enhancing macrophage NOS3 function. Am J Physiol Lung Cell Mol Physiol 2015; 309: L11-16.