Effector molecules released by Th1 but not Th17 cells drive an M1 response in microglia

Brain, Behavior, and Immunity

Volumn 37, Issue , 2014, Pages 248-259

  Prajeeth, Chittappen K ^a   Löhr, Kirsten ^b   Floess, Stefan ^b   Zimmermann, Julian ^e   Ulrich, Reiner ^c   Gudi, Viktoria ^a   Beineke, Andreas ^c   Baumgärtner, Wolfgang ^c,d   Müller, Marcus ^e   Huehn, Jochen ^b   Stangel, Martin ^a,d  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^e UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Microglia; Th1; Th17

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 17; INTERLEUKIN 23;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL CONTACT; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; M1 MACROPHAGE; MACROPHAGE; MALE; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUPERNATANT; TH1 CELL; TH17 CELL; TRANSGENIC MOUSE;

MICROGLIA; TH1; TH17;

ANIMALS; INTERLEUKIN-17; INTERLEUKIN-23 SUBUNIT P19; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; TH1 CELLS; TH17 CELLS;

EID: 84896701840     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.01.001     Document Type: Article

References (56)

1. Aguzzi A., Barres B.A., Bennett M.L. Microglia: Scapegoat, saboteur, or something else?. Science 2013, 339:156-161.
2. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
3. Bhasin M., Wu M., Tsirka S.E. Modulation of microglial/macrophage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis. BMC Immunol. 2007, 8:10.
4. Boje K.M., Arora P.K. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 1992, 587:250-256.
5. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D.A., Stella A.M. Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 2007, 8:766-775.
6. Carlson M.J., West M.L., Coghill J.M., Panoskaltsis-Mortari A., Blazar B.R., Serody J.S. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood 2009, 113:1365-1374.
7. Codarri L., Gyulveszi G., Tosevski V., Hesske L., Fontana A., Magnenat L., Suter T., Becher B. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 2011, 12:560-567.
8. Conductier G., Blondeau N., Guyon A., Nahon J.L., Rovere C. The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J. Neuroimmunol. 2010, 224:93-100.
9. Corbin J.G., Kelly D., Rath E.M., Baerwald K.D., Suzuki K., Popko B. Targeted CNS expression of interferon-gamma in transgenic mice leads to hypomyelination, reactive gliosis, and abnormal cerebellar development. Mol. Cell. Neurosci. 1996, 7:354-370.
10. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12:388-399.
11. de Haas A.H., Boddeke H.W., Biber K. Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 2008, 56:888-894.
12. Deng B., Wehling-Henricks M., Villalta S.A., Wang Y., Tidball J.G. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration. J. Immunol. 2012, 189:3669-3680.
13. Domingues H.S., Mues M., Lassmann H., Wekerle H., Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PloS One 2010, 5:e15531.
14. Dong C. TH17 cells in development: An updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 2008, 8:337-348.
15. Durafourt B.A., Moore C.S., Zammit D.A., Johnson T.A., Zaguia F., Guiot M.C., Bar-Or A., Antel J.P. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 2012, 60:717-727.
16. El-Behi M., Ciric B., Dai H., Yan Y., Cullimore M., Safavi F., Zhang G.X., Dittel B.N., Rostami A. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 2011, 12:568-575.
17. Esen N., Kielian T. Effects of low dose GM-CSF on microglial inflammatory profiles to diverse pathogen-associated molecular patterns (PAMPs). J. Neuroinflamm. 2007, 4:10.
18. Fischer H.G., Nitzgen B., Germann T., Degitz K., Daubener W., Hadding U. Differentiation driven by granulocyte-macrophage colony-stimulating factor endows microglia with interferon-gamma-independent antigen presentation function. J. Neuroimmunol. 1993, 42:87-95.
19. Gerritse K., Laman J.D., Noelle R.J., Aruffo A., Ledbetter J.A., Boersma W.J., Claassen E. CD40-CD40 ligand interactions in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. USA 1996, 93:2499-2504.
20. Gocke A.R., Cravens P.D., Ben L.H., Hussain R.Z., Northrop S.C., Racke M.K., Lovett-Racke A.E. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J. Immunol. 2007, 178:1341-1348.
21. Goldmann T., Prinz M. Role of microglia in CNS autoimmunity. Clin. Dev. Immunol. 2013, 2013:208093.
22. Goverman J. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 2009, 9:393-407.
23. Heppner F.L., Greter M., Marino D., Falsig J., Raivich G., Hovelmeyer N., Waisman A., Rulicke T., Prinz M., Priller J., Becher B., Aguzzi A. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 2005, 11:146-152.
24. Howard L.M., Miga A.J., Vanderlugt C.L., Dal Canto M.C., Laman J.D., Noelle R.J., Miller S.D. Mechanisms of immunotherapeutic intervention by anti-CD40L (CD154) antibody in an animal model of multiple sclerosis. J. Clin. Invest. 1999, 103:281-290.
25. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
26. Janke M., Peine M., Nass A., Morawietz L., Hamann A., Scheffold A. In-vitro-induced Th17 cells fail to induce inflammation in vivo and show an impaired migration into inflamed sites. Eur. J. Immunol. 2010, 40:1089-1098.
27. Jankovic D., Kullberg M.C., Feng C.G., Goldszmid R.S., Collazo C.M., Wilson M., Wynn T.A., Kamanaka M., Flavell R.A., Sher A. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 2007, 204:273-283.
28. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci.: Official J. Soc. Neurosci. 2009, 29:13435-13444.
29. Kolls J.K., Linden A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467-476.
30. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu. Rev. Immunol. 2009, 27:485-517.
31. Lee Y., Awasthi A., Yosef N., Quintana F.J., Xiao S., Peters A., Wu C., Kleinewietfeld M., Kunder S., Hafler D.A., Sobel R.A., Regev A., Kuchroo V.K. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 2012, 13:991-999.
32. Lin W.S., Kemper A., McCarthy K.D., Pytel P., Wang J.P., Campbell I.L., Utset M.F., Popko B. Interferon-gamma induced medulloblastoma in the developing cerebellum. J. Neurosci. 2004, 24:10074-10083.
33. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 2006, 177:7303-7311.
34. McQuillan K., Lynch M.A., Mills K.H. Activation of mixed glia by Abeta-specific Th1 and Th17 cells and its regulation by Th2 cells. Brain Behav. Immun. 2010, 24:598-607.
35. Merson T.D., Binder M.D., Kilpatrick T.J. Role of cytokines as mediators and regulators of microglial activity in inflammatory demyelination of the CNS. Neuromol. Med. 2010, 12:99-132.
36. Murphy A.C., Lalor S.J., Lynch M.A., Mills K.H. Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010, 24:641-651.
37. Nakayamada S., Kanno Y., Takahashi H., Jankovic D., Lu K.T., Johnson T.A., Sun H.W., Vahedi G., Hakim O., Handon R., Schwartzberg P.L., Hager G.L., O'Shea J.J. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011, 35:919-931.
38. Nicklas W., Baneux P., Boot R., Decelle T., Deeny A.A., Fumanelli M., Illgen-Wilcke B. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab. Anim. 2002, 36:20-42.
39. Nurieva R., Yang X.O., Chung Y., Dong C. Cutting edge: in vitro generated Th17 cells maintain their cytokine expression program in normal but not lymphopenic hosts. J. Immunol. 2009, 182:2565-2568.
40. O'Garra A., Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 2007, 7:425-428.
41. Pierson E., Simmons S.B., Castelli L., Goverman J.M. Mechanisms regulating regional localization of inflammation during CNS autoimmunity. Immunol. Rev. 2012, 248:205-215.
42. Ponomarev E.D., Shriver L.P., Maresz K., Pedras-Vasconcelos J., Verthelyi D., Dittel B.N. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J. Immunol. 2007, 178:39-48.
43. Ransohoff R.M., Brown M.A. Innate immunity in the central nervous system. J. Clin. Invest. 2012, 122:1164-1171.
44. Ransohoff R.M., Engelhardt B. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat. Rev. Immunol. 2012, 12:623-635.
45. Sallusto F., Impellizzieri D., Basso C., Laroni A., Uccelli A., Lanzavecchia A., Engelhardt B. T-cell trafficking in the central nervous system. Immunol. Rev. 2012, 248:216-227.
46. Semple B.D., Kossmann T., Morganti-Kossmann M.C. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cerebr. Blood Flow Metab.: Official J. Int. Soc. Cerebr. Blood Flow Metab. 2010, 30:459-473.
47. Sierra A., Gottfried-Blackmore A.C., McEwen B.S., Bulloch K. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 2007, 55:412-424.
48. Stockinger B., Veldhoen M. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 2007, 19:281-286.
49. Tambuyzer B.R., Ponsaerts P., Nouwen E.J. Microglia: gatekeepers of central nervous system immunology. J. Leukocyte Biol. 2009, 85:352-370.
50. Trajkovic V., Stosic-Grujicic S., Samardzic T., Markovic M., Miljkovic D., Ramic Z., Mostarica Stojkovic M. Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J. Neuroimmunol. 2001, 119:183-191.
51. Vass K., Heininger K., Schafer B., Linington C., Lassmann H. Interferon-gamma potentiates antibody-mediated demyelination in vivo. Ann. Neurol. 1992, 32:198-206.
52. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189.
53. Wilson C.B., Rowell E., Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 2009, 9:91-105.
54. Yang Y., Weiner J., Liu Y., Smith A.J., Huss D.J., Winger R., Peng H., Cravens P.D., Racke M.K., Lovett-Racke A.E. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J. Exp. Med. 2009, 206:1549-1564.
55. Yosef N., Shalek A.K., Gaublomme J.T., Jin H., Lee Y., Awasthi A., Wu C., Karwacz K., Xiao S., Jorgolli M., Gennert D., Satija R., Shakya A., Lu D.Y., Trombetta J.J., Pillai M.R., Ratcliffe P.J., Coleman M.L., Bix M., Tantin D., Park H., Kuchroo V.K., Regev A. Dynamic regulatory network controlling TH17 cell differentiation. Nature 2013, 496:461-468.
56. Zimmermann J., Krauthausen M., Hofer M.J., Heneka M.T., Campbell I.L., Muller M. CNS-targeted production of IL-17A induces glial activation, microvascular pathology and enhances the neuroinflammatory response to systemic endotoxemia. PloS One 2013, 8:e57307.