γδ T cells as early sensors of tissue damage and mediators of secondary neurodegeneration

Frontiers in Cellular Neuroscience

Volumn 8, Issue November, 2014, Pages 1-5

  Gelderblom, Mathias ^a   Arunachalam, Priyadharshini ^a   Magnus, Tim ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Brain; IL 17; Inflammation; Ischemia; Lymphocyte; Neutrophils; Stroke; T cell

Indexed keywords

CD24 ANTIGEN; CD38 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR; CXCL1 CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GELATINASE B; HEAT SHOCK PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 21; INTERLEUKIN 23; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; NATURAL KILLER CELL RECEPTOR; PATTERN RECOGNITION RECEPTOR; PURINERGIC P2X7 RECEPTOR; SOMATOMEDIN C; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; CELL ACTIVATION; CELL INFILTRATION; CEREBROVASCULAR ACCIDENT; CLINICAL TRIAL (TOPIC); GAMMA DELTA T LYMPHOCYTE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATION; INTRACELLULAR SIGNALING; MICROGLIA; NATURAL KILLER CELL; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REPERFUSION; REVIEW; T LYMPHOCYTE SUBPOPULATION; TISSUE INJURY;

EID: 84908617531     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00368     Document Type: Review

References (48)

1. Arbeloa, J., Pérez-Samartín, A., Gottlieb, M., and Matute, C. (2012). P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol. Dis. 45, 954-961. doi: 10.1016/j.nbd.2011.12.014
2. Becker, K., Kindrick, D., McCarron, R., Hallenbeck, J., and Winn, R. (2003). Adoptive transfer of myelin basic protein-tolerized splenocytes to naive animals reduces infarct size: a role for lymphocytes in ischemic brain injury?Stroke 34, 1809-1815. doi: 10.1161/01.str.0000078308.77727.ea
3. Becker, K. J., McCarron, R. M., Ruetzler, C., Laban, O., Sternberg, E., Flanders, K. C., et al. (1997). Immunologic tolerance to myelin basic protein decreases stroke size after transient focal cerebral ischemia. Proc. Natl. Acad. Sci. U S A 94, 10873-10878. doi: 10.1073/pnas.94.20.10873
4. Bonneville, M., O'Brien, R. L., and Born, W. K. (2010). Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10, 467-478. doi: 10.1038/nri2781
5. Caccamo, N., La Mendola, C., Orlando, V., Meraviglia, S., Todaro, M., Stassi, G., et al. (2011). Differentiation, phenotype and function of interleukin-17-producing human Vγ9Vδ2 T cells. Blood 118, 129-138. doi: 10.1182/blood-2011-01-331298
6. Chen, G. Y., and Nuñez, G. (2010). Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-837. doi: 10.1038/nri2873
7. Choe, C.-U., Lardong, K., Gelderblom, M., Ludewig, P., Leypoldt, F., Koch-Nolte, F., et al. (2011). CD38 exacerbates focal cytokine production, postischemic inflammation and brain injury after focal cerebral ischemia. PLoS One6:e19046. doi: 10.1371/journal.pone.0019046
8. Chuaqui, R., and Tapia, J. (1993). Histologic assessment of the age of recent brain infarcts in man. J. Neuropathol. Exp. Neurol. 52, 481-489. doi: 10.1097/00005072-199309000-00006
9. Clarkson, B. D. S., Ling, C., Shi, Y., Harris, M. G., Rayasam, A., Sun, D., et al. (2014). T cell-derived interleukin (IL)-21 promotes brain injury following stroke in mice. J. Exp. Med. 211, 595-604. doi: 10.1084/jem.20131377
10. del Zoppo, G. J. (2010). Acute anti-inflammatory approaches to ischemic stroke. Ann. N Y Acad. Sci. 1207, 143-148. doi: 10.1111/j.1749-6632.2010.05761.x
11. Frenkel, D., Huang, Z., Maron, R., Koldzic, D. N., Moskowitz, M. A., and Weiner, H. L. (2005). Neuroprotection by IL-10-producing MOG CD4+ T cells following ischemic stroke. J. Neurol. Sci. 233, 125-132. doi: 10.1016/j.jns.2005.03.022
12. Gan, Y., Liu, Q., Wu, W., Yin, J. X., Bai, X. F., Shen, R., et al. (2014). Ischemic neurons recruit natural killer cells that accelerate brain infarction. Proc. Natl. Acad. Sci. U S A 111, 2704-2709. doi: 10.1073/pnas.1315943111
13. Gelderblom, M., Weymar, A., Bernreuther, C., Velden, J., Arunachalam, P., Steinbach, K., et al. (2012). Neutralization of the IL-17 axis diminishes neutrophil invasion and protects from ischemic stroke. Blood 120, 3793-3802. doi: 10.1182/blood-2012-02-412726
14. Hammerich, L., Bangen, J. M., Govaere, O., Zimmermann, H. W., Gassler, N., Huss, S., et al. (2014). Chemokine receptor CCR6-dependent accumulation of γδ T cells in injured liver restricts hepatic inflammation and fibrosis.Hepatology 59, 630-642. doi: 10.1002/hep.26697
15. Heuschmann, P., Busse, O., Wagner, M., Endres, M., Villringer, A., Röther, J., et al. (2010). Schlaganfallhäufigkeit und Versorgung von Schlaganfallpatienten in Deutschland. Akt. Neurol. 37, 333-340. doi: 10.1055/s-0030-1248611
16. Hueber, W., Patel, D. D., Dryja, T., Wright, A. M., Koroleva, I., Bruin, G., et al. (2010). Effects of AIN457, a fully human antibody to Interleukin-17A, on Psoriasis, Rheumatoid Arthritis and Uveitis. Sci. Transl. Med. 2:52ra72. doi: 10.1126/scitranslmed.3001107
17. Hurn, P. D., Subramanian, S., Parker, S. M., Afentoulis, M. E., Kaler, L. J., Vandenbark, A. A., et al. (2007). T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. J. Cereb. Blood Flow Metab. 27, 1798-1805. doi: 10.1038/sj.jcbfm.9600482
18. Iadecola, C., and Anrather, J. (2011). The immunology of stroke: from mechanisms to translation. Nat. Med. 17, 796-808. doi: 10.1038/nm.2399
19. Jensen, K. D. C., Su, X., Shin, S., Li, L., Youssef, S., Yamasaki, S., et al. (2008). Thymic selection determines γδ T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon γ. Immunity29, 90-100. doi: 10.1016/j.immuni.2008.04.022
20. Kebir, H., Kreymborg, K., Ifergan, I., Dodelet-Devillers, A., Cayrol, R., Bernard, M., et al. (2007). Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13, 1173-1175. doi: 10.1038/nm1651
21. Kleinschnitz, C., Kraft, P., Dreykluft, A., Hagedorn, I., Göbel, K., Schuhmann, M. K., et al. (2013). Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature.Blood 121, 679-691. doi: 10.1182/blood-2012-04-426734
22. Kleinschnitz, C., Schwab, N., Kraft, P., Hagedorn, I., Dreykluft, A., Schwarz, T., et al. (2010). Early detrimental T-cell effects in experimental cerebral ischemia are neither related to adaptive immunity nor thrombus formation. Blood115, 3835-3842. doi: 10.1182/blood-2009-10-249078
23. Korn, T., and Petermann, F. (2012). Development and function of interleukin 17-producing γδ T cells. Ann. N Y Acad. Sci. 1247, 34-45. doi: 10.1111/j.1749-6632.2011.06355.x
24. Li, P., Gan, Y., Sun, B.-L., Zhang, F., Lu, B., Gao, Y., et al. (2013). Adoptive regulatory T-cell therapy protects against cerebral ischemia. Ann. Neurol. 74, 458-471. doi: 10.1002/ana.23815
25. Li, P., Mao, L., Liu, X., Gan, Y., Zheng, J., Thomson, A. W., et al. (2014). Essential role of program death 1-Ligand 1 in regulatory T-cell-afforded protection against blood-brain barrier damage after stroke. Stroke 45, 857-864. doi: 10.1161/STROKEAHA.113.004100
26. Li, G.-Z., Zhong, D., Yang, L.-M., Sun, B., Zhongy, Z.-H., Yin, Y.-H., et al. (2005). Expression of interleukin-17 in ischemic brain tissue. Scand. J. Immunol. 62, 481-486. doi: 10.1111/j.1365-3083.2005.01683.x
27. Liesz, A., Suri-Payer, E., Veltkamp, C., Doerr, H., Sommer, C., Rivest, S., et al. (2009). Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat. Med. 15, 192-199. doi: 10.1038/nm.1927
28. Liesz, A., Zhou, W., Mracskó, E., Karcher, S., Bauer, H., Schwarting, S., et al. (2011). Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain 134, 704-720. doi: 10.1093/brain/awr008
29. Liesz, A., Zhou, W., Na, S. Y., Hämmerling, G. J., Garbi, N., Karcher, S., et al. (2013). Boosting regulatory T cells limits neuroinflammation in permanent cortical stroke. J. Neurosci. 33, 17350-17362. doi: 10.1523/JNEUROSCI.4901-12.2013
30. Liu, K., Mori, S., Takahashi, H. K., Tomono, Y., Wake, H., Kanke, T., et al. (2007). Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J. 21, 3904-3916. doi: 10.1096/fj.07-8770com
31. Martin, B., Hirota, K., Cua, D. J., Stockinger, B., and Veldhoen, M. (2009). Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31, 321-330. doi: 10.1016/j.immuni.2009.06.020
32. Mena, H., Cadavid, D., and Rushing, E. J. (2004). Human cerebral infarct: a proposed histopathologic classification based on 137 cases. Acta Neuropathol. 108, 524-530. doi: 10.1007/s00401-004-0918-z
33. Price, C. J. S., Menon, D. K., Peters, A. M., Ballinger, J. R., Barber, R. W., Balan, K. K., et al. (2004). Cerebral neutrophil recruitment, histology and outcome in acute ischemic stroke: an imaging-based study. Stroke 35, 1659-1664. doi: 10.1161/01.str.0000130592.71028.92
34. Raulet, D. H. (1989). The structure, function, and molecular genetics of the gamma/delta T cell receptor. Annu. Rev. Immunol. 7, 175-207. doi: 10.1146/annurev.immunol.7.1.175
35. Ren, X., Akiyoshi, K., Vandenbark, A. A., Hurn, P. D., and Offner, H. (2011). CD4+FoxP3+ regulatory T-cells in cerebral ischemic stroke. Metab. Brain Dis. 26, 87-90. doi: 10.1007/s11011-010-9226-6
36. Roark, C. L., French, J. D., Taylor, M. A., Bendele, A. M., Born, W. K., and O'Brien, R. L. (2007). Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing γδ T cells. J. Immunol. 179, 5576-5583. doi: 10.4049/jimmunol.179.8.5576
37. Sharkey, J., and Butcher, S. P. (1994). Immunophilins mediate the neuroprotective effects of Fk506 in focal cerebral-ischemia. Nature 371, 336-339. doi: 10.1038/371336a0
38. Shen, H., Kreisel, D., and Goldstein, D. R. (2013). Processes of Sterile Inflammation. J. Immunol. 191, 2857-2863. doi: 10.4049/jimmunol.1301539
39. Shibata, K., Yamada, H., Hara, H., Kishihara, K., and Yoshikai, Y. (2007). Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178, 4466-4472. doi: 10.4049/jimmunol.178.7.4466
40. Shichita, T., Sugiyama, Y., Ooboshi, H., Sugimori, H., Nakagawa, R., Takada, I., et al. (2009). Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat. Med. 15, 946-950. doi: 10.1038/nm.1999
41. Simonian, P. L., Roark, C. L., Wehrmann, F., Lanham, A. M., Born, W. K., O'Brien, R. L., et al. (2009). IL-17A-Expressing T Cells are essential for bacterial clearance in a Murine Model of Hypersensitivity Pneumonitis. J. Immunol. 182, 6540-6549. doi: 10.4049/jimmunol.0900013
42. Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C., and Mills, K. H. G. (2009). Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity.Immunity 31, 331-341. doi: 10.1016/j.immuni.2009.08.001
43. Sutton, C. E., Mielke, L. A., and Mills, K. H. G. (2012). IL-17-producing γδ T cells and innate lymphoid cells. Eur. J. Immunol. 42, 2221-2231. doi: 10.1002/eji.201242569
44. Tang, S.-C., Lathia, J. D., Selvaraj, P. K., Jo, D.-G., Mughal, M. R., Cheng, A., et al. (2008). Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp. Neurol. 213, 114-121. doi: 10.1016/j.expneurol.2008.05.014
45. Thiel, A., and Heiss, W.-D. (2011). Imaging of microglia activation in stroke. Stroke 42, 507-512. doi: 10.1161/STROKEAHA.110.598821
46. Vantourout, P., and Hayday, A. (2013). Six-of-the-best: unique contributions of. Nat. Rev. Immunol. 13, 88-100. doi: 10.1038/nri3384
47. Yilmaz, G., Arumugam, T. V., Stokes, K. Y., and Granger, D. N. (2006). Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 113, 2105-2112. doi: 10.1161/circulationaha.105.593046
48. Yilmaz, G., and Granger, D. N. (2008). Cell adhesion molecules and ischemic stroke. Neurol. Res. 30, 783-793. doi: 10.1179/174313208X341085