The paradox role of regulatory T cells in ischemic stroke

The Scientific World Journal

Volumn 2013, Issue , 2013, Pages

  Xu, Xiaomeng ^a   Li, Min ^a   Jiang, Yongjun ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; METALLOPROTEINASE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATHEROSCLEROSIS; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL CONTACT; CELL FUNCTION; CYTOLYSIS; DENDRITIC CELL; GAP JUNCTION; HEART INFARCTION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; REGULATORY T LYMPHOCYTE; REPERFUSION INJURY; SPLEEN CELL; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; ANIMAL; CEREBROVASCULAR ACCIDENT; IMMUNOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; REVIEW; T LYMPHOCYTE;

ANIMALS; BRAIN ISCHEMIA; HUMANS; STROKE; T-LYMPHOCYTES;

EID: 84889069185     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1155/2013/174373     Document Type: Article

References (61)

1. Macrez R., Ali C., Toutirais O., Le Mauff B., Defer G., Dirnagl U., Vivien Denis D., Stroke and the immune system: from pathophysiology to new therapeutic strategies. The Lancet Neurology 2011 10 5 471 480 2-s2.0-79954579638 10.1016/S1474-4422(11)70066-7
2. Jiang Y., Wei N., Lu T., Zhu J., Xu G., Liu X., Intranasal brain-derived neurotrophic factor protects brain from ischemic insult via modulating local inflammation in rats. Neuroscience 2011 172 398 405 2-s2.0-78650748359 10.1016/j.neuroscience.2010.10.054
3. Liu X., Beyond the time window of intravenous thrombolysis: standing by or by stenting? Interventional Neurology 2012 1 1 3 15 10.1159/000338389
4. Xu G., Ma M., Liu X., Hankey G. J., Is there a stroke belt in China and why? Stroke 2013 44 7 1775 1783 10.1161/STROKEAHA.113.001238
5. Downes C. E., Crack P. J., Neural injury following stroke: are Toll-like receptors the link between the immune system and the CNS? British Journal of Pharmacology 2010 160 8 1872 1888 2-s2.0-77954884148 10.1111/j.1476-5381.2010. 00864.x
6. Jiang Y., Zhu J., Xu G., Liu X., Intranasal delivery of stem cells to the brain. Expert Opinion on Drug Delivery 2011 8 5 623 632 2-s2.0-79955122693 10.1517/17425247.2011.566267
7. Chamorro Á., Meisel A., Planas A. M., Urra X., van de Beek D., Veltkamp R., The immunology of acute stroke. Nature Reviews Neurology 2012 8 7 401 410
8. Steinman L., Elaborate interactions between the immune and nervous systems. Nature Immunology 2004 5 6 575 581 2-s2.0-2942687605 10.1038/ni1078 (Pubitemid 38811881)
9. Schabitz W. R., Regulatory T cells in ischemic stroke: helpful or hazardous? Stroke 2013 44 8 e84 10.1161/STROKEAHA.113.002228
10. Chamorro Á., Hallenbeck J., The harms and benefits of inflammatory and immune responses in vascular disease. Stroke 2006 37 2 291 293 2-s2.0-33644863548 10.1161/01.STR.0000200561.69611.f8 (Pubitemid 43731945)
11. Magnus T., Wiendl H., Kleinschnitz C., Immune mechanisms of stroke. Current Opinion in Neurology 2012 25 3 334 340 10.1097/WCO.0b013e328352ede6
12. Planas A. M., Chamorro A., Regulatory T cells protect the brain after stroke. Nature Medicine 2009 15 2 138 139 2-s2.0-59649128971 10.1038/nm0209-138
13. Gelderblom M., Leypoldt F., Steinbach K., Behrens D., Choe C.-U., Siler D. A., Arumugam T. V., Orthey E., Gerloff C., Tolosa E., Magnus T., Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009 40 5 1849 1857 2-s2.0-65549130913 10.1161/STROKEAHA.108.534503
14. Hurn P. D., Subramanian S., Parker S. M., Afentoulis M. E., Kaler L. J., Vandenbark A. A., Offner H., T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. Journal of Cerebral Blood Flow and Metabolism 2007 27 11 1798 1805 2-s2.0-35448947910 10.1038/sj.jcbfm.9600482 (Pubitemid 47624547)
15. Kleinschnitz C., Wiendl H., CON: regulatory T cells are protective in ischemic stroke. Stroke 2013 44 8 e87 e88 10.1161/STROKEAHA.113.001268
16. Sakaguchi S., Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annual Review of Immunology 2004 22 531 562 2-s2.0-2442484053 10.1146/annurev.immunol.21.120601. 141122 (Pubitemid 38680433)
17. Sakaguchi S., Yamaguchi T., Nomura T., Ono M., Regulatory T cells and immune tolerance. Cell 2008 133 5 775 787 2-s2.0-43949105866 10.1016/j.cell.2008.05.009 (Pubitemid 351707693)
18. Hori S., Nomura T., Sakaguchi S., Control of regulatory T cell development by the transcription factor Foxp3. Science 2003 299 5609 1057 1061 2-s2.0-0347785480 10.1126/science.1079490 (Pubitemid 36222930)
19. Sakaguchi S., Miyara M., Costantino C. M., Hafler D. A., FOXP3 + regulatory T cells in the human immune system. Nature Reviews Immunology 2010 10 7 490 500 2-s2.0-77954141914 10.1038/nri2785
20. Gershon R. K., Kondo K., Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970 18 5 723 737 2-s2.0-0014792798
21. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M., Immunologic self-tolerance maintained by activated T cells expressing IL- 2 receptor -chains (CD25): breakdown of a single mechanism of self- tolerance causes various autoimmune diseases. The Journal of Immunology 1995 155 3 1151 1164 2-s2.0-0029150110
22. Sakaguchi S., Wing K., Miyara M., Regulatory T cells-a brief history and perspective. European Journal of Immunology 2007 37 1 S116 S123 2-s2.0-36249024247 10.1002/eji.200737593 (Pubitemid 350131275)
23. Baecher-Allan C., Brown J. A., Freeman G. J., Hafler D. A., CD4+ CD25high regulatory cells in human peripheral blood. The Journal of Immunology 2001 167 3 1245 1253 2-s2.0-0035413350 (Pubitemid 32703119)
24. Dieckmann D., Plottner H., Berchtold S., Berger T., Schuler G., Ex vivo isolation and characterization of CD4+CD25+ T cells with regulatory properties from human blood. The Journal of Experimental Medicine 2001 193 11 1303 1310 2-s2.0-0035806244 10.1084/jem.193.11.1303 (Pubitemid 32524780)
25. Levings M. K., Sangregorio R., Roncarolo M.-G., Human CD25+CD4+ T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. The Journal of Experimental Medicine 2001 193 11 1295 1302 2-s2.0-0035806323 10.1084/jem.193.11.1295 (Pubitemid 32524779)
26. Maloy K. J., Powrie F., Regulatory T cells in the control of immune pathology. Nature Immunology 2001 2 9 816 822 2-s2.0-0035554676 10.1038/ni0901-816
27. Ng W. F., Duggan P. J., Ponchel F., Matarese G., Lombardi G., David Edwards A., Isaacs J. D., Lechler R. I., Human CD4+CD25+ cells: a naturally occurring population of regulatory T cells. Blood 2001 98 9 2736 2744 2-s2.0-0035525739 10.1182/blood.V98.9.2736
28. Thornton A. M., Shevach E. M., CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. The Journal of Experimental Medicine 1998 188 2 287 296 2-s2.0-0031821875 10.1084/jem.188.2.287 (Pubitemid 28357757)
29. Gondek D. C., Lu L.-F., Quezada S. A., Sakaguchi S., Noelle R. J., Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. The Journal of Immunology 2005 174 4 1783 1786 2-s2.0-13544271161 (Pubitemid 40223916)
30. Grossman W. J., Verbsky J. W., Tollefsen B. L., Kemper C., Atkinson J. P., Ley T. J., Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 2004 104 9 2840 2848 2-s2.0-5644238762 10.1182/blood-2004-03-0859 (Pubitemid 39434970)
31. Grossman W. J., Verbsky J. W., Barchet W., Colonna M., Atkinson J. P., Ley T. J., Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 2004 21 4 589 601 2-s2.0-5644302161 10.1016/j.immuni.2004.09.002 (Pubitemid 39370513)
32. Cao X., Cai S. F., Fehniger T. A., Song J., Collins L. I., Piwnica-Worms D. R., Ley T. J., Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 2007 27 4 635 646 2-s2.0-35449006679 10.1016/j.immuni.2007.08.014 (Pubitemid 47628832)
33. Deaglio S., Dwyer K. M., Gao W., Friedman D., Usheva A., Erat A., Chen J.-F., Enjyoji K., Linden J., Oukka M., Kuchroo V. K., Strom T. B., Robson S. C., Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. The Journal of Experimental Medicine 2007 204 6 1257 1265 2-s2.0-34250351459 10.1084/jem.20062512 (Pubitemid 46919862)
34. Borsellino G., Kleinewietfeld M., Di Mitri D., Sternjak A., Diamantini A., Giometto R., Höpner S., Centonze D., Bernardi G., Dell'Acqua M. L., Rossini P. M., Battistini L., Rötzschke O., Falk K., Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007 110 4 1225 1232 2-s2.0-34547098277 10.1182/blood-2006-12-064527 (Pubitemid 47281420)
35. Kobie J. J., Shah P. R., Yang L., Rebhahn J. A., Fowell D. J., Mosmann T. R., T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5′-adenosine monophosphate to adenosine. The Journal of Immunology 2006 177 10 6780 6786 2-s2.0-33750832563 (Pubitemid 44715042)
36. Bopp T., Becker C., Klein M., Klein-Heßling S., Palmetshofer A., Serfling E., Heib V., Becker M., Kubach J., Schmitt S., Stoll S., Schild H., Staege M. S., Stassen M., Jonuleit H., Schmitt E., Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. The Journal of Experimental Medicine 2007 204 6 1303 1310 2-s2.0-34250376423 10.1084/jem.20062129 (Pubitemid 46919868)
37. Serra P., Amrani A., Yamanouchi J., Han B., Thiessen S., Utsugi T., Verdaguer J., Santamaria P., CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity 2003 19 6 877 889 2-s2.0-0347480215 10.1016/S1074-7613(03)00327-3 (Pubitemid 37542307)
38. Tadokoro C. E., Shakhar G., Shen S., Ding Y., Lino A. C., Maraver A., Lafaille J. J., Dustin M. L., Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. The Journal of Experimental Medicine 2006 203 3 505 511 2-s2.0-33645067654 10.1084/jem.20050783
39. Fallarino F., Grohmann U., Hwang K. W., Orabona C., Vacca C., Bianchi R., Belladonna M. L., Fioretti M. C., Alegre M.-L., Puccetti P., Modulation of tryptophan catabolism by regulatory T cells. Nature Immunology 2003 4 12 1206 1212 2-s2.0-0346119234 10.1038/ni1003 (Pubitemid 37547898)
40. Vignali D. A. A., Collison L. W., Workman C. J., How regulatory T cells work. Nature Reviews Immunology 2008 8 7 523 532 2-s2.0-46249101518 10.1038/nri2343
41. Takahashi T., Kuniyasu Y., Toda M., Sakaguchi N., Itoh M., Iwata M., Shimizu J., Sakaguchi S., Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. International Immunology 1998 10 12 1969 1980 2-s2.0-0031647622 (Pubitemid 28566059)
42. Shevach E. M., From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 2006 25 2 195 201 2-s2.0-33747143361 10.1016/j.immuni.2006.08.003 (Pubitemid 44224153)
43. Wigren M., Björkbacka H., Andersson L., Ljungcrantz I., Fredrikson G. N., Persson M., Bryngelsson C., Hedblad B., Nilsson J., Low levels of circulating CD4+FoxP3+ T cells are associated with an increased risk for development of myocardial infarction but not for stroke. Arteriosclerosis Thrombosis and Vascular Biology 2012 32 8 2000 2007
44. Hansson G. K., Atherosclerosis-an immune disease. The anitschkov lecture 2007. Atherosclerosis 2009 202 1 2 10 2-s2.0-57849117801 10.1016/j. atherosclerosis.2008.08.039
45. Kassan M., Wecker A., Kadowitz P., Trebak M., Matrougui K., CD4+CD25+Foxp3 regulatory T cells and vascular dysfunction in hypertension. Journal of Hypertension 2013 31 10 1939 1943
46. Offner H., Subramanian S., Parker S. M., Wang C., Afentoulis M. E., Lewis A., Vandenbark A. A., Hurn P. D., Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. The Journal of Immunology 2006 176 11 6523 6531 2-s2.0-33646874015 (Pubitemid 43787834)
47. Urra X., Cervera Á., Villamor N., Planas A. M., Chamorro Á., Harms and benefits of lymphocyte subpopulations in patients with acute stroke. Neuroscience 2009 158 3 1174 1183 2-s2.0-59349112750 10.1016/j.neuroscience.2008.06.014
48. Yan J., Read S. J., Henderson R. D., Hull R., O'Sullivan J. D., McCombe P. A., Greer J. M., Frequency and function of regulatory T cells after ischaemic stroke in humans. Journal of Neuroimmunology 2012 243 1-2 89 94 2-s2.0-84856955229 10.1016/j.jneuroim.2011.12.019
49. Seifert H. A., Hall A. A., Chapman C. B., Collier L. A., Willing A. E., Pennypacker K. R., A transient decrease in spleen size following stroke corresponds to splenocyte release into systemic circulation. Journal of Neuroimmune Pharmacology 2012 7 4 1017 1024
50. Kleinschnitz C., Kraft P., Dreykluft A., Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature. Blood 2013 121 4 679 691 10.1182/blood-2012-04-426734
51. Li P., Gan Y., Sun B. L., Zhang F., Lu B., Gao Y., Liang W., Thomson A. W., Chen J., Hu X., Adoptive regulatory T-cell therapy protects against cerebral ischemia. Annals of Neurology 2012 10. 1002/ana. 23815
52. Stubbe T., Ebner F., Richter D., Engel O., Klehmet J., Royl G., Meisel A., Nitsch R., Meisel C., Brandt C., Regulatory T cells accumulate and proliferate in the ischemic hemisphere for up to 30 days after MCAO. Journal of Cerebral Blood Flow and Metabolism 2013 33 1 37 47
53. Hu X., Li P., Chen J., PRO: regulatory T cells are protective in ischemic stroke. Stroke 2013 44 8 e85 e86
54. Ait-Oufella H., Salomon B. L., Potteaux S., Robertson A.-K. L., Gourdy P., Zoll J., Merval R., Esposito B., Cohen J. L., Fisson S., Flavell R. A., Hansson G. K., Klatzmann D., Tedgui A., Mallat Z., Natural regulatory T cells control the development of atherosclerosis in mice. Nature Medicine 2006 12 2 178 180 2-s2.0-32244445416 10.1038/nm1343 (Pubitemid 43214743)
55. Liesz A., Suri-Payer E., Veltkamp C., Doerr H., Sommer C., Rivest S., Giese T., Veltkamp R., Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nature Medicine 2009 15 2 192 199 2-s2.0-59649123881 10.1038/nm.1927
56. Matsumoto K., Ogawa M., Suzuki J.-I., Hirata Y., Nagai R., Isobe M., Regulatory T lymphocytes attenuate myocardial infarction-induced ventricular remodeling in mice. International Heart Journal 2011 52 6 382 387 2-s2.0-84255169303 10.1536/ihj.52.382
57. Lu L., Li G., Rao J., Pu L., Yu Y., Wang X., Zhang F., In vitro induced CD4+CD25+Foxp3+ Tregs attenuate hepatic ischemia-reperfusion injury. International Immunopharmacology 2009 9 5 549 552 2-s2.0-63549097293 10.1016/j.intimp.2009.01.020
58. Ferenbach D. A., Kluth D. C., Hughes J., Regulatory T cells: a brake on ischemic injury or an active promoter of tissue healing. Kidney International 2009 76 7 689 691 2-s2.0-70349212418 10.1038/ki.2009.302
59. Iadecola C., Anrather J., The immunology of stroke: from mechanisms to translation. Nature Medicine 2011 17 7 796 808 2-s2.0-79960141471 10.1038/nm.2399
60. Ren X., Akiyoshi K., Vandenbark A. A., Hurn P. D., Offner H., CD4+FoxP3+ regulatory T-cells in cerebral ischemic stroke. Metabolic Brain Disease 2011 26 1 87 90 2-s2.0-79955083477 10.1007/s11011-010-9226-6
61. Gu L., Xiong X., Zhang H., Xu B., Steinberg G. K., Zhao H., Distinctive effects of T cell subsets in neuronal injury induced by cocultured splenocytes in vitro and by in vivo stroke in mice. Stroke 2012 43 7 1941 1946