Ifn-γ-dependent secretion of IL-10 from Th1 cells and microglia/macrophages contributes to functional recovery after spinal cord injury

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Ishii, H ^a,b,c   Tanabe, S ^a,b   Ueno, M ^a,b   Kubo, T ^c   Kayama, H ^a   Serada, S ^d   Fujimoto, M ^d   Takeda, K ^a   Naka, T ^d   Yamashita, T ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c CHIBA UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

Author keywords

Interleukin 10; Microglia macrophages; Spinal cord injury; Th1 cells

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CONVALESCENCE; CYTOKINE RELEASE; FEMALE; KNOCKOUT MOUSE; LYMPHOCYTE TRANSFER; MACROPHAGE; MACROPHAGE ACTIVATION; MICROGLIA; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY; TH1 CELL;

EID: 84881060258     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.234     Document Type: Article

References (38)

1. David S, Aguayo AJ. Axonal elongation into peripheral nervous system 'bridges' after central nervous system injury in adult rats. Science 1981; 214: 931-933.
2. Bye N, Habgood MD, Callaway JK, Malakooti N, Potter A, Kossmann T et al. Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp Neurol 2007; 204: 220-233.
3. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 2010; 133: 433-447.
4. Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 2008; 209: 378-388.
5. Potas JR, Zheng Y, Moussa C, Venn M, Gorrie CA, Deng C et al. Augmented locomotor recovery after spinal cord injury in the athymic nude rat. J Neurotrauma 2006; 23: 660-673.
6. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I et al. Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med 2009; 15: 946-950.
7. Hofstetter HH, Sewell DL, Liu F, Sandor M, Forsthuber T, Lehmann PV et al. Autoreactive T cells promote post-traumatic healing in the central nervous system. J Neuroimmunol 2003; 134: 25-34.
8. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006; 9: 268-275.
9. Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK et al. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci USA 2008; 105: 17913-17918.
10. Ishii H, Jin X, Ueno M, Tanabe S, Kubo T, Serada S et al. Adoptive transfer of Th1-conditioned lymphocytes promotes axonal remodeling and functional recovery after spinal cord injury. Cell Death Dis 2012; 3: e363.
11. Hendrix S, Nitsch R. The role of T helper cells in neuroprotection and regeneration. J Neuroimmunol 2007; 184: 100-112.
12. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR et al. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 2010; 207: 1067-1080.
13. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007; 13: 1173-1175.
14. Hafler DA. Multiple sclerosis. J Clin Invest 2004; 113: 788-794.
15. Fransson ME, Liljenfeldt LS, Fagius J, Tötterman TH, Loskog AS. The T-cell pool is anergized in patients with multiple sclerosis in remission. Immunology 2009; 126: 92-101.
16. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 2009; 31: 539-550.
17. Mullen AC, High FA, Hutchins AS, Lee HW, Villarino AV, Livingston DM et al. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 2001; 292: 1907-1910.
18. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 2006; 23: 635-659.
19. Metz GA, Merkler D, Dietz V, Schwab ME, Fouad K. Efficient testing of motor function in spinal cord injured rats. Brain Res 2000; 883: 165-177.
20. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4\+ T cells compared. J Immunol 1995; 154: 4309-4321.
21. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 2009; 15: 192-199.
22. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 2011; 12: 388-399.
23. Iannotti C, Ping Zhang Y, Shields CB, Han Y, Burke DA, Xu XM. A neuroprotective role of glial cell line-derived neurotrophic factor following moderate spinal cord contusion injury. Exp Neurol 2004; 189: 317-332.
24. Ghosh A, Greenberg ME. Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 1995; 15: 89-103.
25. Zhou Z, Peng X, Insolera R, Fink DJ, Mata M. IL-10 promotes neuronal survival following spinal cord injury. Exp Neurol 2009; 220: 183-190.
26. Saraiva M, Christensen JR, Veldhoen M, Murphy TL, Murphy KM, O'Garra A. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 2009; 31: 209-219.
27. Ishii H, Kubo T, Kumanogoh A, Yamashita T. Th1 cells promote neurite outgrowth from cortical neurons via a mechanism dependent on semaphorins. Biochem Biophys Res Commun 2010; 402: 168-172.
28. Shaw MH, Freeman GJ, Scott MF, Fox BA, Bzik DJ, Belkaid Y et al. Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma-dependent IL-10 reactivation. J Immunol 2006; 176: 7263-7271.
29. Wong G, Goldshmit Y, Turnley AM. Interferon-gamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Exp Neurol 2004; 187: 171-177.
30. Baron R, Nemirovsky A, Harpaz I, Cohen H, Owens T, Monsonego A. IFN-gamma enhances neurogenesis in wild-type mice and in a mouse model of Alzheimer's disease. FASEB J 2008; 22: 2843-2852.
31. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006; 31: 149-160.
32. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 2009; 6: e1000113.
33. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009; 29: 13435-13444.
34. Horino J, Fujimoto M, Terabe F, Serada S, Takahashi T, Soma Y et al. Suppressor of cytokine signaling-1 ameliorates dextran sulfate sodium-induced colitis in mice. Int Immunol 2008; 20: 753-762.
35. Hirotani T, Lee PY, Kuwata H, Yamamoto M, Matsumoto M, Kawase I et al. The nuclear IkappaB protein IkappaBNS selectively inhibits lipopolysaccharideinduced IL-6 production in macrophages of the colonic lamina propria. J Immunol 2005; 174: 3650-3657.
36. Engesser-Cesar C, Anderson AJ, Basso DM, Edgerton VR, Cotman CW. Voluntary wheel running improves recovery from a moderate spinal cord injury. J Neurotrauma 2005; 22: 157-171.
37. Serada S, Fujimoto M, Mihara M, Koike N, Ohsugi Y, Nomura S et al. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2008; 105: 9041-9046.
38. Kitayama M, Ueno M, Itakura T, Yamashita T. Activated microglia inhibit axonal growth through RGMa. PLoS One 2011; 6: e25234.